control of flowering and reproduction in temperate grasses

8/2/2019 Control of Flowering and Reproduction in Temperate Grasses

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Control of Flowering and Reproduction in Temperate GrassesAuthor(s): O. M. HeideReviewed work(s):Source: New Phytologist, Vol. 128, No. 2 (Oct., 1994), pp. 347-362Published by: Blackwell Publishing on behalf of the New Phytologist TrustStable URL: http://www.jstor.org/stable/2558331 .

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New Phytol. (1994), 128, 347-362

Con t r o l o f f l ower ing a n d reproduction i ntemperate g r a s s e s

BY 0. M. HEIDEDepartment of Biology and Nature Conservation, Agricultural University of Norway,0P.O. Box 5014, N-1432 As, Norway(Received 3 June 1994)

CONTENTSSummary 347 III. Inflorescence development 356I. Introduction 348 IV. Inflorescence proliferation 357

II. Induction 348 V. The role of gibberellin 3581. Terminology 348 VI. Synchronization with seasonal climatic2. Juvenility and the flower-inducible stage 349 changes 3593. Induction types and classification 350 References 360

(a) Species with single LD induction 350(b) Species with dual induction

requirements 350

SUMMARYTemperate grasses of the subfamily Festucioideae can be grouped into two main categories according to theirenvironmental control of flowering, species with a regular long day (LD) induction, and those with dual inductionrequirements. The former group includes the temperate annual grasses and a few perennial species such as Phleumpratense and Poa nemoralis. These species have no winter requirement and require only LD to flower.

Most temperature perennial grasses have a dual induction requirement for flowering, a primary induction whichis brought about by low temperature (vernalization) and/or short days (SD), and a secondary induction whichrequires a transition to long days and is enhanced by moderately high temperatures. In most dual induction speciesSD and low temperature are interchangeable and independently able to fulfil the primary induction requirement.Yet, they are highly interactive in this process. Commonly the plants become day neutral at low temperature(0-6 ?C) and primary induction takes place in both SD and LD. Primary induction is then identical with thecommon vernalization response. At higher temperatures induction becomes increasingly dependent on SD, untila critical temperature is reached, usually c. 12-18 ?C, at which primary induction cannot take place regardless ofthe photoperiod. In a few species, e.g. Bromus inermis,Phalaris arundinaceaand to some extent Dactylis glomerata,the SD response predominates while low temperature induction is weak or absent.Critical temperatures and photoperiods for primary induction vary greatly among species and, within thespecies, among ecotypes of different geographical origin. Critical exposure time may vary from 3-4 wk in arctic-alpine Poa species to 20 wk in some Festuca species. Generally, ecotypes from high latitudes and especially arctic-alpine ones, have wider temperature and daylength limits and require fewer inductive cycles for primary inductionthan their low-latitude counterparts. In some grasses, especially arctic-alpine species, initiation of inflorescenceprimordia takes place during SD primary induction, in others it requires a transition to LD. In the former group,primordia are initiated in the autumn, an important adaptation to arctic-alpine conditions.

Critical photoperiods for secondary induction vary from 9-10 h in Mediterranean ecotypes to more than 16 h,and the critical number of LD cycles from four to eight, whereas 12-16 LD cycles are needed for the full saturatedresponse. Generally, high-latitude ecotypes have longer critical photoperiods and require more LD cycles forsecondary induction than do those from lower latitudes. Culm elongation, heading and inflorescence developmentare all promoted by LD. The more inductive cycles given and the more favourable their daylength, the greateris the response.

Grasses also have eficient vegetative means of reproduction which are also environmentally controlled.Vegetative proliferation of inflorescences or 'vivipary ' is readily induced in habitually seminiferous grasses of bothLD and dual induction types, by marginal LD induction of floweringi On the other hand, a high proportion ofnormal flowering can be obtained in habitually viviparous species and ecotypes by optimal primary and secondaryfloral induction. Thus, sexuality is by no means entirely suppressed in viviparous species but is underenvironmental control.


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348 O. M. HeideIn the high-latitude environment the primary induction requirements are met by the decreasing daylength andtemperature of autumn and winter, while the increasing daylength and temperature of spring and early summerfulfil the secondary induction requirements. Thus, the dual floral induction control system of the temperateperennial grasses provides an efficient and important mechanism for fitting their life cycles to the dramatic seasonalchanges of the high-latitude environment in which they live.

Key words: Dual floral induction, flowering control, inflorescence proliferation, photoperiod, reproduction,temperate grasses, temperature, vivipary.

I INTRODUCTIONControl of flowering time is important for the successof a plant in a given environment. Climatic factors -especially daylength and temperature - are import-ant controlling factors in this respect. The ability ofa plant to respond to such seasonal environmentalsignals represents an effective mechanism for fittingthe plant's life cycle to seasonal changes.The seasonal change in daylength - identical fromone year to the next -is ideally suited for thisregulatory purpose. Although its physiological im-portance for controlling plant development has beenwidely documented since the pioneering work ofTournois (1914) and Garner & Allard (1920), itsecological significance for adaptation of plants totheir environment is still not fully recognized. Theobvious reason for this is that this effect of daylengthis not evident until plants are transferred to anotherlatitude. Plants must be well adapted to the annualdaylength cycle at the latitudes where they exist,otherwise they would not be able to survive, flowerand reproduce there.As explained below, temperature also plays animportant role in the control of flowering time,interacting with daylength and often determiningthe daylength response. The interaction may controlboth the initial steps of the flowering process, leadingto inflorescence initiation, and the speed and di-rection of the inflorescence's further development.The highly successful grasses are no exception inthis regard. Their success is due to a variety ofmorphological and physiological characters, amongwhich are the close control of flowering time and theeffective morphological protection of vegetative aswell as reproductive shoot apices. Thus, thedeveloping inflorescence is enclosed by the leafsheaths until fully differentiated and during much ofthe culm elongation period. After heading hasoccurred, each individual floret is in turn protectedby the lemma and palea, except for the brief periodwhen they are forced apart by the swelling lodiculesto allow pollen dispersal and exposure of the stigmasto cross pollination. Highly effective vegetativemeans of reproduction of many grasses add to theirsuccess even in adverse environments.The aim of this review is to provide an overview ofhow daylength and temperature control the varioussteps in the flowering process in temperate grasses,

and how they may modify the process into avegetative reproduction system in some grasses.A comprehensive review of reproduction in grassesby Evans (1964) covers both temperate and tropicalgrasses and cereals. Readers are referred to thatreview for much of the older literature in the field.The present review will confine itself to the herbagegrasses of the Festucoideae subfamily - cultivatedand wildgrowing - of the high-latitude and tem-perate regions, emphasizing more recent work.II. INDUCTION1. TerminologyIn most temperate perennial grasses the control offlowering is complex, often stepwise (dual) and withinterchangeable effects of temperature and day-length. Induction in general can be referred to as theperception, transduction and transmittance of en-vironmental signals resulting in a change in plantdevelopmental patterns from vegetative to repro-ductive. The inductive signal must be perceived byand is mediated in the plant by a variety of poorlyunderstood physiological and biochemical processes,the nature of which is generally beyond the scope ofthis review. Nevertheless, we must clarify some oftheir components and terminology.In photoperiodic control of flowering the followingsteps or component processes can be distinguished:(i) Photoperiodic induction- the perception of thephotoperiodic signal in the leaf (Knott, 1934) via themorphogenetic pigment phytochrome (Sage, 1992),and the synthesis and transport of (a) florigenicsignal(s) to the shoot apices (meristems). (ii) Evo-cation - the processes occurring at the apex (Evans,1969 b) after arrival of the florigenic principle,leading to (iii) Initiation of floral primordia-themorphological changes of the apex by which thevarious parts of the inflorescence and flower pri-mordia are laid down. (iv) Inflorescenceand flozverdevelopment. In grasses and rosette dicots this isassociated with rapid stem elongation (heading orbolting), and (v) Anthesis.

