berry and bjorkman 1980. photosynthetic response and adaptation

Ann. Rev. Plant Physiol 198a 31:491-543 Copyright © /98() by Annual Reviews Inc. All rights reserved

PHOTOSYNTHETIC RESPONSE AND ADAPTATION TO TEMPERATURE IN HIGHER PLANTS

Joseph Berry and Olle Bjorkman 1

Department of Plant Biology, Carnegie Institution of Washington, Stanford, California 94305

CONTENTS

.7699

INTRODUCTION ........................................................................................................ 492 ECOLOGICAL ASPECTS OF PHOTOSYNTHETIC TEMPERATURE

ADAPTATION ............................................................................................ 493 Photosynthetic Temperature Dependence in Thermally Contrasting Climates ........ 493 Photosynthetic Temperature Acclimation .................................................................. 497

Seasonal acclimation in natural habitats ......................... ........... ...... ................... ....... 497 Studies in controlled environments ............................................................................ 499

THE MECHANISTIC BASIS FOR PHOTOSYNTHETIC RESPONSE AND ADAPTATION TO TEMPERATURE .................................................... 504

Reversible Temperature Respon.ses ............................................................................ 505 Stomata! effec� o� the

. temJH!.rature response 0/ photo.rynthesis ......... .................... ....... 505

Interacttons with /lght mtenslty ................................................................................ 507 C, photo.rynthesis (lM photorespiration ............ ..................... ........... .......................... 507 C, photo.rynthesis ........................... ..................................... .................................... 515 Comparison 0/ plants from contrasting thermol regimes ........................ ...... ...... .......... 517

["eversible Temperature Respon.ses .......................................................................... 519 Low temperature sensitMty ....... ............................................................................... 519 High temperature sensitivity ...................................................................................... 524 Adoptive responses in the heat stability 0/ the photosynthetic apparatus .......................... 530

CONCLUDING REMARKS ...................................................................................... 532

IC.I.W.-C.P.B. Publication No. 673.

491 0066-4294/80/0601-0491$01.00

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492 BERRY & BJORKMAN

INTRODUCTION

Temperature is prominent among the major tcological variables that determine the natural distribution of plants. Habitats occupied by higher plants show dramatic differences in the prevailing temperature during the period of active growth, ranging from near freezing in certain arctic and alpine environments to over 50°C in the hottest deserts. Moreover, in many habitats the same plant individual is subjected to a very wide seasonal variation in temperature regime and even diurnal temperature fluctuation can be considerable.

Like almost all other growth processe:., photosynthesis is strongly affected by temperature. In most plants, chllnges in photosynthetic rate in response to temperature are reversible over a considerable range (commonly 10° to 35°C), but exposure to temperatures l:>elow or above this range may cause irreversible injury to the photosynthetic system. Thus, in addition to the effect of temperature on photosynthesis arising from the intrinsic temperature dependence of the process in the mnge over which the functional integrity of the photosynthetic apparatus remains intact, extreme temperatures can drastically inhibit photosynthesis by disrupting the integrity of the system.

Higher plants from thermally contrasting habitats show considerable differences in their photosynthetic respons�: to temperature, and especially in their ability to maintain functional integrity at low and high temperature extremes. Such adaptations may be considE!red as a genotypic variation in key constituents of the photosynthetic appa.ratus, enabling plants to function efficiently under the temperature regimes of their various native habitats. In addition, certain plants possess considerable phenotypic plasticity in their photosynthetic characteristics. Growth of a given genotype under a cool regime results in an improved photosynthetic capacity at low temperature whereas growth under a warm regime results in an imprOVed photosynthetic performance at high temperatures. The potential for such photosynthetic acclimation to growth temp�rature is quite variable between species.

The purpose of this review is to discuss n:cent advances in our knowledge of the effect of temperature on the photosynthetic process as it occurs in higher plant leaves, to evaluate the extent of photosynthetic temperature adaptation in higher plants, and to consiCler the underlying physiological and biochemical mechanisms. Our treatment is limited to levels of organizational complexity ranging from single leaft<> isolated chloroplasts or chloroplast constituents. The relaxation times of the responses under consideration will vary from less than a second to several months. Consideration of other important aspects such as the heat exchange between plant

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TEMPERATURE RESPONSE OF PHOTOSYNTHESIS 493

canopies and the environment, the effect of temperature on photosynthate partitioning, and on whole plant productivity, as well as freezing injury, and the interactions between the effects temperature and water stress on whole plant photosynthesis are outside the scope of this review.

ECOLOGICAL ASPECTS OF PHOTOSYNTHETIC TEMPERATURE ADAPTATION

There are numerous reports in the literature on the temperature response of net CO2 exchange determined on a variety of species in a diversity of natural and variously modified environments. Our review of this largely descriptive research is not exhaustive and with some exceptions covers only the past 10 years. Pisek (158) has provided an extensive treatment of most of the earlier work in this field. Osmond, Bjorkman & Anderson (147) have provided a treatment of photosynthetic response to environmental factors in the context of plant physiological ecology.

Unfortunately, attempts to compare the results obtained by different investigators on different species and in different environments suffer from the problems that the temperature dependence of photosynthesis, even for a single leaf, is strongly influenced by other environmental factors. As discussed in detail in a later section, light intensity and intercellular CO2 pressure have especially pronounced effects. The temperature dependence of photosynthesis becomes increasingly pronounced in the case that either light or intercellular CO2 level is increased. Because of its influence on intercellular CO2 pressure, stomatal conductance greatly affects the temperature response of photosynthesis. Only rarely is there sufficient information to permit an assessment of the effect of these interacting factors in comparisons of the temperature-related characteristics of photosynthesis among species, especially in natural situations. Such comparisons are further complicated by the fact that these characteristics are also influenced by the previous history of the plant. Not only does the growth temperature affect the temperature response of photosynthesis, but also leaf age and the light, water, and nutrient regimes to which the plant has been subjected have a marked influence, either by directly affecting the intrinsic photosynthetic properties or indirectly by affecting stomatal conductance.

Photosynthetic Temperature Dependence in Thermally Contrasting Climates In spite of the complications mentioned above, it is nevertheless clear that plants occupying thermally contrasting habitats generally exhibit photosynthetic temperature responses that reflect an adaptation to the temperature regimes of their respective habitats. Plants which are native to and grown

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in cool environments generally exhibit high(:r photosynthetic rates at low temperatures, and optimum photosynthetic rates occur at lower temperatures in comparison with plants which are native to and grown in warm environments. Conversely, the latter plants exhibit a superior photosynthetic performance at high temperatures, in large part as a result of an increased heat stability of the photosyntheti.c apparatus.

The two types of responses are illustrated in Figure I (38), which compares the temperature dependence of photosynthesis of Atrip/ex g/abriuscu/a, native to and grown in a cool coastal environment, with that of Tidestromia ob/ongifolia, a summer-active, winter-dormant species native to and grown in the extremely hot desert of Death Valley, California (40). Photosynthesis measurements were made under similar conditions of high light and normal atmospheric CO2 and O2 levels, and simultaneous determinations of stomatal conductance showed that stomatal factors were in no part responsible for the differences in photosynthetic temperature depen-

'u I» 4 Tidestromio oblongifolio, C4 1/1

N Hot desert Ie u I» (; e 3 0 c 0 c: I» � 0 2 ..... 0-:l N

0 U '-0 I» -0 a::

°10 Leaf temperclture. °c

Figure J Comparison of the temperature dependences of photosynthesis by whole plants of Tidestromia ob/ongijOlia during the summer in Death Valley, California, and Atriplex glabriuscu/a, grown under a temperature regime simulatinll that of its native coastal habitat. From

(38).

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dence between the two species. The cool coastal species has high photosynthetic rates in the 10° to 20°C range, very much superior to those of the hot desert species. By contrast, the desert species is greatly superior at high temperatures. It continues to increase its photosynthetic rate as temperature is increased over a wide range, and the temperature optimum does not occur until 46°C. This temperature causes irreversible inhibition of photosynthetic activity in the coastal species.

Comparison with field studies on a number of other unrelated species occupying cool coastal environments (H. A. Mooney, unpublished) indicates that the photosynthetic temperature dependence of A. glabriuscula, shown in Figure 1, provides a good representation for such plants. Species possessing the C4 dicarboxylic acid pathway of CO2 fixation (C4 species) tend to exhibit higher optimum temperatures for photosynthesis at normal air levels of CO2 than do species lacking this pathway (C3 species). The underlying reasons for this difference are discussed later. In accordance with this generalization, the cold-adapted C4 plant Atriplex sabulosa is capable of high photosynthetic rates at higher temperatures than A. glabriuscula (C3), with which it frequently coexists in cool strand habitats both in northern Europe and northeastern North America. Nevertheless, the photosynthetic capacity at low temperatures of these two C3 and C4 species are similarly high, and neither species possess a high heat tolerance (38; cf Figure 2).

Comparisons of a number of investigations on a wide diversity of higher plant species from cool-temperature environments, conducted either in the native sites or on plants grown under a cool temperature regime simulating the native habitat (e.g. 1,23,38,39,72,89, 140, 187-191, 196,217), indicate that the temperature response curves for photosynthesis are rather similar in shape, generally resembling that shown in Figure I for A. glabriuscula, although there is a tendency for a shift in the position of the optimum temperature in concert with the habitat or growth temperature, and the maximum photosynthetic rate may exhibit large differences among species. Similar temperature-dependence curves have also been found in desert winter annuals and in C3 evergreen desert perennials during the cool season or when grown under a cool temperature regime (30, 54, 111, 128, 130, 131).

Not even cold-adapted plants such as Oxyria digyna from extreme environments such as arctic Ellesmere Island at 82° north latitude or alpine San Francisco Peak in Arizona at 3414 m altitude reach their optimum temperature for photosynthesis unti115° to 200e and their temperature response curves are broad, permitting rates to remain at L 75% of the maximum over a range extending from 10° to 30°C (23). Field studies on several mosses growing in the oceanic-arctic habitat of Barrow, Alaska (71° north

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N 'E

u (5 E c r; -+-o l-t/)

'iii m

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A. sabulosa

I I Hot,O' _0_ '0,

,Cf I J:J� I \

p" I 0" I 0

N. oleander

I I

I T. oblongifolia tp,o..q I I

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I I Cool I I--' ........ �"""

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I O �--�--��--�--��--�--�-- -��--�---L--�--�

10 20 30 40 50 10 20 30 40 50 10 20 30 40 5(

Leaf temper<lture, °C

Figu,.e 2 Effect of growth temperature regime on the rate and temperature dependence of light-saturated photosynthesis in normal air for a number of species native to habitats with contrasting thermal regimes. The vertical broken lines indicate the daytime temperatures of the "cool" and "hot" growth regimes for each species, Based on data of (30, 38, 130, 149).

latitude) indicate that the optimum temperatures for photosynthesis are somewhat lower than those obtained with higher plants (143, 145). Also, these mosses exhibited relatively flat temperature-response curves so that the photosynthetic rates in the range from 5° to 200e were at least 80% of the optimum rate.

The decidedly thennophilic photosynthetic characteristics exhibited by the hot desert C4 species T. oblongifolia (Figure 1) probably represent the

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opposite extreme among vascular plants. No other higher plant examined so far matches this species in terms of temperature optimum or photosynthetic rate at temperatures in excess of 40°C, although numerous other C4 species from hot climates possess photosynthetic characteristics that approach those of T. oblongifolia. Examples of such species are found not only among other members of the Amaranthaceae, such as Amaranthus edulis (64), but also among unrelated taxa such as Atriplex lentiformis (149, 152), Hammada scoparia (111). and many tropical-origin C4 grasses (63, 119). C3 plants growing in hot-arid or semiarid environments also have relatively high optimum temperatures, e.g. Larrea divaricata during the summer in Death Valley, California (130), and several C3 shrubs from Western Australia (85). Similar results have also been obtained on warmclimate C3 plants grown under controlled high temperature regimes, e.g. Heliotropum curassivicum (128), La"ea divaricata (130) and Nerium oleander (30). Such heat-adapted C3 plants may be as tolerant of heat damage to the photosynthetic apparatus as are heat-adapted C4 plants, and in the presence of high CO2 pressure the photosynthetic performance of heat-adapted C3 plants such as Larrea divaricata at high temperatures can equal that of extreme C4 thermophiles such as Tidestromia oblongifolia. However, at normal air levels of CO2 the high-temperature performance of the C4 species is decidedly superior.

Photosynthetic Temperature Acclimation The temperature dependence of photosynthesis for a given plant as observed in its natural habitat is the result of a complex interaction between the prevailing environment and the characteristics inherent in the species or genotype. Numerous investigations have been undertaken to determine the relative importance of genotypic and environmental factors in photosynthetic temperature adaptation. For this review we shall use the expression "photosynthetic acclimation" to denote environmentally induced changes in photosynthetic characteristics that result in an imprOVed performance under the new growth regime. The genetically determined ability to so acclimate will be termed "acclimation potential."

SEASONAL ACCLIMATION IN NATURAL HABITATS Investigations of photosynthetic acclimation to seasonal temperature variation in nature are few but nevertheless include a wide diversity of life forms and habitat types, ranging from mosses in the arctic tundra to trees at the timberline in high mountains and to C3 and C4 shrubs in hot deserts. Oechel (143), working on three moss species at Barrow, Alaska, found that the optimum temperature for photosynthesis shifted from 12° - DOC early in the season to 19° - 21°C during the warmest period of the year, corresponding to about 1°C

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shift for each 2°C difference in growth temperature. There was little seasonal change in the maximum photosynthetic rate. In spite of the seasonal shift in the temperature dependence of photosynthesis, the optimum temperature was considerably higher than the prevailing tissue temperature for most of the time. As an explanation for tais observation, Oechel (143) advanced the hypothesis that "C3 plants ha�e not evolved to the full range of thermal regimes in which they are found." While this statement may well be true in many cases, especially in relation to hot arid habitats, maximum photosynthetic effectiveness is not necessarily obtained at the temperature optimum but rather below it.

In a study on Eucalyptus pauciflora alonJ� an altitudinal gradient in the Snowy Mountains of southeastern Australia, Slatyer & Morrow (191) found that the maximum photosynthetic rate and the optimum temperature declined with increasing site elevation and at any one site increased from spring to summer and declined in the autunm. At the highest elevation the optimum temperature occurred at 7.SoC in early spring, increased to 17.SoC in midsummer, and declined to 7°C in the late autumn. Corresponding values for the lowest elevation were 13°, 24c" and 12.5°C. At each site there was a close correlation between the optimum temperature for photosynthesis and the mean maximum temperature (If the 10 days prior to the date of measurement. As discussed later, subHequent experiments on plants grown under controlled conditions showed that photosynthetic acclimation is a predominant cause of the altitudinal shift in optimum temperature, although ecotypic differences among the populations are also important (187, 189).

Seasonal changes in the temperature dependence have also been reported for other trees such as Sitka spruce in Scotland (140) and Pinus taeda in southeastern United States (201). In both cases the temperature optimum was considerably higher in the summer than in the winter, an observation which appears to be in general agreement with the trend found in early work on forest trees (158).

DePuit & Caldwell (54) found that the optimum temperature for the C3 shrub Artemisa tridentata growing in file cold desert in Utah was lower in early spring than later in the season. However, in the mid and late summer, other factors, especially water stress, became the main determinants of photosynthetic performance, largely overriding the temperature responses. Lange et al (111), working with the C4 shrub Hammada scoparia in the warm Negev desert, Israel, found that the optimum temperature for light-saturated photosynthesis gradually changed from a minimum of 29°C at the beginning of the growing season in early spring to a maximum of 41°C in the hottest summer months and then gradually declined to 28°C in the autumn. Similar trends were also observed in apricot (Prunus armeniaca) cultivated in the Negev desert, but the optimum temperatures

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were lower in this C3 plant. The seasonal shifts in temperature optima occurred both in irrigated plants and in plants growing under natural water stress conditions, and cannot be explained by changes in stomatal responses.

The same conclusions apply to results obtained with the evergreen desert shrub Larrea divaricata in Death Valley, California (130). The optimum temperature varied from about 20°C in January to 28°C in May and 34°C in September, while the maximum rate of photosynthesis showed little seasonal change (cf Figure 2). The shift in temperature optimum provides only partial compensation for the seasonal change in prevailing leaf temperature in this C3 plant; photosynthesis operated near the optimum during the cooler seasons but well above the optimum during the warmest months in this extremely hot desert. However, another perhaps even more important consideration is that acclimation to high temperature in this and other desert species greatly raises the threshold temperature at which heat damage to the photosynthetic apparatus occurs. It is clear from these field studies that acclimation of temperature-related photosynthetic characteristics to seasonal changes in prevailing temperature is a common phenomenon among plants occupying habitats where such changes are dramatic.

STUDIES IN CONTROLLED ENVIRONMENTS Although investigations on photosynthetic acclimation in natural environments are quite limited, numerous such studies have been conducted under controlled conditions. In addition to extending greatly the data base obtained in field investigations, these studies provide important information on the differences and similarities in the potential for photosynthetic acclimation that exists among different species and different populations of the same species.

Acclimation potential of different species Figure 2 illustrates the effect of growth temperature on the temperature dependence of photosynthesis in species representing three different types. In all cases, high growth temperature causes an upward shift in the optimum temperature for light-saturated photosynthesis. However, in the coastal species A. glabriuscula (C3) and A. sabulosa (C4), growth at high temperature results in a depression of the photosynthetic rate at all measurement temperatures. Thus, the positive changes in the temperature dependence of photosynthesis in relative terms are accompanied by pronounced counteracting changes in photosynthetic capacity in absolute terms, resulting in an inferior rather than superior overall performance. Such responses therefore indicate that the plant lacks the ability to acclimate to high temperature, and actually suffers damage to the photosynthetic apparatus (21, 27, 28, 33, 130). Responses similar to those of A. glabriuscula and A. sabulosa have been found also in other plants whose natural distribution is limited to cool-temperature environments (e.g. 149, 219) and may indeed be typical of such plants.

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The response of the summer-active hClt-desert species Tidestromia oblongfolia (also shown in Figure 2) is in sharp contrast to those of the two coastal species. When grown under a hot regime this thermophilic C4 plant is capable of extremely high photosynthetic I ates at high temperatures, but the rates at low temperatures are very poor. However, lowering the growth temperature to below 20°C does not result in an improved performance at low temperatures, but causes a drastic redu(:tion in photosynthetic rate of all measurement temperatures. Similar but leiS extreme responses have been found in other warm-climate species such as the C4 grass Bouleloua gracilis (219).

Although the response of T. oblongifo/ia is the opposite of that found in the coastal species, both kinds of plants are similar in possessing a limited potential range for photosynthetic temperature acclimation. A considerably greater acclimation potential is found among evergreen desert shrubs that are subjected to large seasonal temperature: variation. The lower part of Figure 2 shows examples of three such species. Of these, C4 Atrip/ex /entiformis and C3 Larrea divaricata are both native to Death Valley; Nerium oleander orginates from the deserts of S,)uthwest Asia and Northeast Mrica. All three species remain photosynthetically active throughout the year in Death Valley (30, 130, 148). The dependence of light-saturated photosynthesis shifted with the growth temperature regime in a manner similar to the seasonal shifts observed in the field (30). The plants have higher photosynthetic rates at low measurement temperatures when grown under a cool regime and higher rates at hlgh measurement temperatures when grown under a hot regime. The rates at the respective optimum temperatures were similar, irrespective of growth temperature.

As discussed later, acclimation to low temperature may be considered to involve an increase in the capacity of tempc:rature-limited enzymic steps of the photosynthetic process whereas acclimation to high temperature involves an increased heat stability of the photosynthetic apparatus. Changes in either of these two factors may result in ,il shift in the optimum temperature. The position of this optimum is also affected by the point at which largely temperature-independent reactions (such as diffusive transport of CO2 into the leaf) become limiting and th(: rate of counteracting reactions (such as photorespiratory CO2 release) increases to a greater extent than the activity of reactions that promote photos)nthetic activity.

It follows that an improvement in photmynthetic effectiveness at a given low temperature, e.g. 5°C, requires that the photosynthetic rate at that temperature be increased. This increase, presumably brought about by an increase in the amount of rate-limiting enzymes, will tend to cause a downward shift of the temperature optimum toward, but not necessarily to, SoC. Depression of the temperature optimum all the way to SoC by raising the

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rate to the ceiling imposed by temperature-independent reactions and by counteracting reactions is likely to require an inordinately large investment in rate-limiting enzymes with only a marginal photosynthetic gain. Lowering of the ceiling could of course also result in a downward shift in the temperature optimum all the way to SoC, but this shift would be counterproductive since the photosynthetic rate would not increase but would fall.

This reasoning may provide an explanation for the common observation that in cold environments the optimum temperature for photosynthesis tends to be higher than the prevailing leaf temperature. Caution is clearly advisable in basing interpretations of photosynthetic adaptation on optimum temperatures alone, but the relative position of this optimum is nevertheless a useful indicator.

Acclimation potential of mature leaves Ability to acclimate to an altered growth temperature need not be limited to newly developing leaves. Slatyer & Ferrar (190) followed the time course of changes in photosynthetic characteristics of the same Eucalyptus pauciflora leaves after transfer of field-grown plants to controlled conditions. They found that, given sufficient time, both the optimum temperature and the maximum photosynthetic rate changed to the same values as those exhibited by control plants continuously kept under the controlled growth regime. Depending on the original site from which the plants were taken, full acclimation to the new growth regime required at least one week and in some cases more than two weeks. The acclimation involved changes both in stomatal conductance and intrinsic photosynthetic characteristics. Stomatal conductance appeared to change over a narrower range, with most of the change occurring early in the period, and nonstomatal factors appeared to change over a wider range and later in the period following transfer of the plants.

In Nerium oleander, which normally retains any one leaf for at least one year, even fully expanded mature leaves are capable of a complete reversal of their photosynthetic temperature-response characteristics after transfer of plants from a 200e to a 45°e growth temperature regime, and the reciprocal (29). As discussed in a later section, N oleander leaves grown at 20°C have more than twofold higher photosynthetic capacity at 200e and a considerably higher level of certain enzymes of photosynthetic carbon metabolism than do leaves grown at 4SoC. Mter transfer of 4S0C-grown

-plants to 20oe, the photosynthetic capacity and the enzyme levels of fully mature leaves gradually increased and after 10-12 days were indistinguishable from those of leaves that had developed and were continuously maintained at 20°C. Conversely, mature leaves from plants grown at 45°C have a considerably higher optimum temperature, a much higher heat stability of certain components of the photosynthetic apparatus, and distinctly al-

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S02 BERRY & BJORKMAN

tered properties of the chloroplast membrane lipids in comparison with material grown at 20°C (29, 30, 164). Upon transfer of 20°C-grown plants to 45°C the optimum gradually shifted upward, and the photosynthetic capacity and the enzyme level both decliu.::d, whereas the heat stability increased and the properties of the chloroplast lipids changed toward those of the control grown at 4SoC. The acclimation was essentially complete in about one week after transfer. Since seasonal changes in prevailing temperature in nature are much more gradual than those imposed in these experiments, it seems probable that leaves develop::d during one season should be capable of continuous acclimation, enabling the photosynthetic characteristics to remain in tune with the environment during all seasons.