Often, induction takes place without any im-mediately visible effects, and only becomes evidentin subsequent development. Indeed, it has beencommon to refer to induction only in this sense, asopposed to direct effects, especially of temperature(e.g. Chouard, 1960; Lang, 1965). However, present


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Flowering and reproduction n temperategrasses 349knowledge provides little basis for such a distinction.Here the term induction refers in a broad sense to allthe effects exerted by external factors in specificallychanging the direction and/or speed of plant de-velopment, whether directly or as an aftereffect.As already mentioned, flowering in many per-ennial grasses has a two step (dual) inductionrequirement. This has further confused the ter-minology. Commonly, such plants must undergo awinter influence before they will respond to thecorrect daylength and flower. Vernalization, theeffect of low temperature, was early identified withthis response (for references see Chouard, 1960;Lang, 1965). However, in a number of temperateperennial grasses SD can fully substitute for lowtemperature in this response (see below). The term'short day vernalization' has been used to refer tothis effect (e.g. Evans, 1964). Since the termvernalization is used specifically to refer to lowtemperature effects on flowering (see Chouard,1960), such confusions should be avoided. Also,because of the dual induction requirement forflowering in so many temperate grasses, the terms'induction' and 'induced' have been used to refer todifferent processes and conditions. Whereas Evans(1964) used induction to refer to the photoperiodicresponse of plants that have previously been exposedto vernalization and/or short days, Cooper (1960)and coworkers (e.g. Cooper & Calder, 1964), re-stricted the same term to the primary effect whichrenders the plant able to respond to the appropriatedaylength and flower.In his work with Dactylis glomerata, which has atypical dual induction requirement, Blondon (1972)introduced the terms primary and secondary in-duction of flowering, relating to these processes.This terminology, clearly expressing the dual natureof floral induction in such plants, has many advan-tages and has therefore been adopted by the presentauthor (Heide, 1980) and is summarized in Figure 1.

The length of this maturation or juvenile phasevaries considerably in grasses and may even beabsent in some which respond to low temperature(vernalization) as germinating seeds (Cooper, 1960;Koller & Highkin, 1960; Bommer, 1961). Vernal-ization of imbibed caryopses at 2 ?C in darkness washighly effective in primary induction of Loliumperenne, a minimum of 63 d being required, whiletreatment for up to 116 d was without effect in otherperennial grasses such as Dactylis glomerata, Festucapratensis, F. rubra and Poapratensis (Bommer, 1961).Six weeks of similar treatment was effective inHordeum bulbosum (Koller & Highkin, 1960), andoutdoor overwintering of caryopses in 'snow-boxes'resulted in heavy first-year flowering in Agropyrumintermedium, but was without effect in Phalaristuberosa (Frischknecht, 1959). In winter rye, evendeveloping caryopses can be vernalized on themother plant by low autumn temperature (Gregory& Purvis, 1938). Vernalized seeds may be dried andsown in the field without loss of effect.Although seed vernalization is possible in somegrasses like L. perenne, the rate of vernalization isgreater in seedlings (Evans, 1960a), and manygrasses can only be primary induced after somegrowth has occurred. The length of the unresponsivejuvenile phase may vary from 2 wk in Poa pratensis(Meijer, 1984), to 4 wk in Phalaris arundinacea(Heichel, Hovin & Henjum, 1980) and 5 wk inDactylis glomerata (Calder, 1963; Heide, 1987) andFestuca rubra(Meijer, 1984). In Phalaris tuberosa P.aquatica)cold treatment is effective only after severalleaves have been formed (Ketellapper, 1960).The physiological basis for the competence torespond to inductive stimuli is poorly understood. Inseed vernalization carbohydrate supply is essentialand excised embryos are only able to respond to coldif cultured in the presence of sugars (Gregory &Purvis, 1938). This agrees with the finding that seedvernalization has been successful only in grasses withrelatively large caryopses such as Lolium species(Bommer, 1961), Hordeum bulbosum (Koller &Highkin, 1960) and the winter cereals (e.g. Gregory& Purvis, 1938). The size of the endosperm carbo-hydrate pool may thus be a limiting factor. Sincejuvenility in seedlings can be related to leaf area(Calder, 1963; Heide, 1987), accumulation of photo-synthates may also be essential for the competence ofseedlings to respond. The important role of SD forprimary induction in grasses, and its perception bythe leaves, suggest that the photoperiodic sensitivityof the leaves is important. Indeed, reciprocal graftingexperiments indicated that the inability of juvenileplants of the dicotyledon species Bryophyllum andPerilla to respond to photoperiod resided in theinability of juvenile (lower) leaves to undergophotoperiodic induction and not in limitations ofevocation at the apex (Zeevaart, 1958, 1962, 1985).Similarly, it was demonstrated in the LD grass

2. Juvenility and theflower-induciblestageMany plants, including many grasses, are unable torespond to inductive conditions and to flower beforethey have reached a certain age or size, the so-called'ripeness to flower' or adult stage (e.g. Lang, 1965).

SDVegetative Primary LD Secondaryplant _ induced induced

Low temperature(LD)

Flowering(Anthesis)Figure 1. Illustration of the dual floral induction pathwayscommon in temperate perennial grasses: alternative pri-mary induction by short day or low temperature (vernal-ization), followed by secondary induction by long day.


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350 O.M.HeideLolium temulentum hat a given area of an upper leafis far more effective in induction than the same areaof lower older leaves (Evans, 1960d). However, inthe latter species it was also demonstrated thatexcised apices from plants of greater age had greatersensitivity in vitro to both a single LD given beforeexcision and to gibberellins in the medium (King,Blundell & Evans, 1993).3. Induction types and classification(a) Species zvith single LD induction. Only a fewtemperate perennial grasses have been found toflower in response to LD alone. A prominentexample is the obligatory LDP Phleum pratense(timothy) which, because of its economic import-ance, has been extensively studied and documented(Evans & Allard, 1934; Allard & Evans, 1941;Langer, 1955; Cooper, 1958; Ryle & Langer, 1963;Heide, 1982; Junttila, 1985). Other examples arePoa nemoralis (Cooper & Calder, 1964; Heide,1986 a), also an obligatory LDP, and Phippsia algidawhich initiates inflorescence primordia in both SDand LD, but has an obligatory requirement forLD for heading and flower development (Heide,1992).These grasses have no winter requirement forflowering and first-year seedlings readily flower inLD without any previous exposure to low tem-peratureor SD. In Phleumpratense, however, Langer(1956) found that tillers produced after the middle ofApril in Britain rarely produced inflorescences, andCocks (1958) showed that cultivars differed in theirability to head after summer sowing due tointeraction with temperature, high temperatureshaving an inhibitory effect on floral initiation even ifthe photoperiod is adequate (Cooper, 1958; Ryle &Langer, 1963; Heide, 1982). This effect is stronglyaugmented by even modest reductions in irradiance(Heide, 1982). The inhibitory effect of high tem-perature varies among ecotypes and appeared to berelated to the May temperature of the region oforigin (Cooper, 1958). Those adapted to northernScandinavian conditions were especially sensitive tothis high temperature/low irradiance inhibition(Cooper, 1958; Heide, 1982). Apparently, normalsummer temperatures in Britain can be inhibitory toflowering in the field (Langer, 1956; Cocks, 1958;Cooper, 1958), and the effect is enhanced by reducedlight flux in late summer (Heide, 1982). Thus,shading in the field reduced flowering in timothysignificantly (Ryle, 1961). High temperature alsolengthens -the critical photoperiod for flowering,while diurnal temperature fluctuations markedlyenhanced flowering compared with correspondingconstant temperatures (Junttila, 1985).