Although few other studies of the time course of photosynthetic temperature acclimation of the same leaves have oom made, the available evidence suggests that such acclimation may occur in a variety of plants (88, 132, 172, 177, 196, 200) and that it requires at least several days and often a week or longer, although substantial changes mny occur in the first day or two after transfer. However, as mentioned earlier, a large part of the rapid initial increases in photosynthetic rate and upward shift of the optimum temperature often observed shortly after transfer from a cool growth regime to warmer conditions may simply reflect an increase in stomatal conductance rather than acclimatory changes in intrinsk photosynthetic characteristics.

Acclimation potential 0/ populations withil! the same species Species that occur in a wide diversity of habitats are often composed of ecological races or ecotypes, each of which is genotypical1y adapted to its particular habitat. A surprising number of investigation:. have been directed toward determining the possible role of ecotypic differentiation in photosynthetic temperature adaptation. Differences in the temperature dependence of photosynthesis among populations native to thermally dissimilar habitats but grown in a common environment have been reported for a number of widely distributed herbaceous perennials ai. well as deciduous and evergreen woody perennials. The extensive studies by Billings and his coworkers (23, 129) show that arctic populations of Ox),ria digyna have lower optimum temperatures for photosynthesis than do alpine populations when grown in the same environment. Similar differences have also been reported for other herbaceous perennials such as Solidago virgaurea popUlations from arctic versus temperate regions of Scandinavia (34) and for a series of Ledum groenlandicum populations (196). In all of these species and populations there was also a pronounced influence of growth temperature on the temperature dependence of photosynthesis. The mean shift in optimum temperature for a range of arctic and alpine Oxyria populations was about 1°C for each 3°C change in growth temperature, and similar values are apparent

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for the Ledum populations. In Oxyria, growth under a cold regime also resulted in higher photosynthetic rates at low temperatures. Gro�th under a warm regime decreased the maximum photosynthetic rates in all arctic but only in a few of the alpine· populations.

Several studies have compared the responses of populations growing along altitudinal gradients. As mentioned earlier, field studies showed that the optimum temperature for photosynthesis of Eucalyptus paucijlora declined with increasing site elevation (19 1). When plants were collected from the different field sites and grown under a series of controlled temperature regimes, it was found that in each population the optimum temperature shifted in the direction of the growth temperature by about 1°C for every 3°e shift in growth temperature (1 89). However, there was also a distinct genotypic effect. When the plants were grown at day temperatures of 15°e and 33°e, the optimum temperatures for photosynthesis in the high elevation plants were 20°C and 25°C. respectively, whereas the corresponding optima in the low elevation material were 25° and 30°C. Moreover, the low elevation plants have a limited potential in acclimating to a much lower growth temperature, whereas the high elevation plants have a limited ability to acclimate to high temperatures.

Other work involving altitudinal gradients include the studies of Pisek et al (159), who found that the optimum temperature for net photosynthesis in Picea excelsa from 1900 m in the Austrian alps was about 3°C lower than in those from 900 m, corresponding to a shift in optimum temperature of about 1°C for every 5°C shift in prevailing growth temperature. At the other extreme are the results of Fryer & Ledig (72) with Abies balsamea, collected from a range of elevations in the mountains of New Hampshire and grown under a common growth regime. These workers found a close agreement between the optimum temperature of photosynthesis and the mean maximum temperature of the site elevations and little acclimation to the growth temperature regime used in their experiments.

An especially striking difference in photosynthetic acclimation potential between different populations of the same species is found in Pearcy's investigations on the C4 shrub Atriplex lentiformis ( 148, 149). This species inhabits both the hot interior low deserts and mild coastal areas of California. As shown in Figure 2, desert clones of this species are capable of acclimating over a wide range of growth temperatures. Growth at a 43°e day/30°C night regime resulted in a photosynthetic performance at high temperatures, clearly superior to that obtained when the same clone was grown at a 23°e day/18°C night regime. The photosynthetic performances of the desert and the coastal clones were remarkably similar when they had been grown under the cooler regime. HoweVer, in contrast to the response of the desert clones, growth of the coastal clones under the hot regime

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resulted in a severe reduction in photosynthetic capacity at all measurement temperatures (data not shown in Figure 2). This result suggests that the coastal populations of A. lentiformis during the course of microevolution have either lost, or (perhaps less likely) failed to acquire, the high photosynthetic acclimation potential found in the desert populations.

Unlike A. lenti/ormis, the widely distributed C3 perennial Heliotropum carassivicum does not appear to have evolved ecotypic differences in photosynthetic characteristics (128). Clones froIl populations of this species, collected from sites on the cool coast of Northern California, exhibited a potential for photosynthetic acclimation to tcigh temperatures equal to that found in desert clones collected from the Boor of Death Valley. The photosynthetic characteristics of coastal and desert clones were almost alike when the clones were in the same conditions, and both of the coastal and desert clones exhibited an unusually high pheno';ypic plasticity. The optimum temperature for photosynthesis shifted by as much as 2°C for every 3°C change in growth temperature over a range extending from 25°C to 40°C, while the photosynthetic rate determined at the respective optimum temperatures was little affected.

Conclusions In general. the results of studies on both interspecific and intraspecific differentiation indicate that plants restricted in distribution to cool environments tend to have a relatively low "preferred" temperature and a limited potential for acclimation to high temperatures. whereas plants from prevailing warm environments (especially C4 species) have a relatively high "preferred" temperature and a limited ability to acclimate to cool temperatures. It is also apparent that plants from habitats with large temperature variations during the growing s<:ason tend to possess a greater potential for acclimation over a wide temperature range than do plants from habitats with relatively stable temperatw'es during the period of active growth. Species with distributions in bott!. cool and warm habitats may either be composed of ecotypes, each havill.g different "preferred" temperatures and limited acclimation potentials, or in some cases, such as Helitropum curassivicum, they may possess a high potential for photosynthetic acclimation over a wide temperature range similar to the response of species that occupy habitats with large seasonal ·temperature variation.

THE MECHANISTIC BASIS FOR PHOTOSYNTHETIC RESPONSE AND ADAPTATION TO TEMPERATURE

The temperature response profiles for phctosynthesis of intact leaves is the integrated result of specific effects of temperature on the component biochemical and biophysical reactions of thl: photosynthetic process. Even if

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the temperature dependence of all of these component reactions were known, it would be a formidable task to integrate them over such widely different levels of organization so that the ultimate temperature response of the system could be predicted. For now we must be content with a deductive analysis of the response of the whole system, coupled where possible with mechanistic investigations of the component reactions. This approach makes it possible to examine the relationships between the responses at different levels of organization, and comparative studies of plant material with contrasting thermal responses provide the additional opportunity to examine differences in integrated response to differences in mechanism and help to separate those mechanistic differences that are causally related to a response difference from those that are merely different. Examples of such approaches are given below. The first sections deal with the basis of the temperature reponses of photosynthesis over the normal physiological range of tolerance within which these responses are reversible. The following sections deal with factors that determine the high and the low temperature limits of tolerance. Exposure to temperatures exceeding these limits tends to have irreversible effects on the photosynthetic apparatus.

Reversible Temperature Responses

STOMATAL EFFEcrS ON THE TEMPERATURE RESPONSE OF PHOTO

SYNTHESIS Stomata control the resistance to the diffusive transfer of water vapor and CO2 between the leaf and the ambient air and hence affect the CO2 concentration in the intercellular spaces of photosynthesizing leaves. In normal air the photosynthetic rate is dependent on the concentration of CO2 in the leaf intercellular spaces, especially in C3 plants. This CO2 dependence can be relatively small at low temperatures but becomes increasingly pronounced as the temperature is increased (see below). Hence stomata may exert a strong influence both on the rate and on the temperature dependence of photosynthesis. The CO2 concentration gradient developing between the ambient and the intercellular air is equal to the product of the net CO2 flux rate and the stomatal resistance to CO2 diffusion. Both can be determined experimentally as can the dependence of photosynthesis on intercellular CO2 concentration, and if all of these parameters are known, it is possible to predict the effect of stomatal conductance (i.e. the inverse of resistance) on the temperature dependence of photosynthesis.

Stomata respond to a number of major environmental factors such as temperature, light, humidity, and CO2 concentration. Feedback control via photosynthesis may also occur and internal water status may have profound effects (for reviews see 52, 77, 169, 183). There are a number of reports on the response of stomata to temperature. Some indicate that stomata tend

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to open with increasing temperature (e.g. 53, :;8, 59, 91); others indicate that they close at higher temperature (e.g. 56, 83. 84, 171, 222). There are also many reports that stomata open maximally at intermediate temperatures (e.g. 91, 117, 118, 139, 168, 182, 218). It i:; now widely recognized that stomatal response to temperature is stronglylnfiuenced by other interacting factors of which the internal plant water statt,S and the water vapor pressure difference between the leaf and the surrounding air are particularly important.

It appears that the interactions between th,� effects of temperature and the water vapor pressure difference in large part account for the contradictory reports on stomatal response to temperature. In many instances in which stomata tended to close with increasing terr..perature, the closure probably resulted from a stomatal response to an ircreased vapor pressure deficit which normally results when the leaf tempeJature is increased (76, 77, 117, 118). For example, when temperature was increased and the vapor pressure of the air held constant, the stomata of Sesamum indicum and Citrus sinensis tended to close, but when the water vapor pressure of the air was so adjusted that the vapor pressure diff(:rence remained constant, the stomata continued to open with increasing temperature (75, 77).

Somewhat similar interactions have alHo been observed between the effects of plant water status and temperature: on stomatal conductance (l18, 179, 180,213). In well-watered plants stomata tend to continue to open, or at least to remain open, as the temperature is increased over a wide range. In water-stressed plants there is tendency f(lr reduction in stomatal conductance above a certain temperature. The effects of atmospheric humidity and internal plant water status on the stomatal response to temperature appear to be largely independent and additive.

Thus in the absence of water stress and high water vapor pressure gradients, stomata tend to respond to temperature in concert with the changing photosynthetic demand for CO2, In any event, it is clear from a number of studies where measurements cf stomatal conductance accompanied the determinations of the temperature response of photosynthesis (15,29,30,38, 111, 130, 140, 149, 187, 190) that the observed differences in photosynthetic characteristics between contrasting species or between plants grown under different temperature regimes (e.g. those shown in Figures 1 and 2) cannot be explained by stomatal responses. It is also evident that the sharp decline in photosynthesis that takes place at very high temperatures is not caused by stomatal closure (16, 168). Indeed, stomatal conductance remains high or even increases when leaves are heated to temperatures that cause damage to the photosynthetic apparatus (16, 38, 168), and stomata may open in the dark wilen leaves are heated to temperatures above 35°C to 40°C (46, 123, 154).

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INTERACTIONS WITH LIGHT INTENSITY The photosynthetic temperature response of whole leaves is also quite sensitive to the light intensity. As shown in Figure 3 [redrawn after Ludlow & Wilson (1 19)], the maximum temperature dependence is observed under rate-saturating light intensities. At these intensities C4 plants generally have more pronounced temperature responses than C3 plants and the temperature optimum of C4 plants is usually higher. As light intensity is progressively lowered, the temperature response curves become Batter and broader. Since the light intensities required to saturate photosynthesis at low temperatures are lower than at high temperatures, a reduction in light intensity has little effect on photosynthesis until the intensity becomes limiting at that temperature. Ultimately, when light intensity is low enough to be limiting over the entire temperature range, the temperature curve is fully truncated and the net photosynthesis declines with increasing temperature. This decline is expected since at a given constant light-limited rate of gross photosynthesis, net photosynthesis would decrease with increasing respiratory production of CO2• However, Figure 6 below, based on the results of Ehleringer & Bjorkman (62), shows that there is a substantial difference in the temperature dependence of photosynthesis between C3 and C4 species at strictly rate-limiting light intensities. The basis of this difference will be discussed later.

It is obvious that meailingful comparisons of temperature response curves of leaves require that the light intensity dependence of photosynthesis is known. Comparisons should preferably be made at light intensities that are saturating over the entire temperature range studied, but it should be realized that plants in natural situations are subject to temporal and spatial variations in light intensity, and a complete understanding of the effect of temperature on photosynthetic productivity in a field situation requires considerably more information than can be obtained from temperature response curves determined at any single light intensity.

C3 PHOTOSYNTHESIS AND PHOTORESPIRATION The temperature response of leaves of C3 plants interacts with the CO2 and O2 concentrations during the measurement. Figure 4 [after (30)] compares the responses of Nerium oleander leaves acclimated either to a hot or to a cool growth regime and measured either at normal atmospheric or rate-saturating CO2 concentrations. The rate and the optimum temperature of lightsaturated photosynthesis are considerably higher at rate-saturating CO2 than at normal CO2• Similar differences between responses at normal and high CO2 concentration are observed irrespective of the temperature at which the plant was grown. However, differences in the rate at low temperature and the sensitivity of photosynthesis to high temperature inhibition of

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5 .------.-------.--,-----r------.

I." 4 N ' E

u 0 E

c 3 CI) 'iii III -C -+- 2 c >-<I) 0 -+-0 L a.

-+-(\) co

'+-0 (\)

-+-0 0 0::

- I 10 20 30 40 50

Leaf tempernture. °c Figure 3 Effect of light intensity on the temperature dependence of net photosynthesis in

leaves of Pennisetum purpureum. Number near each curve depicts the approximate light intensity (W m-z in the 400--700 nm waveband), Adapted from Ludlow & Wilson (1 19), these differently acclimated leaves are evidl�nt both at high and at low CO2 concentration. A similar enhancement of the rate of photosynthesis also occurs if the Oz concentration is decreased 1(24, 39, 41, 86, 96, 97, 1 53, 216); see review by Yolk & Jackson (94)]. These I�ffects of O2 and COz concentration are interpreted as arising from COz limitation of the RuPz carboxylase reaction and to effects on the ratio of photorespiratory COz release to total photosynthetic COz fixation. The comparative studies reviewed here do not indicate any significant role for differences in the mechanisms of photorespiration in the acclimation of C3 plants to various temperatures. However, it is important to consider these mechanisms in some detail since they do affect the temperature response ofphotosytlthesis in all C3 plants, and since they are basic to understanding the functi onal differences between C3 and C4 plants.

Recent biochemical studies of RuPz carboxylase have resolved many of the problems which had frustrated earlier efforts to correlate the kinetic

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5

TV) 4

'liE I I

(f(f C1

v (5 E I

I I

c 3 P , I ,

I I b

I , , I

I , 6 ,

h

OI0L---�'5----J---�----�---L----k---4�5�--5�0� 20 25 30 35 40 Leaf temperature, °C

Figure 4 Effect of CO2 concentration on the temperature dependence of photosynthesis in leaves of Nerium oleander grown at 20°C (filled symbols) and 45°C (open symbols). Triangles and circles depict measurements at normal saturating CO2, respectively. Adapted from (30).

properties of this enzyme with photosynthesis. When properly activated the enzyme is sufficiently active at low CO2 concentrations to account for the observed rates of CO2 fixation by the intact leaf [for review see Lorimer. Badger & Heldt (1 1 5)]. Also. the recent discovery of the alternate activity of this enzyme with O2 [(43); for review see Andrews & Lorimer (7)] has helped to understand the enigma of photorespiration better.

Osmond and coworkers (1 16. 146) have introduced the concept that photosynthetic carbon metabolism occurs by two linked cycles as shown in Figure 5. One of these, the photosynthetic carbon reduction cycle (PCR). occurs upon carboxylation of RuP2; the other, the photorespiratory carbon oxidation cycle (PCO). occurs upon oxygenation of RuP 2 (1 16). Since both reactions occur at normal atmospheric concentrations of O2 and CO2• both

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5 10 BERRY & BJORKMAN

(-3---PG-A�)� (P-glycolate) � -b e

t X t

PCO POfl�

I NADPH I I ATP I I co2 1 Figu,e 5 Schematic diagram indicating the key rela":ionships of the photosynthetic carbon reduction (PCR) and photorespiratory carbon oxidation (PCO) pathways. The balance between the RuPz carboxylase (A) and RuPz oxygenase -:0) reactions controls the relative rates of the two pathways (cf» . NADPH and ATP produced by the photosynthetic membranes are used to drive each pathway. For each carboxylation 3ATP and 2NADPH are required to regenerate RuPz; for each oxygenation 3.5ATP and 2NADPH are required to regenerate RuPz, and 1;2 COz is produced by the PCO pathway for each oxygenation (1 10). A genetic lesion at (C) of an A,abidopsis mutant inhibits photl)respiratory CO2 release.

cycles must operate simultaneously during photosynthesis of C3 plants. Given the occurrence of the oxygenase reaction, both cycles may be considered essential for photosynthetic carbon ass:tm.ilation. While at first sight the PCO cycle would seem to be counter productive since it produces C02 and since it competes with the PCR cycle for ATP and NADPH produced in the light reactions, the pathway apparently serves an essential function in metabolizing phosphoglycolate, a product of the RuP2 oxygenase reaction, to 3-PGA which can reenter the peR cycle. The importance of this pathway is demonstrated by recent studies by Somerville & Ogren (197) of a mutant of Arabidopsis thaliana which lack, phosphoglycolate phosphatase, an enzyme essential to metabolism of phospho glycolate. This mutant plant is photosynthetically incompetent under conditions which permit the RuP2 oxygenase reaction to occur. The inhibition is attributed to accumulation of phosphoglycolate.

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TEMPERATURE RESPONSE OF PHOTOSYNTHESIS 5 1 1

While the PCO pathway is apparently essential, net assimilation of COz is diminished and the energetic cost of the COz assimilated is increased as an increasing fraction of RUP2 is diverted to the PCO cycle. This branch point in photosynthetic carbon metabolism is assumed to be mediated by the dual activities of RuPz carboxylase (COzase) and RuPz oxygenase (Or ase). Other mechanisms for synthesis of photorespiratory substrates have been suggested (see 105). However, these mechanisms are not as well characterized as the RuPz oxygenase reaction and it is uncertain to what extent they occur in vivo. That the 02ase reaction is a major patl} of phosphoglycolate synthesis and metabolism is supported by several studies which have compared the control and isotopic labeling of glycolate synthesis by intact leaves and chloroplasts to that observed with the RuP 2 oxygenase enzyme (22, 1 16) and demonstrated that phosphoglycolate is a major precursor of photorespiratory CO2 production (197). In the absence of compelling evidence to the contrary (see 7), glycolate synthesis in vivo by mechanisms other than the RuPz oxygenase will for the present be assumed to be negligible.

Farquhar et al (69) derived a kinetic expression which relates the ratio rP of the rate of oxygenase reaction ( V02ase) to the rate of carboxylase ' reaction ( VCOzase):

rP = VOzase = Vmax 02ase X Km (C02) X [021 VC02ase V max C02ase Km (02) [C02] 1 .

At a given condition there will be ¢ oxygenations ofRuP2 for each carboxylation. This ratio is directly proportional to the ratio of concentrations of O2 and CO2; directly proportional to the ratio of the V max activities of the enzyme for Ozase relative to carboxylase; and inversely proportional to the ratio of the corresponding Km terms. The value of the ratio rP, but not the fluxes, at a constant temperature and gas concentrations appears to be independent of light intensity (47). There is abundant evidence suggesting that rP must increase with temperature. The CO2 compensation point (at which rP = 2) (36), the O2 inhibition of photosynthesis (35, 39, 41 , 96, 108), and the postillumination release of CO2 (87) all increase with increasing temperature. Also the quantum yield of C3 plants decreases with increasing temperature (62, 109). Ku & Edwards (107, 108) argue that these effects can be accounted for by temperature-dependent changes in the solubilities

. of Oz and COz in water. Their argument is based entirely upon studies of photosynthesis of intact leaves. As shown in Equation 1 , other parameters in addition to the solubility could affect the temperature dependence of ¢. We would have to assume that these additional terms remain constant in order to attribute the temperature dependence of photosynthesis in vivo

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exclusively to solubility. Laing et al ( 1 10) and Badger & Collatz (13) have examined the temperature dependence of the V max and Km terms. They conclude that the K",(C02) increases more rapidly with temperature (i.e. has a larger apparent activation energy) th:lfl does the Km(Oz). The ratio of these values thus increases with temperature, while that of the V max activities remain fairly constant.

Badger & Collatz (13) also address the solubility problem and conclude that the Km values are found to change with temperature whether the concentrations o( CO2 and O2 are expressed as gaseous partial pressures or as concentrations of dissolved gases. They also point out that expressing the Km 's directly in terms of partial pressures h�LS the advantage that the in vitro determinations of kinetic constants of the: enzyme can be related more directly to in vivo photosynthetic response; which are normally expressed in terms of gaseous partial pressure or concentration.

The temperature responses of the above kinetic parameters and the stoichiometry of the reactions of carbon metabolism can be utilized to examine how well the biochemical parameters predic:t actual measured leaf responses to temperature. Simulations of changes in ',he requirement for NADPH or ATP per unit of net CO2 assimilation with temperature (20) closely match actual measured determinations of changl� in the apparent quantum requirement for C02 fixation in normal air (62.). Figure 6 compares the results of calculations of the maximum rates of net assimilation (with rate-saturating RuPz supply to the enzyme) and the measured response of a leaf of Nerium oleander.

The simulations illustrate that the temperature dependence of the enzymatic processes contributing to net C02 assimilation is much lower at normal atmospheric concentrations of O2 and CO2 than at rate-saturating CO2, Two factors contribute to this efi'€:ct: (a) both the V max and Kin increase with temperature, and at low COz concentration these changes have nearly compensatory effects on the rate; (b) the value of tP increases with increasing temperature and decreasing CO2 according to Equation 1 , and the resulting photorespiratory CO2 p;:oduction diminishes the net rate of CO2 assimilation.

In contrast to the simulation of energe':ic efficiency of COz assimilation, the measured performance only matches the corresponding simulation at temperatures below 20°C. Irreversible loss of RuP z carboxylase activity does not occur until temperatures are in ex:cess of 50°C with Nerium oleander (30); and the rate of the RuPz carboxylase reaction in vitro does not decrease until temperatures are in exces�, of 35°C (13). It is therefore unlikely that the deviation between the simulated rate and the measured rate above 20°C reflects a loss in enzymatic capacity for CO2 fixation. A more

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I <I) (\j I e

u

'0 e �

5

4

3

2


I I

I I

, I

, ,

I ,

I

,

, ,' Saturating CO2

I I

I I ,

.; I ,

I ,

,.