In Poa nemoralis and Phippsia algida no inhibitoryeffect of high temperature was observed on LDinduction of flowering which was almost unaffected

by temperatures across the range 9-21 ?C (Heide,1986 a, 1992).After exposure to a minimum number of LD

cycles flowering can occur in SD conditions in suchLD species, although at reduced rate. In Phleumpratense and Poa nemoralis a minimum of two LDcycles of 24 h is required for 50-600% flowering,while four LD cycles are needed for initiation in allplants in a sample (Ryle & Langer, 1963; Heide,1986a). More inductive cycles are needed when thephotoperiod is reduced in length (Fig. 2). In Poanemoralis more LD cycles are needed to bring aboutflowering in subsequent 8-h than in 12-h photoperiod(Heide, 1986 a), demonstrating the well-known in-hibitory effect of SD on flower development in LDP(e.g. Evans & King, 1985). In Phippsia, a single LDcycle of 24 h is enough to trigger inflorescencedevelopment and anthesis in plants which haveformed fully differentiated primordia in SD, whilefive cycles are needed for the full (saturated) response(Heide, 1992).The LD response is typical also for annual grassesof higher-latitude origin (Cooper & Calder, 1964;Evans, 1964). The 'Ceres' strain of the annualLolium temulentum of Canadian origin flowers inresponse to a single LD cycle of more than 18 hlength (Evans, 1958). This plant has been thoroughlystudied (Evans, 1969a; Evans & King, 1985) andbecause of its sensitivity and strict photoperiodicresponse it has become one of the classical modelplants for flowering studies.All lines of L. temulentum hat have been examinedare LDP, but there is variation between them bothin number of LD cycles required and in the strict-ness of the LD requirement. Most lines requiremore than one LD cycle (Evans & King, 1985), andsome are even winter annuals in which floweringis accelerated by vernalization (Cooper, 1960;Peterson, Cooper & Bendixen, 1961). In the 'Ceres'line the responsiveness to LD increases with plantage; whereas 12-d-old plants required six LDcycles for floral initiation, plants aged 17, 27 and33 d required only four, two and one LD, re-spectively (Evans, 1960 c). Other annual Loliumspecies, as well as those of other genera of thesubfamily Festucoideae which have been studied,have also proved to be LDP (Cooper &Calder, 1964;Evans, 1964).(b) Species wvith dual induction requirements. Asindicated above, most temperate, perennial grasseshave a dual induction requirement for flowering; aprimary induction requirement for low temperature(vernalization) and/or SD which enables the plant toinitiate inflorescence primordia, either directly inSD or after transition to LD, and a secondaryinduction requirement for LD allowing for culmelongation, inflorescence development and anthesis.Such plants may correctly be referred to both as


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Flowering and reproduction n temperategrasses 351

1 0 O. 2 .

C,.

10

14 12 10 8 6 4 2 0Number of cycles

Figure 2. Effects of photoperiod length and number of inductive cycles in the long day plant, Poa nemoralis.Number of heading plants out of 10 in each treatment (Heide, 1986a).

short-long-day plants and long day plants with avernalization requirement (cf. Fig. 1).

Basic to the understanding of flowering control inthe dual induction grasses, is the fact that theprimary induction effect is local, i.e. induced tillerscannot induce later-formed adjacent tillers. In otherwords, the stimulus or whatever change produced inprimary induced tillers is not transmissible to otherapices. In perennial grasses therefore the primaryinduction needs to be repeated every year, eachindividual tiller having a biennial and monocarpiclife cycle.Temperature and daylength are highly interactivein the primary induction process. In most species thegeneral pattern is that the plants become day neutralat low temperatures (0-6 ?C), and under theseconditions primary induction is identical with thecommon vernalization response (e.g. Chouard, 1960;Lang, 1965). However, as temperature rises, primaryinduction will occur in SD only, until a certainthreshold temperature level is reached, above whichprimary induction cannot take place regardless of thephotoperiod and duration of treatment. This dy-namic interaction of temperature, photoperiod andexposure time is well demonstrated on Poa pratensis(see Fig. 3; Lindsley & Peterson, 1964; Heide,1980). Although SD and low temperature areindependently- able to bring about the primaryinduction response, their effects are additive whenapplied sequentially, especially if the SD treatmentis applied first (Heide, 1980, 1988a).Critical temperatures and daylengths, as well asthe critical duration of exposure for primary in-duction vary greatly among the grass species (Table

1), and may also vary much among ecotypes ofdifferent geographic origin within the same species(e.g. H'abjorg, 1978; Heide, 1980,1988 a). Generally,ecotypes from high latitudes and especially arctic-alpine ones, have wider temperature and daylengthlimits and require fewer inductive cycles for primaryinduction than their low-latitude and maritimecounterparts.Among the species with the least requirements forprimary induction are arctic-alpine Poa species andecotypes (Heide, 1980, 1989 a, b) and Alopecuruspratensis (Heide, 1986b). In high-arctic ecotypes ofPoa alpina and P. alpigena from Svalbard, 3-4 wkexposure to 3-6 ?C in 8 h photoperiods was sufficientfor primary induction (Heide, 1989 a), while in high-latitude ecotypes of Poa pratensis and Alopecuruspratensis, 6 wk at the same conditions were required(Heide, 1980, 1986b). With extended exposure time,induction was obtained in these species at tempera-tures up to 12 ?C in 24-h photoperiod and up to18 ?C in short days of less than 12 h duration (Heide,1986b, 1989a).An interesting point is, however, that the high-arctic Poa species from Svalbard which hardly everexperience short days in a non-frozen condition,have retained such a strong SD response. This wasfound also in Cerastium regelii, a high-arctic dicotspecies from Svalbard (Heide, Pedersen & Dahl,1990). Such a SD response is apparently of littleadaptive value in the high-arctic environment and isprobably a relict character (with no negative fitnesseffect) inherited from ancestors at lower latitudes.Another species in this group is Bromus inermisinwhich primary induction takes place in SD at


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352 0. M. Heide

6 wk10 10

5 -5

8 wk10SD ---G 10

CU

10 _U wk10 - -- ~~~~~~~~~~~~~~~~~~

5 5

3 6 9 12 3 6 9 12Temperature (IC)