/

'" "

" ,

'" "

, '" "

" "

, / 330 f bar CO2 " - I " Cs = 00 em s

" - - - - - -" .... -

/ ... ... _ ... - 330 f bar CO2 ,, "

., Cs = 0,5 em 5-1 , .,

Measured data 330 f bar CO2 Cs = 0.5 em 5-1

°10':-----l:15:---2.L0---':!--..L---:l-::--...I.--�-5..J.0----.J

55 Leaf temperature. °c

Figure 6 A comparison of the temperature dependence of the net CO2 assimilation by a leaf of Nerium oleander at rate-saturating light intensity and ambient CO2 and 02 concentration (solid line) [Ilfter (30)] with simulated net CO2 assimilation by:RuP2 carboxylase at comparable stomatal conductances (Q�) and concentrations of CO2 and O2• The predicted effect of entirely removing stomatai limitations (Cs = (0) and CO2 concentration limitations (saturating CO2) are also shown. The simulations were made with the C3 photosynthesis model of Berry & Farquhar (20). and RuP2 carboxylase activity per unit leaf area and kinetic constants for N. oleander RuP2 carboxylase (30). The simulations assume rate-saturating RUP2 concentratiorts at all C02 concentrations.

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5 14 BERRY & BJORKMAN

likely explanation is that the capacity of the: leaf to form RuP2 may not be able to keep pace with the capacity of the t:llzymes of the leaf to consume RUP2 in the C02ase and 02ase reactions as temperature increases. These reactions would be rate-limited by the concentration of RuP2 available.

Farquhar has recently discussed the possible regulation ofRuP2 carboxylase activity in vivo by the rate of supply of RuPz (68), and Collatz (51) has demonstrated that the steady state concentration of RuP2 in spinach leaf cells during photosynthesis falls precipitowily above 25°C. The results suggest a limitation in the rate at which RllP2 can be supplied at higher temperatures. Such a limitation could be explained if the maximum capacity for photophosphorylation or NADP reduetion became limiting.

A few measurements of the light-saturated capacities of electron transport reactions of isolated chloroplasts as Il function of temperature have been made (9, 30, 142). These studies all indicate a strong inhibition of whole chain electron transport activity at :trigh temperature. Furthermore, the maximum capacity for photosynthetk electron transport by isolated chloroplasts may not be much higher than that required to sustain CO2-saturated rates of COz fixation in vivo (32). It seems likely therefore that a substantial decline in the rate of ele�tron transport at high temperatures could result in a decline in the rate of RuP2 regeneration and ultimately lead to a lower steady-state RuP2 I�ncentration and hence a lower rate of net CO2 assimilation. Comparativf! studies of plants with differing responses to high temperature show a strong correlation between the effect of temperature on electron transport and that of photosynthetic CO2 assimilation (19, 30, 33).

As shown in Figure 4, there is a stron g interaction of the rate of CO2 assimilation with C02 concentration ov(:r the entire temperature range. According to the arguments above, the rate of photosynthesis is probably limited by the supply of ATP and/or NADPH over the upper temperature range. Thus a stimulation of the rate by CO2 under these conditions might not be expected. This apparent contradicti.on is another example of the dual effect of CO2 concentration on photosY:ilthetic carbon metabolism. CO2 concentration can affect the maximum capacity of the enzymic process of CO2 assimilation and, because it is a key factor controlling ¢ (the ratio of Ozase to C02ase reactions), it can alsc' affect the energetic cost per unit of COz assimilated. It is difficult to distiilguish between these two effects, and both may play a part in determining the response of photosynthesis under contrasting conditions. The latter effect on efficiency would seem to dominate under rate-limiting light intennities such as those uSed for measurement of the quantum yield for CO2 fixation, whereas the effects of CO2 concentration on the maximum em:y:mic capacity for CO2 fixation is most likely limiting under conditions of rate-saturating light intensity and

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TEMPERATURE RESPONSE OF PHOTOSYNTHESIS SIS

suboptimal temperature. Farquhar (68) argues that the steady-state concentration of RuP2 in the chloroplast may provide a reliable indication of the factors limiting the carboxylation process. However, the available data are inadequate to assess this possibility at the present time.

These discussions provide a rather complex picture of carbon metabolism of C3 plants and indicate a need for more information about internal factors that may influence the carboxylation process in vivo. The temperature response is partially determined by the kinetic properties of the RUP2 carboxylase of the leaf, by the temperature response of the photosynthetic electron transport system, and by the relative capacities of carboxylation and electron transport. The interactions are complex, and at present the best inferences are based upon data obtained from comparative studies of plants with contrasting thermal responses. These studies have indicated that the ability to maintain high rates of photosynthesis at high temperatures are correlated with increased stability and rate of photosynthetic electron transport at high temperatures (30, 33), and that capacity for photosynthesis at suboptimal temperature is limited by the total catalytic activity of potentially rate-limiting enzymes (26). These latter studies will be discussed in greater detail below. The above arguments also indicate a large scope for modification of the temperature effects via modification of RuP2 carboxylase properties. A few studies suggest that this may be possible. However this variability has not yet been related to differences in photosynthetic characteristics [for a review see Ogren & Hunt (145)].

C4 PHOTOSYNTHESIS As noted above, C. plants generally have a higher optimum temperature for photosynthesis than do C3 plants from similar habitats, and at low temperature the temperature dependence of photosynthesis is much steeper than that of C3 plants at normal air levels of CO2 and O2, These differences are entirely consistent with the now generally accepted hypothesis that the C. pathway serves as a mechanism for increasing the concentration of CO2 available for the carboxylation of RuP2 which is localized in the bundle sheath cells (19, 25, 26, 79, 8 1).

Leaves of C3 plants are stimulated to higher photosynthetic rates and in general have higher apparent temperature optima if the measurements are made at CO2 concentrations several-fold the normal atmospheric level whereas C. plants are affected little if at all by such CO2 enrichment. Thus, many of the differences between C3 and C4 plants are greatly reduced if the comparisons are made at rate-saturating CO2 for both species. Much of the apparent superiority of C4 species at ambient CO2 concentrations can be attributed to the fact that in C4 plants the normal air level of CO2 is nearly or fully rate-saturating whereas it is far from saturating in C3 plants. As shown in Figure 7, which compares the effect of temperature on the quan-

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tum yield for CO2 fixation by C3 and C4 spl�cies, C4 photosynthesis can be inferior to C3 photosynthesis under certain c:onditions. Ehleringer & Bjorkman (62) showed that the quantum yield, determined at rate-limiting light intensities and at the normal air level of CO2 and O2, is temperaturedependent in C3 species. As noted previously, this effect of temperature on the quantum yield is probably related to �, stimulation of oxygenation of RuP2 as temperature increases. Photores:piration is suppressed at high CO2 concentrations (49), and the quantum yield of C3 species is higher and temperature-independent if measured at either low O2 or high CO2 (Figure 7). The quantum yield of C4 plantil is independent of temperature even at normal air levels of CO2, consistent with the presence of a high internal concentration of CO2, However, the absolute value of the quantum yield in the C4 species is lower than in the ,e3 species at saturating CO2 (or low O2), consistent with the higher theorc:tical energy requirement in C4 photosynthesis [SATP, 2 NADPH/C02 fiied compared with 3ATP, 2 NADPH/C02 fixed in C3 photosynthesis (78)].

In normal air the quantum yield of C3 plants exceeds that of C4 plants at low temperatures, approximately matches that of C4 plants at 25° to 30°C, and becomes inferior at higher temperatures (Figure 7). The lower quantum yield of C4 plants at temperatures below 25°C is the only known disadvantage of the C4 mechanism relative to the C3 mechanism. Ehleringer (61) has argued that this disadvantage pla:rs a significant role in explaining the natural distribution of C3 and C4 gra:;ses. C4 species tend to be more

le I :;at CO2 I 0.08 � �3 ___ __ --I"'-_-l

il 0.061-'>'

c;---...!Jormal CO2

C4-----� E a i ;:, a 0.04 1- -

0.02 � -

o ��----�-----�� 10 20 30

Leaf tem�erature, °c

Figure 7 Effect of COl concentration on the temperature dependence of the quantum yield

for photosynthetic COl fixation (mol COl per ein:;tein) in C3 and C. plants, determined at

rate-limiting light intensities. In C4 plants the quantum yield is the same at normal and at saturating C014• Adapted from (62).

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abundant in regions where the prevailing temperatures are in excess of 30°C whereas C3 species tend to predominate in cooler habitats (55, 90, 2 12, 214).

It is clear that C4 species have photosynthetic characteristics which would be best suited to warm habitats. Although C4 species are rare in prevailingly cool regions and are entirely absent in many cold environments, certain C4 species such as Atriplex sabulosa, mentioned elsewhere in this review, and Spartina townsendii (1 14) nevertheless successfully occupy cool-temperate habitats. It may well be that in these cool habitats the disadvantage at low light intensities of the lower quantum yield associated with C4 photosynthesis is counterbalanced by the benefits of this pathway at high light intensities. In any event, C4 photosynthesis is not causally linked to a decreased tolerance to irreversible inhibition of photosynthetic activity by low temperatures nor to an increased tolerance to irreversible inhibition by high temperatures. The possible factors that underly differences in tolerance to damage by low and by high temperatures are causally unrelated to C4 photosynthesis and will be discussed later.

COMPARISON OF PLANTS FROM CONTRASTING THERMAL REGIMES

As discussed previously, and as'illustrated in Figure 2, species from native habitats with contrasting temperatures have different temperature response characteristics. Similar differences have been observed with plants that have a wide acclimation potential and which are grown under contrasting thermal regimes. At least two factors are involved in these adaptations or acclimations: (0) a general change in photosynthetic capacity at suboptimal temperatures, and (b) a change in the rate and the stability ofphotosynthesis at superoptimal temperatures. Differences between contrasting species in sensitivity to damage to the photosynthetic apparatus at low temperatures probably also exist (cfFigure 2). These factors appear to have separate mechanistic bases even though reciprocal changes in high- and low-temper-

_!\ture performance are nearly always observed. In part these changes result from adjustments in the photosynthetic apparatus which modify the thermal limits of tolerance. The basis of such changes will be discussed in following sections. It is important to note, however, that these limits, which are generally characterized according to the threshold temperature for an irreversible or only slowly reversible loss of photosynthetic activity, are usually preceded by a region of fully reversible inhibition. It is not known how these reversible effects, which seem immediately to precede the irreversible effects, are causally related to the factors which determine the limits for tolerance.

The general changes in photosynthetic capacity at suboptimal temperature might be predicted to result from changes in the activity of enzymes which become rate-limiting at low temperatures. This hypothesis has received considerable support. Pearcy (149) showed that changes in the

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5 1 8 BERRY & BJORKMAN

photosynthetic capacity of Atriplex lentiformis when grown at contrasting thermal regimes (Figure 2) were correlated with changes in the activity of RuP2 carboxylase present in the leaves of thh C4 species. Bjorkman & Badger (28) found that on measurement of 14 enzymes of photosynthetic metabolism, total leaf dry matter, chlorophyll or protein per unit area, only the activity of RuPz carboxylase differed in proportion to differences in photosynthetic capacity of Atriplex sabuloscl and Tidestromia oblongifolia (Figure 2) at suboptimal temperature. A. sahulosa, which had greater activity of RuP2 carboxylase and a larger amount of Fraction I protein, also had a higher photosynthetic rate at SUboptimal temperatures. This very specific correlation strongly suggests that the differences in RuPz carboxylase activity were responsibile for the differences in photosynthetic capacity. Furthermore, the measured activity of RUP2 carbm;ylase per unit leaf area of each species was almost adequate to support the measured rates of CO2 fixation at 20°C, if one assumes a rate-saturating CO2 concentration in the bundle sheath cells of these C4 plants.

For C3 plants, growth temperature-induced changes in photosynthetic capacity did not correlate exactly to the VauA RuP2Case activity. A comparative study of Nerium oleander plants grO"wn at contrasting temperatures showed that the activity of the chloroplast fructose- l ,6-bisphosphate phosphatase (Fru-P2 phosphatase) was best correlated with differences in the rate of photosynthesis at suboptimal temperature (29). It is perhaps not surprising that RuP2 carboxylase plays a II!Sser role in regulating the temperature response of C3 plants since, as shown in Figure 6, the activity of this enzyme is much less temperature dependent at the normal atmospheric concentration of C02 than it is at the rate-saturating concentrations which presumably prevail in the bundle sheath <;ells of C4 plants.

Further support to the argument that FJU-P2 phosphatase is a key factor limiting photosynthesis was obtained in e:cperiments which compared the time course of acclimation of photosynthesis by fully expanded leaves of N. oleander to a new and contrasting thermal regime with changes in the activity of this enzyme. As photosynthetic rate at 20°C increased upon transfer from hot to cool growth temperature over several days, there was a parallel change in Fru-P2 phosphatase activity. A similar response, but in the opposite direction, was observed upon transfer from cool to hot conditions (3 1).

The reaction catalyzed by Fru-P2 phosphatase is considered to be one of the key steps for regulation of the photosynthetic carbon reduction pathway (160). It may be that changes in the level of this enzyme are necessary to maintain effective control of this pathwa� as temperature is changed. This hypothesis would imply that the rate of CO2 assimilation at temperatures far removed from the growth temperature or outside of the normal tempera-

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ture range of a species may be limited because the mechanisms which control the metabolic pools of the peR cycle are not able to maintain an appropriate balance at these extreme temperatures.

Irreversible Temperature Responses The structural entities, enzymes, pigment-protein complexes, reaction centers, and membranes which enable the photosynthetic process to function are quite fragile. Exposure to unfavorable conditions, particularly to temperatures outside of the normal physiological range, may result in irreversible damage to these components. Photosynthetic capacity is lost in proportion to the extent of damage, and depending upon the severity of the damage, may recover over the course of a few hours to several days, or the tissue may die (16). In general the damage may be regarded as some form of denaturation. However, as will be discussed below, the limits of tolerance are determined by very specific lesions in the photosynthetic apparatus. Specific enzymatic activities are lost and specific functions of the photosynthetic membranes are altered at temperatures just beyond the threshold for damage. More severe damage and thermal breakdown of cellular integrity will occur at temperatures which far exceed this threshold.

The specific nature of the damage suggests that the properties of certain components of the photosynthetic apparatus determine the overall tolerance limits. There is an extensive literature dealing with the chemical and thermodynamic factors which maintain native protein and membrane structure (60, 206, 207). These factors interact strongly with temperature such that some native protein conformation may become lost both at high and low temperature (44, 204, 205). The stability of most proteins is thus optimal over a limited temperature range. The most important factor influencing the temperature for optimum stability is the primary structure of the protein which ultimately determines the extent of intramolecular interactions, such as hydrogen bonds, salt bridges, disulfide links, and hydrophobic interactions which tend to maintain the native conformation (e.g. 3). In addition, solutes which effect the ionization of a protein, or the structure of water, may modify the temperature stability of proteins, and some organisms alter the fatty acid composition of their lipids according to growth temperature. Such changes affect the melting point and physical properties of the lipid region ofbiomembranes and may dramatically affect the interactions between these lipids and proteins which associate with the membrane (1 65).

LOW TEMPERATURE ;iENSITIVITY There is no evidence that photosynthetic characteristics play a direct role in determining the capacity of a tissue to survive freezing, and this review will focus instead upon limitations

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to photosynthesis which may occur at temperatures above the freezing point of tissue water [for a review of freezing tolerance see Steponkus (199)]. With affected species photosynthesis may be irreversibly inhibited by exposure to chilling temperatures (45, 2 10). In addition, the photosynthetic characteristics of plants which develop at low temperatures may be nonadaptive, as illustrated by Tidestromia oblongifolia grown at 16/10°C growth regime (Figure 2) (38). Similar responses have been observed with other species (57, 1 19, 1 77). Most of these are so-called chilling-sensitive plants (121). However, low temperature inhibition is not restricted to such species. For example, Sawada et al (177) found that the photol.ynthetic rate of winter wheat was depressed in plants grown at cold temperatures (5-6°C), and Smillie et al ( 194) observed inhibition of normal chloroplast development of barley at 2°C. Both winter wheat and barley are considered chilling-resistant.

Development of chilling injury In considering the mechanisms which limit photosynthesis at low temperature, it is important to note that the symptoms of low temperature damage are the r;:sult of cumulative and often indirect effects of temperature over time. Exposure to chilling temperatures for only a few minutes is often not damaging, in part because chilling injury affects developmental processes which lead to synthesis of the photosynthetic apparatus at least as severely as it does the functional processes of photosynthesis. Chlorophyll synthesis may be severely impaired (14, 67, 126, 1 86, 194) at low growth temperatures. Slack et al (1 86) proposed that the developmental lesions in Sorghum may be caused by a failure to synthesize chloroplast ribosomes at chilling temp�ratures. Smillie (192) emphasized the importance of differential effects of temperature on the rate of development of chilling-resistant and chillil1g-sensitive species.

A strong stimulation of the severity of low temperature injury by exposure to high light intensity has been noted (210). Similar damage may be observed at a nonchilling temperature on exposure to excessively high light (32, 98, 99) or on treatment of the leaf under conditions which restrict normal photosynthetic and photorespiratory metabolism of the leaf (161). This injury, termed photoinhibition, is attributed to damaging effects of light absorption in excess of that which can be utilized for normal photochemical reactions. Since a reduction in temperature causes a general decline in the rate of the dark reactions of photosynthesis, the light required to saturate this capacity falls as temperature decreases and the threshold for sensitivity to photoinhibition increases. Tlis sensitization becomes especially acute with species which have other r�strictions upon their photosynthetic capacity, caused by low temperature, and may add to other chilling effects at low temperature (73, 208, 209, 2 1 1) or may in itself be a primary cause of damage at low temperature (37).

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C4 photosynthesis and chilling Many plants with the C4 pathway of photosynthesis are chilling-sensitive, and at one time it seemed likely that some step in the C4 mechanism was unusually sensitive to low temperature. Recent evidence indicates that this is not so. Atriplex confertifolia and A. vesicaria, two C4 species native to cool regions, grew well in laboratory studies at 8°C, and biochemical studies did not detect any disruption of the normal metabolic sequence of C4 photosynthesis at low temperatures (48). Neither did growth at low temperature result in any impairment of chlorophyll formation or disruption of chloroplast development, features which have been associated with chilling-sensitive C4 plants (45, 126, 1 86). However, other features of C4 photosynthesis provide advantages to C4 plants at warm temperatures, and most C4 plants are native to warm or tropical regions. Many C3 species from these regions are also chilling-sensitive; thus the sensitivity of these C4 plants to chilling is probably not some special property of C4 photosynthesis, but may occur with it.

Lipid properties Many of the reactions of the photosynthetic process are associated with membranes, and changes with temperature in the structure of these membraneS might be expected to have significant effects on the overall rate of photosynthesis. As early as the 19208 it was proposed that "solidification point of the contained lipoid" could account for the observed injury or death of sensitive tissue at low temperature (203), and in the 1960s the application of physical techniques such as X-ray crystallography (120), differential scanning calorimetry (198), freeze-fracture electron microscopy (95), and spin label probes (167) permitted detection of such solidification of biological membranes and polar lipid bilayers. At a certain temperature, dependent upon the composition of the lipid mixture, a change from a Buid to a gel phase occurs. With the complex lipid mixture of biological membranes this phase change occurs over a temperature range of several degrees. and within this range the two phases separate to form a bilayer of mixed phase. The process has been termed lateral phase separation ( 1 1 3) [for a review see Raison (163)].

Most evidence now indicates that the membrane lipids of higher plants are usually in the Buid phase at normal physiological temperatures ( 156), and that phase separation of membane lipids may occur in chilling-sensitive plants at chilling temperatures (162). These correlations, however, are based on studies of a limited number of species. Additional evidence for a role of lipid phase boundaries in the thermal tolerance of plants is derived from studies of the lipid properties of plants in relation to the habitat preference of native vegetation. If there is a physiological disadvantage to having lipids which show phase separation at temperatures which the plant is likely to experience. then natural selection should lead to lower phase

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S22 BERRY & BJORKMAN

separation temperatures for plants growing in cool as opposed to warm climates. Results with species of the Sonoran and Mojave deserts which grow in cool or hot seasons (156) and species which are native to temperate or tropical Australia (166) are consistent with this proposal. Plants native to cool thermal regimes have membrane lipids which do not show phase separation until near or below QOC, whereas most species which grow at high temperatures have lipids which begin phf1Se separation at temperatures from 15°C to SoC. The evergreen species oftt:mperate regions change their lipids with the season (157).

Membranes become much more permeable to ions and large hydrophilic molecules when the lipids are in the mixed mther than in the entirely fluid phase (42). According to the chemiosmotic mechanism of energy transduction, the chloroplast membranes must have a very low passive permeability to H+. Nobel (141) showed that the chloroplasts of chilling-sensitive plants become more permeable to glycerol and erythritol at chilling temperatures, and Fork and coworkers ( 1 1 . 137) have show:il more rapid dissipation of the "energized state" of chloroplast membranes (attributed to ion leakage) from chilling-sensitive species at low temperatUIes. They also point out that diffusion of electron transport components of the membrane may be restricted in gel phase regions (138).

Lipid-protein interactions are also altered by membrane lipid solidification. Freeze-fracture electron microscopy of membranes of microorganisms provides the most dramatic demonstration of these changes. Regions of the membrane which are in the solid phase are Il.pparently without protein (see 10). The protein which was (at higher temperature) associated with these solidified regions has been variously interprded as having moved (a) laterally to the remaining fluid regions of the membrane (95), or (b) vertically out of the plane of the membrane (10). In t�ither case some of the protein of the membrane is in a different environment than it is at temperatures above the phase separation temperature, �nd catalytic activities of such protein may be altered or lost.

Photosynthetic reaction center proteins :md electron transport proteins are located in the chloroplast membranes. Abrupt changes in the apparent activation energies of photosynthetic electron transport reactions at the phase separation temperature (138. 185) have been reported. Loss of membrane-bound Mn+2 ion essential for photosystem II activity during exposure to chilling temperatures (101, 124) and formation of free fatty acids (presumably the result of lipase activity) at chilling temperatures (100) have both been reported. All of these above etfc�ts might be related to altered lipid-protein interactions. In addition. many developmental processes such as ribosome and protein synthesis take plaee on the chloroplast membrane and could also be affected by structural changes of that membrane (127).

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The hypothesis that lipid phase changes may have far reaching effects upon plant metabolism and play a key role in determining the sensitivity of a plant to chilling is simple and attractive, but it is important to add some notes of caution. The hypothesis as now formulated is based primarily upon studies with model systems of purified lipids and upon studies of the comparatively simple membranes of prokaryotic organisms. It is not clear that interpretations based upon these studies alone can be applied to the more complex membranes of higher plants. There are also divergent opinions as to the use and interpretation of techniques for determining the phase boundaries of membrane lipids from higher plants. A recent paper has proposed that other lipid properties (which may be correlated with the phase boundary) are the actual determinants of chilling injury (220). In any event, lipids do play a role in determining the low temperature limit of certain photosynthetic processes, although the causal relationships are complex and not well established at this time.

Denaturation of soluble proteins Certain enzymes which participate in photosynthetic carbon metabolism may be labile at low temperature. RUP2 carboxylase of Nicotiana loses activity upon storage at DoC, and this activity can be recovered upon brief heat treatment of the enzyme (103). There is some evidence that this process may be of importance in vivo. Sawada et al (176) report that photosynthesis of winter wheat, grown under cold conditions, is initially very low and increases dramatically over several hours if the plants are warmed to 25°C. They suggest that the increase in rate is related to an increase in RuP2 carboxylase activity. Huner & MacDowall (92) have characterized a form ofRuP2 carboxylase which is formed in rye seedlings grown at low temperature. This form is more stable to low temperature inactivation and has a more favorable Km (C02) at low temperature than does RUP2 carboxylase from rye seedlings grown at higher temperatures (93). Huner and MacDowall suggest (but do not show) that the RuP2 carboxylase formed in cold-hardened seedlings may improve their photosynthetic performance at low temperatures.