Figure 3. Interaction of temperature, photoperiod and exposure time in primary induction of Poa pratensis cv.Holt. Five-wk-old seedlings were exposed to photoperiods of 10 (a), 16 (0) and 24 (L1) h at temperaturesranging from 3 to 12 'C for 6, 8 or 10 wk. Ordinates indicate number of flowering plants out of 10 and meannumber of panicles in each treatment in subsequent 24-h photoperiod at 21 'C (Heide, 1980, withpermission).

temperatures ranging from 6 to 24 ?C with anoptimum response at 15-21 ?C (Heide, 1984). Atsuch optimal temperatures 4-6 wk of SD treatmentare optimal for primary induction, whereas noinduction takes place in 24-h LD at 3 ?C even with16 wk of treatment. This species, unlike most otherperennial temperate grasses, appears to have aspecific SD requirement for primary inductionwhich cannot be replaced by low temperaturevernalization in LD (cf. Fig. 1). Critical photoperiodsfor primary induction at 15 and 24 ?C, respectively,were 13 5 and 12 h in the North-American cv.Manchar, and 14 5 and 13 h in the Norwegian cv.

Lofar. The latter also had somewhat lower tem-perature optima (Heide, 1984, cf. Fig. 4).An intermediate primary induction requirement isfound in Dactylis glomerata (Heide, 1987), Festucavivipara and F. ovina (Heide, 1988a), and Phleumalpinum (Heide, 1990 a). These species require8-12 wk of exposure to optimal conditions forprimary induction, but they vary considerably withrespect to the range of inductive conditions. In threeScandinavian cultivars of D. glomeratafull inductionwas obtained at temperatures of up to 18 ?C in 8-hSD (10 wk exposure) and 5000 flowering even at21 'C. In 24-h LD, however, induction was re-


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Flowering and reproduction n temperategrasses 353Table 1. Primary induction requirements for flowering in some temperateperennial grasses

In short days (< 12 h) In long days (> 16 h)Temperature Exposure Temperature ExposureSpecies (OC) (wk) (OC) (wk)

Poa alpina 3-18 4-10 3-15 6-10Poa alpigena 3-18 4-8 3-12 6-10Poa pratensis 3-18 6-10 3-12 8-12Alopecurus pratensis 6-18 6 6-15 6-8Bromus inermis 6-24 4-6 n.i. n.i.Dactylis glomerata 9-21 8-10 0-3 > 20Phleum alpinum 3-15 9-12 3-12 12-14Festuca vivipara 3-15 10-18 3-6 10-18Agrostis capillaris 3-12 15 3-6 15Phalaris arundinacea 3-15 12-18 n.i. n.i.Loliumperenne 3-? 12-16 3-? 12-16Festuca pratensis 3-15 16-20 3-12 18-20Festuca rubra 6-15 12-20 3-12 20

Ranges of exposure time requirements indicate variation with temperatureand geographic origin of ecotype/cultivar.n.i., no induction.

100 240

Primary

~'500 Second-ary nductionLL

8 12 16 20 24 812 16 20 24Photoperiod (h)Figure 4. Photoperiodic requirements for primary and secondary induction of flowering at 15 and 24 ?C in twocultivars of Bromus inermis (Heide, 1984, with permission).

stricted to 3 ?C and required more than 20 wk ofexposure. These results confirm the conclusions ofCalder (1963, 1964) and Broue & Nicholls (1973)that SD alone is sufficient for primary induction inD. glomerata, and that at no stage of development isany cold needed for flowering in this species as hasbeen claimed in several reports (for references seeHeide, 1987). Blondon (1972) found that even hightemperature (27 ?C) at high light intensities couldbring about primary induction in a clone used byhim. A point of interest is that the alpine timothy(Phleum alpinum) has a dual induction requirement,while the cultivated hexaploid timothy requires LDonly for flowering. The results by Cooper & Calder(1964) indicate that the closely related diploid P.

pratensesubsp. bertelonii(syn. P. nodosum)resemblesP. alpinum in this respect. Thus, even taxonomicallyclosely related grasses may differ much in their floralinduction requirements.The most extreme primary induction require-ments are found in the genus Festuca (Bean, 1970).In three Scandinavian cultivars of F. pratense16-20 wk at 6 ?C in 10 h photoperiods were neededfor 'saturation' of primary induction (Heide, 1988b).Whereas 9 ?C was optimal (and 12 ?C effective), forinduction in 8-h SD, temperatures of 3-6 ?C wererequired for induction in continuous light. Similarresults were obtained in Norwegian F. rubra eco-types, although with a larger variation among ecotypes(Heide, 1990b). Thus, while an ecotype from North


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354 O. M. HeideNorway reached full induction within 15 wk ofexposure to 6 ?C/SD and with 21 wk at 6 ?C/LD(24 h), an ecotype from South Norway needed 21 wkfor the same response at 6 ?C/SD and had onlymarginal induction with 21 wk at 6 ?C/LD. Thevariable response may at least in part be due to thetaxonomic complexity of this taxon. As with F.pratense, 9 ?C was the optimal temperature for SDinduction in all F. rubra ecotypes (Heide, 1990b).Similar extreme primary induction requirementswere demonstrated in F. arundinacea(Bean, 1970).To this group belongs also the late-flowering(higher-latitude) types of Lolium perenne. The pri-mary induction requirements vary greatly within thespecies, and plants of Mediterranean origin mayeven have none (Cooper, 1960). In the late-floweringBritish strain S.23 Evans (1960 a, b) found that about12 wk of SD treatment at 4 ?C were required for fullresponse, using 16 wk as a standard 'vernalization'treatment. The rate of primary induction increasedwith increase in temperature from 4 to 10 ?C (Evans,1960a). Details on temperature ranges for inductionin SD and LD are, however, missing for thiseconomically very important species.The linkage between primary induction require-ments and perenniality has been beautifully demon-strated in the genus Lolium (Cooper, 1960; Evans,1960 a). Thus, the induction requirement variesfrom obligatory and large in L. perenne throughfacultative and intermediate in hybrids of L.perennex L. multiflorumand in biennial types of L.multiflorum Italian ryegrass), slight in winter annualtypes of L. multiflorumand L. rigidum (Wimmeraryegrass), to none in the typical summer annualstrains of L. multiflorum(Westerwalds ryegrass) andL. temulentum(Cooper, 1960; Evans, 1960a).Large primary induction requirements are alsofound in Phalaris arundinaceaand Agrostis capillaris(syn. A. tenuis). In the P. arundinacea cultivars'Vantage' and 'Rise' 12-15 wk at 6 ?C in 8 hphotoperiods were required for full response(Heichel et al., 1980). Photoperiods of 16 h at thesame temperature were less effective. While theresults with 'Vantage' were confirmed, Norwegiancultivars and breeding lines of P. arundinacearequired up to 18 wk at 6-9 ?C/8 h photoperiod forfull induction (Heide, unpublished results). In SDprimary induction was effective over the 3-12 ?Ctemperature range (somewhat less at 15 ?C), with anoptimum at 9 ?C. In 24-h photoperiods inductionwas virtually absent at these temperatures. Theseresponses are in contrast to those of Phalaris aquatica(syn. P. tuberosa)which is equally well vernalized inshort and long days (Cooper & McWilliam, 1966;McWilliam, 1968) and has a much shorter exposurerequirement (Ketellapper, 1960).