Pyruvate orthophosphate dikinase, an enzyme which serves in C4 photosynthesis to regenerate the primary CO2 acceptor, dissociates to an inactive form at low temperature (82, 1 84). The rate oflow-temperature inactivation of this enzyme in vitro differs according to the species from which the enzyme is extracted (202). The enzyme of species that are successful at low temperature is more stable at low temperature. Effects of cold treatment in vivo on the extractable activity of pyruvate orthophosphate dikinase were also demonstrated and seem to be correlated with the overall sensitivity of the species used (202).

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Graham et al (74) have examined the eif<:cts of temperature on PEP carboxylase from various species, and point Oilt that additional studies are required to determine if the primary cause of low temperature injury to plants is through denaturation of soluble proteins or is related to lipid properties. Comprehensive comparative studi{s of the low temperature sensitivity of plants and metabolic factors such as the lipid properties or soluble proteins of the same plant have not been conducted. The complex, timedependent nature of low temperature inhibition makes such comparison difficult.

HIGH TEMPERATURE SENSITIVITY Ther'� is unequivocal evidence that inhibition of whole leaf photosynthesis by hiE;h temperature is caused by a disruption of the functional integrity of the photosynthetic apparatus at the chloroplast level (9, 15, 2 1 , 27, 33, 151). As Ilentioned earlier, heat inhibition of CO2 fixation by intact leaves is not caused by stomatal closure. The finding that at any given temperature COz-sllturated photosynthesis is inhibited to the same degree as COz-Iimited pl:.otosynthesis further excludes the possibility that the heat inhibition is cam.ed by an increased resistance to CO2 transport between the intercellular air spaces and the chloroplasts (27, 30, 1 30).

Heat injury to chloroplast function and integrity could a priori result from a heat-reduced loss of the semipermeability of the plasma-membrane, the tonoplast, or other partitioning membranes in the cell. Such a loss of semipermeability is likely to cause adverse changes in the immediate cellular environment of the chloroplast, such as a (:hange in pH or ionic composition. However, while such effects undoubteclly occur if the temperature is sufficiently high, it is evident that the heat stability of the partitioning membranes far exceeds that of photosynthe:,is. For example, loss of semipermeability ofthe membranes which prevent leakage of solutes from leaves or leaf sections of Atriplex sribulosa, Tidestlomia oblongifolia and Nerium oleander into surrounding aqueous media [a ;;tandard method used to assess the heat tolerance of leaves; see Levitt (l 12}) does not occur until temperatures about lOOC higher than those which cause inhibition of.photosynthesis are reached (21 , 3 1).

Dark respiration is also much more heat resistant than photosynthesis; nearly complete inhibition of photosynthesis occurs before any inhibition of dark respiration or other symptoms of high temperature injury can be detected in the same leaf tissue (27). Moreover, as shown by Krause & Santarius (l06) with isolated spinach chloroplasts, the chloroplast envelope is more resistant to heat damage than are the internal photosynthetic membranes. It is thus probable that inactivation of photosynthesis that occurs when leaves are subject to high temperatures primarily reflects a direct effect of heat on chloroplast function.

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A related problem is that the heat stabilities of various activities determined in experiments in which preparations of isolated chloroplasts, thylakoid membranes, and enzymes are heated in vitro may differ from their intrinsic heat stabilities in vivo. Isolated chloroplasts, at least when the outer membrane has been lost during isolation, generally exhibit a lower heat tolerance than they do in situ, indicating that the natural internal environment is more favorable than that provided by the artificial suspending medium (cf 106). Interpretations of heat responses, based on studies in vitro alone, must therefore be made with some caution, especially when the in vitro heat stability of a particular reaction or structure is relatively low. These considerations may be even more important in comparisons of heat stability of the activities of extracted enzymes since the heat stability of many enzymes in solution is dramatically affected by factors such as pH, ionic composition, substrates, activators, enzyme concentration, and the presence of other proteins.

Heat inactivation of thylakoid membrane reactions Heat treatment of photosynthesizing leaves causes a progressive inactivation of chloroplasts subsequently isolated from the leaves (i.e. heat treatment of chloroplasts in vivo) (17, 21 , 30, 33, 15 1). Moreover, for a given plant material, the onset of these inactivations occurs at nearly the same temperature as that which causes the following: (a) a reduction of the quantum yield for whole leaf photosynthesis (27, 33, 1 5 1, 178); (b) a sudden rise in the Fo level of chlorophyll a fluorescence emitted from the leaves (9, 1 5 1, 164, 178); and (c) irreversible inhibition of light-saturated photosynthetic CO2 uptake in intact leaves (28, 30, 33). Examples of some of these responses are shown in Figure 8 for Atriplex sabulosa and Tidestromia oblongifolia. The quantum yield for electron transport driven by photosystem II (pS In in these two species (33) and the light-saturated PS II activity of Nerium oleander (30) chloroplasts were much more sensitive to heat treatment of the leaves than the corresponding activities of photosystem I (PS I)-driven electron transport. Bauer & Senser (17) also observed that the activity of the Hill reaction (with DCIP as the electron acceptor) of chloroplasts isolated from heat-treated Hedera helix leaves exhibited a high-temperature sensitivity resembling that of whole leaf photosynthesis. Heat treatment of Nerium oleander leaves resulted in very similar kinetics for inactivation of whole:' chain electron transport (H20 � methylviologen) and noncyclic photophosphorylation (ADP-dependent pH change), whereas little inactivation of PS I activity (DCIPH � methylviologen in the presence of DCMU) occurred over the same temperature range (30). Inactivation of photophosphorylation seems, at least in part, to be caused by uncoupling from electron transport in leaves of Atriplex sabulosa, Tidestromia oblongifo/ia and Atrip/ex /entiformis (33, 15 1).

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Figure 8 Effect of leaf temperature on the quantum yield for photosynthesis in intact Atrip/ex sabulosa (I-I) and Tidestromia ob/ongifo/ia (0-0) leaves, and of pretreating illuminated leaves for 10 min at different temperatures on the quantum yields for photosynthetic electron transport by chloroplasts isolated from the leaves [redrawn after (33)]. Also shown is the effect of leaf --------.. -- �- .1.._ .... �.��O�M .,;ol,l nf rI .. t�,.h....1 1p�v"" rr .. <irawn after (178)1 .

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The above results obtained by heat treatment of intact leaves qualitatively resemble those obtained in numerous experiments in which isolated chloroplasts were sUbjected to heat treatment in vitro (9, 2 1 , 65, 66, 102, 106, 1 22, 1 3�136, 142, 1 73, 223). Heating of isolated chloroplasts also leads to preferential inactivation ofPS II activity and of non cyclic photophosphorylation. PS I activity is very heat-stable; significant inactivation ofPS I is not detected until temperatures are reached that cause complete inactivation of PS II activity.

Several studies indicate that the water-splitting apparatus of PS II is especially sensitive to heat. One line of evidence supporting this conclusion is that PS II-driven electron transport by heat-inactivated chloroplasts can be partially restored by addition of suitable compounds (such as 1,5-diphenylcarbazide) which can act as artificial electron donors to PS II ( 1 5 1 , 175, 223). Other support for this conclusion i s provided by Cheniae & Martin (50), who attributed the effect to the loss of manganese from the water-splitting system of PS II; by Babcock & Sauer (12), who showed that the decline in the rate of O2 evolution that occurs upon heat treatment of spinach chloroplasts parallels an increase in rapid ESR signal linked to the inactivation ofPS II; and by Maison & Lavorel (122), who studied the effect of temperature on the changes in various kinetic parameters of the O2 evolving system.

Heat inactivation of noncyclic photophosphorylation probably results from a concurrent inactivation of PS II-driven electron transport and an uncoupling of phosphorylation from electron transport. Numerous studies have been made on the uncoupling effect of heat in isolated chloroplasts (65, 66, 106, 1 33-1 35, 173-175). The ATP-synthesizing enzyme (coupling factor) has a much higher heat stability than photophosphorylation (135, 1 75), and the uncoupling has been attributed to heat-induced irreversible changes in the permeability of the thylakoid membranes, causing a reduction in the proton gradient so that it becomes insufficient to drive photophosphorylation. On the other hand, photophosphorylation has been found to become heat inactivated before the formation of the proton gradient is affected (66, 106, 175); also see (193). Emmett & Walker (66) suggested that heat treatment may increase the permeability of the membranes to charge-compensating ions so that the light-induced charge separation is decreased. This explanation assumes that the proton gradient alone is not enough to drive photophosphorylation. Santarius ( 175) suggested the possibility that photophosphorylation is especially heat-sensitive because the coupling site is close to the PS II water-splitting system. It is noteworthy that PS II and photophosphorylation activities are also both lost by water stress (104), by chilling (73, 100), and by addition of long-chain alcohol treatment (136) of chloroplasts, suggesting a close link between the two activities.

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Armond, Schreiber & Bjorkman (9) sug�;ested that the association between the light-harvesting pigments and (tie reaction center complexes might be even more sensitive to heat damag,e than the water-splitting system. In Larrea divaricata chloroplasts. heat inhibition results in a decrease in the quantum yield of electron transport, followed at temperatures several degrees higher by a loss of capacity for light-saturated electron transport. The authors attributed this decline in quantum yield to a heat-induced decrease in the efficiency of excitation eneqy transfer from chlorophyll b to chlorophyll a and changes in the distribution of energy transfer to PS II and PS I. The block in excitation energy transfer was characterized by a preferential loss of the effectiveness of �f80 nm light to drive electron transport and the appearance of a chlorophyll b fluorescence emission peak at 660 nm.

Analyses of thylakoid membranes from Nerium oleander leaves by freeze-fracture electron microscopy showed that heat treatment causes a progressive change in size distribution of membrane particles, consistent with the hypothesis that the light-harvestbg complex becomes physically dissociated from the PS II core complex (8, 1 65). Raison et al (165) suggest that such dissociation may be related to an alteration of the relative strength of hydrophilic and hydrophobic interactions. If it is assumed that the forces linking the light-harvesting pigment-protei.n complex with the PS II complex are hydrophilic, then with increasing temperature the strength of these hydrophilic interactions decreases while that of hydrophobic interactions increases so that the pigment-protein complexes will tend to associate more with the lipids in which these supramolecu) ar complexes are embedded than with each other. As a result, the distance between the light-harvesting pigment protein and the reaction center protein will increase, and if the interactions became sufficiently unbalanced, the complexes would tend to dissociate. It is noteworthy that the temperature at which such dissociation occurs appears to be related to the fluidity of the thylakoid membrane lipids (164, 1 65). It would not be surprising if such dissociation had multiple disruptive effects on chloroplast function, However. as mentioned earlier, such disruptions may also be caused by other more direct effects of high temperature on the membrane proteins 2.ssociated with PS II photophosphorylation and ion transport.