In experiments with Norwegian ecotypes ofAgrostis capillaris Karlsen (1988) found that at least15 wk of exposure were required for full primary

induction response, but only temperatures of 12 ?Cor below and daylengths of 8 or 16 h were highlyeffective. At 3 and 6 ?C induction took place even in24-h photoperiod. Again, 9 ?C was the most effectivetemperature in SD; this seems to be the case for anumber of temperate grasses (Heide, 1990b). Pre-liminary experiments with Deschampsia species (D.caespitosa, D. alpina, D. flexuosa) indicate that theyall fall into this category with an extreme primaryinduction requirement (Heide, unpublished results).The extent of the primary induction requirementis also reflected in the time and progress of floralinitiation of the grasses in the field. In an extensivestudy conducted by Bommer (1959) in Germany,Alopecuruspratensiswas the earliest species to initiatefloral primordia in the autumn followed by Antho-xanthum odoratum whereas Phalaris arundinacea,Agrostis alba, Lolium perenneand the Festuca specieswere among the latest, with initiation in the spring.However, in many dual induction grasses nomorphological changes take place at the apex duringSD primary induction. In other words, primaryinduction alone does not trigger floral initiation,which only takes place after a shift from short to longdays. This has been demonstrated in one group ofgrasses including Lolium perenne (Evans, 1960 a),Bromusinermis, Dactylis glomerata, Festuca pratensisand F. rubra, Phleum alpinum (Heide, 1984, 1987,1988b, 1990a, b) and Phalaris arundinacea (Heide,unpublished). Cultivars within a species may, how-ever, differ in this respect as Niemeliiinen (1990),found that in Dactylis glomerata the Finnish cv.Haka initiated inflorescence primordia in bothnatural and artificial SD. On the other hand,cultivars of F. pratensis (Heide, 1988b) and P.arundinacea did not initiate inflorescence primordiain SD at 6-9 ?C even after 27 and 31 wk of exposure,respectively, whereas initiation was immediate aftertransfer to LD. With such over-induction someapices die and the number of developing inflores-cences is actually reduced.In contrast to this is the completion of inflorescenceinitiation and differentiation which takes placeduring SD induction in another group of northerngrasses with a relatively small primary inductionrequirement. This is the case with northern ecotypesof Poa pratensis (Habjorg, 1979; Heide, 1980) andother arctic-alpine Poa species (Heide, 1989 a), aswell as Alopecuruspratensis(Heide, 1986b), Hordeumbulbosum (Koller & Highkin, 1960) and certaincultivars of winter wheat (Evans, 1987). In all thesespecies the complete inflorescence primordia, up tothe terminal spikelet, are formed while the plants arestill in SD (stages 5-6, Jeater, 1956). Thus, althoughthe environmental requirements for flowering aresimilar, the actual control point in the differentiationcycle is different in those two groups of grasses.

In their high-latitude environment the latter groupof grasses initiate floral primordia in the autumn, a


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Flowering and reproduction n temperategrasses 355feature which has also been demonstrated in Alaskangrasses (Hodgson, 1966). This seems to be animportant adaptive strategy to a short and coolgrowing season (Heide, 1985). In Poa pratensis amarked latitudinally determined ecotypic differen-tiation is found in this character (Habjbrg, 1979;Heide, 1980). Similar differences are found amongFestuca vivipara ecotypes (Heide, 1988a). Althoughautumn initiation clearly is associated with a smallinduction requirement (Bommer, 1959; Heide, 1980,1989a), it is not a direct result of it since a transitionfrom SD to LD is clearly required for floral initiationin many species and ecotypes.In nearly all grasses with dual induction require-ments, with the exception of Bromus inermis(Heide,1984) and possibly Phalaris arundinacea(see above),SD and low temperature (vernalization) are inter-changeable in their effects and will independentlyof each other bring about the primary inductionresponse (cf. Fig. 1). This has also been demonstratedin winter annuals like winter rye (Purvis & Gregory,1937) and certain cultivars of winter wheat (Evans,1987), as well as in the biennial and perennial dicotsCampanula medium (Wellensiek, 1985), Scabiosasuccisa(Chouard, 1960) and Cerastiumregelii (Heideet al., 1990).This raises the question of the specificity of thevernalization and photoperiodic responses (Heide,1986b, 1987, 1988b; Evans, 1987). Since the photo-periodic signals are perceived by the leaves (Knott,1934; Lang, 1965) while vernalizing temperaturesact directly on the shoot apex (Purvis, 1940; Lang,1965), it has been assumed that photoperiodism andvernalization are basically different phenomena. Yet,their effect in primary induction is the same; bothenabling the plants to respond to and flower insubsequent LD, suggesting that at least their endproducts are similar or even identical. However, asdiscussed by Evans (1987), several lines of evidenceindicate the utilization of different pathways by thetwo induction processes.It may be argued that these examples are onlyspecial cases of the well-known interaction ofphotoperiod and temperature in the induction offlowering, whereby a number of SDP become dayneutral at lower temperatures (see e.g. Lang, 1965;Bernier, Kinet & Sachs, 1981). In particular, whenthe temperature range for primary induction in LDis as wide as in Alopecuruspratensis and some Poaspecies (Heide, 1986b, 1989 a), it is difficult to arguefor two entirely different processes in LD and SD. Isthis effect of low temperature merely to render theplants insensitive to photoperiod in the primaryinduction process? The fact that the SD responsealways is reduced in effectiveness at the lowertemperatures which are optimal for vernalizationresponse (0-6 ?C) lends support to this possibility(cf. Cooper, 1960). Furthermore, it should beobserved that when primary induction takes place at

intermediate temperatures in LD as in some of theabove examples (cf. Fig. 1), there is in fact no dualinduction. In LD at such temperatures induction,initiation, heading and anthesis proceed uninter-ruptedly in one continuous sequence. Induction maythen be considered a normal LD response similar tothat of Phleum pratense. Such diverse responsesmake response-type classification according to class-ical terminology rather complicated and suggeststhat the various responses have much in commonand simply represent modifications of the sameoverall multiple flowering control mechanism (cf.Evans, 1969; Bernier, 1988).

After the primary induction requirements havebeen met, whether by short days or low temperature(vernalization), secondary induction by long days isnecessary for normal flowering in the dual inductiongrasses. The response of Bromus inermis presented inFigure 4 is a typical example. With some notableexceptions discussed above, floral initiation is trig-gered by the transition from short to long days. Inmost species this LD requirement is obligatory forinflorescence development, but in some arctic-alpinespecies and ecotypes heading and anthesis may takeplace slowly, also in SD, especially at highertemperatures. Examples are northern ecotypes ofPoa pratensis and other northern Poa species,Alopecurus pratensis, Festuca ovina and Phleumalpinum (Heide, 1980, 1989 a, 1986 b, 1988 a, 1990 a).With the exception of Phleum alpinum these are thesame grasses which initiate floral primordia whilestill in SD (see above).

Critical photoperiods for secondary inductionrange from 9-10 h in Mediterranean ecotypes, tomore than 16 h. Usually, ecotypes of high latitudeorigin have the longest critical and optimal photo-periods (Cooper, 1960; Pringle, Elliot & Degenhardt,1975; Habjorg, 1978; Heide, 1984, 1987, 1988b;Karlsen, 1988), and require the highest number ofLD cycles for secondary induction (Heide, 1984,1987, 1988b).

The temperature effect on secondary inductiondiffers between species. In those species forminginflorescence primordia during SD primary induc-tion high temperature (21-24 ?C) can to some extentsubstitute for the LD requirement of secondaryinduction (Heide, 1980, 1986b, 1988a, 1989a),whereas the species in which initiation requires atransition from SD to LD show the oppositeresponse, the critical photoperiod will increase withthe temperature (Evans, 1964; Heide, 1984, Fig. 4).Devernalization by high temperature will occur inthese species if primary induction is marginal orincomplete (Evans, 1964; Heide, 1988b).

The degree of primary induction is also of greatimportance for the secondary induction requirement.The more complete the primary induction, the less isthe critical secondary induction requirement, i.e.fewer LD cycles or shorter photoperiods can trigger


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356 0. M. Heidesecondary induction (Evans, 1960a; Peterson el al.,1961). This suggests that primary induction in someway increases the responsiveness of the shoot apex tosubstances translocated from the leaves in LDconditions (Evans, 1964). It is also in agreement withthe classical vernalization concept that the role ofvernalization is to render the plants responsive tosubsequent photoperiodic induction (e.g. Lang,1965).

The critical number of 24-h LD cycles re-quired for secondary induction in fully primary-induced plants of many grasses ranges from aboutfour to eight cycles, whereas 12-16 LD cycles arerequired for the full response (Evans, 1960b; Heide,1984, 1987, 1989a, b, 1990b). Even in those arctic-alpine species in which flower development mayalso take place in 8-h SD, there is an increasingresponse with up to 12-16 LD cycles (Heide, 1989 a,1990a).

Low light intensities are photoperiodically effec-tive and, as in other LD plants, a high proportion offar-red light is optimal for day-length extension(Vince-Prue, 1975). For all the grasses studied bythe present author about 2,umol m-2 s-1 (400-700 nmrange) supplied by incandescent lamps has beenadequate for extension of 8-10 h of daylight or high-intensity fluorescent light. About 13 ,mol m-2 s-1was sufficient for daylength extension in Phleumpratense (Cooper, 1958), and about 333,mol m-2 s-1in Dactylis glomerata and species of Lolium (Sprague,1948; Cooper, 1956). Night interruptions near themiddle of the dark period have been effective in LDsecondary induction in several dual induction grasses(Sprague, 1948). Our experience is, however, thatsuch night breaks should last for at least 1-2 h to befully effective in the grasses (Heide, Bush & Evans,1985).

In addition to the main control by photoperiodand temperature, both primary and secondary in-duction are modified and may be limited by otherexternal factors. Notable in this respect is the effectof photon flux density (pfd). Thus, primary in-duction, both in the classical vernalization sense andby SD, is highly dependent on adequate lightconditions and a favourable carbohydrate status ofthe plants to be effective (see Lang, 1965; Bernier etal., 1981). Experiments in artificial light conditionsmust take this into account. The need for a highcarbohydrate/energy status was clearly demon-strated by dramatic reductions of flowering causedby moderate defoliation before onset of primaryinduction under greenhouse conditions in both Poapratensis-(Peterson & Loomis, 1949) and Phalarisarundinacea (Heichel et al., 1980). Autumn mowingalso reduced seed yields in first year seed productionleys of Poa pratensis, but was beneficial in older leys,probably by improving the light conditions for thenew tillers in the dense older stands (Aamlid, 1993).Reduction of natural light conditions in the field also

reduced flowering in the single-induction LDPPhleum pratense (Ryle, 1961).

The role of sugars in floral induction has been amatter of contention (e.g. Bernier, 1988). However,a careful recent study of photoperiodic and photo-synthetic effects on apical sugar content in Loliumtemulentum (King & Evans, 1991), revealed thatphotoperiodic time measurement and induction inthe leaves as well as evocation at the apex wereindependent of and unaffected by pfd and sucroseavailability at the apex. On the other hand, inflores-cence development was highly responsive to highsugar availability (King & Evans, 1991). Therefore,the effects of defoliation and low pfd on floralinduction and evocation in grasses seem to be non-specific, a favourable carbohydrate status being aprerequisite for normal photoperiodic and thermalresponses and for production of a high number ofresponsive tillers. Also the growth and rate ofdevelopment of induced tillers increase under highpfd (King & Evans, 1991).

Nitrogenous fertilizers applied before the onset ofprimary induction increase the number of inflores-cences in several dual induction grasses (Evans &Wilsie, 1946; Sprague, 1948; Peterson & Loomis,1949; Newell, 1951; Calder & Cooper, 1961;Aamlid, 1993). Again, the effect is mainly indirectthrough an increase in the number and vigour ofinduceable tillers in the autumn (Meijer & Vreeke,1988; Aamlid, 1993).

III. INFLORESCENCE DEVELOPMENTDevelopment of fully differentiated inflorescenceprimordia is essentially a growth process, and assuch, highly influenced by temperature. Time toheading decreases with increasing temperature dur-ing this stage, at least up to about 25 'C. Never-theless, culm height, panicle size and usually alsofinal inflorescence number will be largest at relativelylow temperatures (12-15 ?C).

In all high-latitude perennial grasses inflorescencedevelopment is also strongly stimulated by longdays. Although heading may take place in 8-h SD insome species (see above), the development is slow, ahigh proportion of the primordia abort, and thosedeveloping are stunted with very short culms (Heide,1980, 1986b, 1988a, 1989a, 1990a). The com-bination of SD and cool temperatures during theperiod following completion of primary induction isstrongly inhibitory to culm elongation. Furthermore,this inhibitory effect is irreversible and cannot beovercome by subsequent LD conditions (Heide,1980). Thus, in Poa pratensis cv. Holt, intercalationof a 6-wk SD period between primary induction for10 wk. at 3 ?C/24 h photoperiod and flower de-velopment at 21 ?C/24 h reduced final culm height toonly 300?o of that of plants which went directly intoLD/high temperature. However, when the same