Heat inactivation of enzymes of photosynthetic carbon metabolism While it is evident that heat inactivation of whole leaf photosynthesis may be explained by the heat sensitivity of thylakoid membrane reactions alone, it is noteworthy that certain soluble enzymes considered to be located outside this membrane, either in the stroma re,�ion of the chloroplast or in the cytoplasm, are also inactivated when lea, es are heated to temperatures that

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cause irreversible inhibition of photosynthesis. Bjorkman and coworkers (28, 30, 33) determined the effect of treating photosynthesizing leaves of Atriplex sabulosa, Tidestromia oblongifolia, and Nerium oleander at a series of temperatures on the activities of 14 enzymes of photosynthetic carbon metabolism subsequently extracted from the leaves. There are marked differences in the heat stabilities between the different enzymes, and as discussed later, the heat stability of any one enzyme also depends on the species and growth temperature regime. Enzyme activities such as NAD malate dehydrogenase, Fru-P2 phosphatase, phosphohexose isomerase, and phosphoglucomutase and NADP reductase are stable to at least 50°C. The heat stability of RuP2 carboxylase also is quite high and . considerably exceeds that for whole leaf photosynthesis in these three species as well as in Hedera helix (17), various grasses (215), and in spinach leaves (224). Certain other enzymes studied by Bjorkman and coworkers, e.g. 3 PGA kinase, Fru-P2 aldolase, and phospJ;toenolpyruvate carboxylase, show somewhat lower heat stabilities, but these .stabilities still exceed that of photosynthesis in the same material. (With respect to heat stability of phosphoenolpyruvate carboxylase cf(125, 1 55, 170).] Adenylate kinase and NAD glyceraldehyde-3P dehydrogenase show initial heat inactivation of activity at temperature close to those that cause irreversible inhibition of photosynthesis in some plants but not in others.

Three enzymes, NADP glyceraldehyde-3P dehydrogenase, ribulose 5P kinase, and NADP malate dehydrogenase, show apparent heat stabilities in vivo surprisingly similar to those of photosynthesis for any one of the three species mentioned above. These enzymes require light for their activation (5, 6, 29, 80), and it is probable that the state of activation depends on the supply of reducing power to ferredoxin (221). Hence, heat inactivation of these "light activated" enzymes in vivo may be linked to the heat inhibition of PS II activity mentioned earlier. While such an indirect mechanism of inactivation seems to provide the most likely explanation for the observed decline in the activity of these "light activated" enzymes at high temperature, the possibility that this decline reflects a low intrinsic heat stability of the enzymes themselves cannot be ruled out (28).

Heat treatment of leaves may also result in a decrease in the amount of soluble leaf protein normally extractable with aqueous buffers. This decrease presumably occurs through some form of denaturation and precipitation of the native protein. A significant loss of extractable protein can be detected at approximately the same temperatures that cause irreversible inhibition of photosynthesis and may be intimately involved in this inhibition (28, 3 1). The general size class of proteins rendered insoluble by heat treatment of leaves is in the < 100,000 daltons category, but so far there is no information on the identity of these proteins. It is, however, clear that

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the loss cannot be explained by denaturation of any of the 12 soluble enzymes studied by Bjorkman and coworkers. These enzymes include the major soluble chloroplast enzymes and should make up more than 50% of the total soluble leaf protein.

Repair of heat damage to the photosyntheti-: apparatus Although in this review the term "irreversible heat inactivation" is used to denote any heat inactivation that has not shown recovery upon return to lower temperature within several minutes to several hours, this usage does not exclude the possibility that, given sufficient time, partia:l or even full recovery can take place. Bauer & Senser (17) showed that heHt inactivation of the photosynthetic electron transport as well as heat-induced alterations in chloroplast ultrastructure in Hedera helix leaves wen: reversible as long as the heat stress was not so severe as to cause extensive impairment of the cell's partitioning membranes and necrosis of the leaves. As might be expected, both the degree of recovery and the time required for recovery depend on the severity of the heat stress. For exampJe, Hedera helix leaves exposed for 30 min to 44°e lost about 50% of their photosynthetic electron transport activity but recovered fully in 7 days after return to 20oe. However, after heat stress at 48°C, causing a 75% loss of activity, recovery took almost 2 months. Similar time courses wen: observed for recovery after heat stress of photosynthetic CO2 uptake by whole leaves of the same plants (5). Little is known about the processes that are responsible for such post-stress repair.

ADAPTIVE RESPONSES IN THE HEAT STABILITY OF THE PHOTOSYN

THETIC APPARATUS As is evident fro:n earlier discussions, differences in the photosynthetic performance at high temperatures may in large part be attributable to differences in the heat stability of the photosynthetic apparatus. The degree of heat stability is related both to the thermal regime of the habitats from which the plants c,riginate and to the temperature regime under which they were grown. Many examples given in previous parts of this review indicate such relatio:l1ships. Recent surveys of species from a wide range of habitats (18 1, 195; J. A. Berry, in preparation) have used the rise in the level F 0 fluorescence as a criterion for heat sensitivity of the photosynthetic apparatus, and have provided further evidence for a general correlation between heat stability and the temperature of the environment in which the plants presumabJy evolved. However, in most instances it is difficult to separate this genotypic influence from the effect brought about by the growth temperatun: regime. Other studies have shown that there is a close relationship between the onset of the steep rise in the level of F 0 fluorescence and irreversible heat inactivation of photosynthesis and PS II activity (178, 193), and that photosynthetic acclinllation to high

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temperatures is accompanied by an upward shift of the temperature at which this rise in fluorescence occurs in Atriplex lentiformis (15 1), Larrea divaricata (9), and Nerium oleander (164). It appears that an increased heat stability of whole leaf photosynthesis, whether genotypically detennined or resulting from acclimation to high temperature, involves an increase in the thermal stability in most, if not all, of the component processes discussed earlier. For example, the difference in heat stability of whole leaf photosynthesis between Atriplex sabulosa and Tidestromia oblongifolia involves similar differences in the temperatures at which impainnent of thylakoid membrane reactions occur (33, 1 78; see Figure 8), extractable soluble protein is lost from the leaves, and certain enzymes of photosynthetic carbon metabolism are inactivated in vivo (28). Similar differences in the apparent heat stability of chloroplast membrane reactions and soluble enzymes are also found between Nerium oleander plants grown at low and high temperatures (30). In the latter species the difference in the temperature at which a functional impainnent of the membrane reactions occurs parallels the difference in the temperature at which a physical dissociation of supramolecular chlorophyll-protein complexes takes place (9).

It is especially noteworthy that acclimation to high temperature in both Nerium oleander and Atriplex lentiformis results in a decreased fluidity (measured at any given temperature) of the polar lipids of the thylakoid membranes (164); moreover, the actual fluidities determined at the temperatures at which the rise in Fo fluorescence occurs in each case are almost identical regardless of species and growing conditions. The lipid modifications responsible for these changes in the physical properties of the membrane lipids have not yet been identified, but it is clear that in both species the decreased fluidity of the polar lipids in response to acclimation to high temperature is accompanied by a considerable decrease in the unsaturation in the fatty acids of the total polar lipids from the leaves in both species (1 50; J. K. Raison, C. S. Pike, and J. A. Berry, in preparation). This change in fatty acid composition is consistent with the observed changes in fluidity.

These results provide strong evidence that changes in the properties of the chloroplast membrane lipids play a major role in photosynthetic acclimation to high temperature by increasing the heat stability of the membranes. Obviously, other factors, such as genetically determined or environmentally induced differences in homologous proteins or in the nature of their aqueous environment, may also affect the heat stability of the photosynthetic apparatus. Such differences are likely to be responsible for the substantial differences that exist in the heat stability of soluble enzymes between species and between plants acclimated to different temperatures (28, 30). The observation that acclimation to high temperature often leads to an increased stability of photosynthetic enzymes whose heat stabilities

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are quite high even in cold-adapted plants is in accordance with Alexandrov's (2-4) proposal that adaptation to hi,�h temperature requires a decreased flexibility of protein molecules through changes in intramolecular bonding, regardless of whether the proteins have high or low heat stability.

CONCLUDING REMARKS

In summary, there is conclusive evidence fllat plants exhibit considerable differences in their photosynthetic response to temperature and that many of these differences reflect an adaptation to the temperature regimes of the respective native environments. For the most part. these differences are based on selective modifications to constituents of the photosynthetic apparatus that may limit the tolerance as wdl as those that determine the capacity of photosynthesis over specific regions of the temperature spectrum. Modifications leading to an improvement in the photosynthetic performance at high temperatures evidently result in decreased performance at low temperatures and vice versa, both in terms of tolerance and capacity. No clear mechanistic basis for this apparently mutual exclusiveness has yet been established. Plants native to habitats characterized by great variations in temperature over their growth season do not necessarily possess a broader temperature range of adequate photosynthetic performance or tolerance at any one time than do plants limited to habitats that are either continually cold or hot with little seasonal variation. However. the former plants tend to possess a higher, genetically determined potential for photosynthetic temperature acclimation, enabling them to shift their temperature range of adequate photosynthetic perfonnance in concert with seasonal changes in temperature regime.

Such temperature acclimation involves changes in several components of the photosynthetic apparatus. For example, increases in the level of enzymes of photosynthetic carbon metabolism, such as RUP2 carboxylase and FruP2 phosphatase, are apparently important determinants of photosynthetic capacity at low temperatu res, and the stability of proteins and appropriate adjustments in membra lle lipids may contribute to low temperature tolerance. Changes in the p hysical properties of chloroplast membrane lipids leading to an increased heat stability of these membranes evidently are a key factor in acclimation to high temperature; there is evidence that an increased heat stability of soluble enzymes may also be involved.

C4 photosynthesis is a genetically fixed adaptation which because of its function as a metabolic CO2-concentrating mechanism greatly improves the photosynthetic performance at higher temperatures. Presence or absence of the C4 pathway is not causally linked to factors that determine the tolerance

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to low or high temperatures, but C4 photosynthesis frequently occurs together with other attributes that are important to effective photosynthetic function at high temperatures. This association is probably related to the evolutionary history of C4 photosynthesis. In all likelihood the C4 pathway evolved polyphyletically in hot, water-limited environments, under conditions where the advantages of an internal COz-concentrating mechanism would be especially great. Hence, the C3 progenitors of C4 plants may already have possessed a number of characteristics associated with high temperature tolerance, and these characteristics (which are probably disadvantageous in cold environments) therefore tend to be genetically linked to C4 photosynthesis.

These comments summarize what might be called the first approach to the problem of photosynthetic temperature adaptation. Our previous discussions also point to the need for a better understanding of the effect of temperature on those processes that underlie the synthesis of the photosynthetic apparatus. For example, ability to sustain photosynthesis at high temperatures is likely to depend on the presence of a heat-stable proteinsynthesizing system which enables the plant to replace or to repair components that are impaired by heat (125). Evidence that inhibition of RUP2 carboxylase synthesis and of proper chloroplast development above 30°C in seedlings of winter rye are caused by heat inhibition of chloroplast rRNA and ribosome fonnatiori (7 1) supports this concept. There are also significant differences between species of higher plants in the response of chloroplast biosynthesis to both high (70) and to low (1 92) temperatures. Little is known about the bases of these differences. Bernstam (18) in his review of heat effects on protein biosynthesis in nonphotosynthetic microorganisms comments that some of the early events in the initiation of translation are likely to occur on or in close proximity to a particular membrane and to be directly intluenced by that membrane. Lipid-protein interactions that affect primary events in protein synthesis could thus strongly intluence chloroplast biogenesis.

The probable effects of temperature and of lipid composition on these interactions lead to our final point that membrane properties, and the control of these properties via temperature-sensitive biosynthetic reactions, appear central to temperature adaptation of photosynthesis (and other ' metabolic processes). The biochemical pathways of chloroplast lipid synthesis are not yet fully understood, and almost nothing is known about the effects of temperature on this synthesis. Genetically detennined differences in pathways, sensory systems. or in the effectiveness of the control mechanisms involved in chloroplast biogenesis, may be largely responsible for the remarkable differences that exist among plants in the potential for photosynthetic acclimation to temperature.

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