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Flowering and reproduction n temperategrasses 357treatments were given in the reverse order SD werehighly stimulatory. Inhibition was maximal at in-termediate temperature (12 ?C) and increased sharp-ly at daylengths below 16 h (Heide, 1980). Theseeffects are very pronounced also under field condi-tions when northern ecotypes of P. pratensis aretransferred to lower latitudes where SD conditionsprevail in early spring, particularly in years withearly snowmelt (Habj6rg, 1978, 1979; Heide, 1980).This has important implications for choice of areafor commercial grass seed production (Heide, 1980;Aamlid, 1993).The intensity of secondary induction in dualinduction grasses also has a strong effect on rate ofinflorescence development. The more inductivecycles given, and the more favourable their day-length, the greater is the rate of subsequent inflores-cence development (Evans, 1960b; Heide, 1980,1984, 1986b, 1987, 1988 a, b, 1989 a, 1990 a, b, 1992).The same applies to single induction LD grasses(Evans, 1958; Heide, 1982, 1986a) and the rate ofinflorescence development provides a sensitive indexof the intensity of induction in both groups (Evans,1958, 1960b). Under marginal or unfavourabledaylength conditions primordia may undergo im-perfect development resulting in vegetative pro-liferation of the inflorescences.IV. INFLORESCENCE PROLIFERATIONAsexual reproduction is widespread and importantin many temperate and high-latitude grasses. Inmany arctic-alpine Poa species three different asexualmechanisms are often at work within the samepopulation, namely vegetative spread by rhizomes,inflorescence proliferation ('vivipary'), and apos-pory. Combinations of these with the various asexualbreeding strategies result in the complex geneticstructures of many grass populations. Richards(1990) has reviewed the diversity of breeding systemsin grasses and their implications for the geneticarchitecture of grass populations. The environmentalinfluence on and regulation of these mechanisms willbe highlighted here.Application of the term vivipary to proliferation ofspikelets has led to some confusion as has beenthoroughly discussed by Latting (1972). In the strictsense the term is applied to mean germination ofseeds while still attached to the parent plant (Arber,1934; Hartman & Kester, 1975). Here it is used inthe sense of Latting (1972) as 'the development ofvegetative shoots among the reproductive organs'.According to Latting (1972) two types of meristemsare involved in the proliferation process, the apicalmeristem of the spikelet and the intercalarymeristemof the lemma. These meristems are activated andgive rise to leafy organs and plantlets, while thesexual parts usually abort. As pointed out by Arber(1934) and Evans (1964), what is essentially an

24

abnormality or error of development in the habituallynon-viviparous (ephemeral) grasses is the normalsituation and has become genetically assimilated inviviparous species to the extent that it is referred toas a form of apomixis (Stebbins, 1941).It is often observed that habitually seminiferousgrasses develop viviparous inflorescences whendeveloping in late summer and autumn (for earlyreferences, see Evans, 1964). Numerous experimen-tal studies indicate that this is due to the decreasingphotoperiod and temperature late in the season(Wycherley, 1954; Evans, 1960b; Junttila, 1985;Heide 1986a, 1987, 1988a, 1989a, 1990b). Suchephemeral vivipary occurs in single induction LDgrasses such as Phleum pratense (Nielsen, 1941;Langer & Ryle, 1958; Junttila, 1985) and Poanemoralis (Heide, 1989a), as well as in many dualinduction grasses (see Evans, 1964; Heide, 1989 a).The most important environmental regulatory factoris daylength. Marginal LD induction, both in theform of marginally inductive photoperiods (Junttila,1985; Heide, 1988a), and of a marginal number offully inductive LD cycles (Wycherley, 1954; Evans,1960b; Junttila, 1985; Heide, 1986a, 1987, 1988a,1989 a, 1990b), commonly induces inflorescenceproliferation in habitually seminiferous temperategrasses. The effect can be modified by temperature.For example in P. pratense, in which the criticalphotoperiod increases with increasing temperature(Heide, 1982; Junttila, 1985) the proportion ofproliferating inflorescences increased when the tem-perature was increased under marginal photoperiodicconditions (Junttila, 1985). In other species in whichLD induction is most effective at high temperatures,low temperatures during LD induction have thesame effect (Youngner, 1960; Heide, 1988a).Similar 'vegetative inflorescence' phenomena areknown also in other plants with different environ-mental requirements for flowering, e.g. the SD plantKalanchoi blossfeldiana (Harder, 1953), the lowtemperature-dependent Freesia x hybrida (Heide,1965), and the long-short-day plant Bryophyllumdaigremontianum(Zeevaart, 1985). In all cases pro-liferation is associated with marginal floral induc-tion; in the case of Bryophyllum proliferation wasproduced also by marginal induction by gibberellinin SD. It can thus be concluded that the ephemeralvivipary in habitually seminiferous grasses as well asother forms of 'vegetative inflorescence' formationare the results of marginal or incomplete floralinduction. In extreme cases a complete reversal tovegetative conditions may occur, leafy shoots beingformed at the top and/or nodes of the culms insteadof inflorescences (cf. Karlsen, 1988).On the other hand, a large proportion of normalflowering was obtained in habitually viviparousforms of Festuca vivipara, Poa alpina and P. alpigenaby optimal floral induction, both primary andsecondary (Heide, 1988a, 1989a). Both daylength

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358 0. M. Heideand temperature effects on flowering were demnon-strated in all species. A complete shift to normalflowering was not observed in any species, however.That such flowers may be reproductively functionalwas suggested by positive pollen staining tests in F.vivipara (Heide, 1988a) and Salvesen (1986) foundvarying degrees of seed production in tetraploidpopulations of this species after open pollination inan experimental garden.Such findings clearly demonstrate that sexuality isby no means entirely suppressed even in the'obligatory' viviparous species, but that it is underenvironmental influence, as suggested by Evans(1964). By these mechanisms, viviparous species canbenefit from the advantage of a highly efficientvegetative reproduction method under marginalclimates in arctic-alpine areas, and still retain thepossibility of genetic recombination allowing forevolution and adaptation to a changing environment.With such an 'optimal versatility' it is understand-able that vivipary has been such a common andsuccessful adaptation to arctic-alpine environments.Of special significance is that a condition such as SDwhich favours vivipary is also seasonally linked to atemperature regime that makes this form of re-production of special advantage. Long days on theother hand, favouring flowering, are linked to theearly part of the growing season when the potentialfor completion of seed development and maturationwould be best (Heide, 1988a).The experimental results with both seminiferousand viviparous species agree with the hypothesis ofWycherley (1954), that a greater amount or con-centration of flowering hormone(s) is needed fornormal flowering than for viviparous proliferation.In this connection it should be noticed that inductionand heading in viviparous species was controlled inthe same way and had the same dual inductionrequirements as in their normal flowering counter-parts (Heide, 1988a, 1989a).Induction of proliferation by growth substanceshas also been demonstrated. Spraying with auxin-type herbicides induced proliferation in severalgrasses (Jeater, 1958), and cytokinin was veryeffective in inducing vivipary in aseptically cultivatedinflorescence primordia and inflorescences of Phleumpratense (Junttila, 1985). The auxin 2,4-D, on theother hand, stimulated root formation at low concen-trations and at higher concentrations it inducedcallus growth, thus preventing spikelet development(Junttila, 1985).

It can sometimes be observed that miniatureviviparous plantlets of obligatory viviparous speciesmay head and develop a new generation of proli-ferated inflorescences while still attached to theirparent plants. However, such development could notbe induced in detached viviparous plantlets of F.vivipara, even by extended primary induction treat-ments by low temperature and SD, but plantlets

remained vegetative when rooted and grown insubsequent LD (Heide, 1988a). Apparently, suchplantlets are in a juvenile state and only becomereceptive to primary induction after root formationand production of some growth, whereas attachedplantlets respond to hormonal stimuli produced bythe parent plant. Such observations support thehypothesis that the limitations of juvenile plantsreside mainly in their inability to produce floweringhormone(s) and not in an ability to respond to suchstimuli (cf. Zeevaart, 1962).V. THE ROLE OF GIBBERELLINThe effects of gibberellin (GA) on flowering havebeen extensively reviewed by Lang (1965), Zeevaart(1978) and Pharis & King (1985). The responses ofvarious plant groups and species are both diverse andcomplex, but some general features are apparent: (a)GA can substitute for LD in many herbaceous LDPand in the LSDP Bryophyllum daigremontianumwhen grown in SD (Zeevaart, 1985). (b) GA can alsosubstitute for low temperature (vernalization) inmany cold-requiring plants (Lang, 1965). (c) In SDPGA is usually ineffective or even inhibitory, althoughthere are exceptions like Chrysanthemum,Impatiensand Pharbitis (Pharis & King, 1985). (d) Inhibitors ofgibberellin biosynthesis (growth retardants) mayinhibit LD induction and exogenous GA mayovercome this inhibition.In the annual LD grass Lolium temulentumexogenous GA applied to leaves or to the apexinduces flowering under non-inductive SD condi-tions (Evans, 1969a). Furthermore, apices excisedfrom 7-8-wk-old plants grown at high irradiances inSD could undergo inflorescence differentiation invitro when GA was provided in the medium (King etal. 1993). The order of effectiveness of gibberellinswas 2,2-dimethyl-GA4> GA5> GA3> GA1, thesame ranking as found for intact plants (Evans et al.,1990). Applications of GA3 to leaves before apexexcision could substitute for GA in the medium, andapices from plants given one LD reached high floralscores even when there was no GA in the medium.The presence of GA in the medium was not requireduntil 4-6 d after excision from plants given one LD,and appeared to be necessary for differentiationbeyond the spikelet primordia stage (King et al.,1993). On the basis of these results the authorsconclude that at present it is not possible to tellwhether the LD stimulus to flowering in L. temu-lentum actually is a GA, or whether a GA is acomponent of the stimulus or is acting synergisticallywith it (King et al., 1993).In the dual induction grasses Poa pratensis cv.Holt and Bromus inermis cv. Manchar, application ofGA3 during primary induction was strongly in-hibitory to flowering (Heide, Bush & Evans, 1987).In P. pratensis weekly spraying with 1 x 10-4 M GA3


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Flowering and reproduction n temperategrasses 359during SD treatment at 9 ?C for 10 wk completely'suppressed primary induction. Lower concentrationsdown to 1 x 10' M also caused significant inhibition,especially with shorter induction periods. In Bromusinermis the same GA3 treatments inhibited primaryinduction in plants exposed to SD at 18 ?C for up to6 wk (Heide et al., 1987). Similar inhibitory effectswere obtained with Arrhenatherumelatius (Bommer,1964). Although the concentrations applied werehigh, they may not have exceeded physiologicalconcentrations which reach as high as 3 x 10-3 M inthe shoot apex of Lolium temulentum(Pharis et al.,1987).

Since both GA and non-inductive LD conditionsgreatly stimulate elongation in these and othertemperate grasses (Hay & Heide, 1983; Heide et al.,1985; Hay, 1990), the degree of primary induction isnegatively correlated with plant height (leaf sheathand blade length). The GA biosynthesis inhibitorCCC which effectively reduces leaf growth of thesegrasses (e.g. Heide et al., 1985) also enhancesprimary induction of flowering especially undermarginal conditions (Buettner, Ensign & Boe, 1976;Heide, unpublished results). Also, experiments inNorway with autumn application of CCC have givenpromising seed yield results in seed production leysof Bromus inermis, a species which tends to getmarginal SD primary induction in high latitudeenvironments (Klebesadel, 1970; Heide, 1984).These results and others relating to the daylengthcontrol of important steps in the GA interconversionpathway (Gilmour et al. 1986; Graebe, 1987) arecompatible with the hypothesis that the SD primaryinduction in dual induction grasses is mediated by areduction in the level of active gibberellins. In otherwords, the effect of SD may be to remove theinhibitory effect of LD (and GA) in a way similar tothat found in strawberry (Guttridge, 1985).Unlike the situation in Lolium temulentumwhereGA can substitute for LD, GA3 applied to primaryinduced B. inermis plants in SD did not substitutefor a transition to LD as expected (Heide et al.,1987). There is thus no parallel in this SLDP to thesituation in the LSDP Bryophyllum which respondsto GA application in SD with normal floral inductionand development (Zeevaart, 1985). Nor could GA3applied to primary-induced Poa pratensis plants inSD with fully differentiated inflorescence primordiasubstitute for LD and trigger culm elongation andinflorescence development (Heide et al., 1987).Although leaf elongation was strongly stimulated,heading and inflorescence development were not. Infact, a large proportion of the primordia aborted incontinuous SD whether GA was applied or not.Possible explanations for this unexpected resultmight be increased competition between inflores-cence and leaf growth due to nutrient diversion tothe GA-sprayed leaves, or that specific gibberellinsare required for flowering (Pharis et al., 1987).

However, there is accumulating evidence for im-portant roles of gibberellin in the control of floweringin both LD and dual induction grasses. Unravellingthese effects is important for the understanding ofthe control of flowering in general.VI. SYNCHRONIZATION WITH SEASONALCLIMATIC CHANGESAn inevitable consequence of the dual floral in-duction requirement of most temperate grasses andthe monocarpic nature of individual tillers is thateach tiller has a biennial life cycle. Therefore, thepotential of these grasses for flowering and seedproduction in any year is determined by the size ofthe population of receptive tillers at the time whenthe combination of temperature and daylengthbecomes favourable for primary induction in theautumn of the previous year. This is the physio-logical basis for the important and widely recognizedpractice of renewing seed production fields byburning or mowing and application of nitrogenfertilizers in late summer and autumn.At high latitudes, where the onset of SD is late andfrost comes early in the autumn, the frost-free SDprimary induction period will necessarily be short ormay even be absent (see Fig. 5). Under suchconditions the alternative LD/low temperature by-pass is of particular importance for facilitation ofprimary induction (Fig. 1). Species and ecotypesadapted to such conditions, e.g. arctic-alpine Poaspecies and ecotypes (Heide, 1980, 1989 a), havewide temperature and daylength limits for primaryinduction as well as a relatively rapid response toinductive conditions (small primary induction re-quirement). In such high-latitude grasses, primaryinduction requirements are readily met even in theabsence of SD at non-freezing temperatures. On theother hand, species adapted to lower latitudes,having a more strict SD requirement for primaryinduction, e.g. Bromus inermis(Heide, 1984) will getinadequate primary induction under high-latitudeconditions as illustrated in Figure 5. These relationshave important implications for localization ofcommercial grass seed production (Heide, 1980,1990; Aamlid, 1993). In Norway the primaryinduction period is often marginal and limiting forseed yield in grasses with predominantly SD in-duction (e.g. Bromusinermisand Dactylis glomerata,Heide, 1984, 1987) especially because of the rela-tively high temperature optimum for the SD re-sponse. This also appears to be the main reason forvery low seed yields of Bromus inermis in Alaska(Hodgson, 1966; Klebesadel, 1970).A further adaptation to the high-latitude en-vironment is the initiation of inflorescence primordiain the autumn among arctic-alpine grasses (e.g.Hodgson, 1966; Habjorg, 1979; Heide, 1980,1989 a). This facilitates early heading and flowering

24-2


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360 0. M. Heide

20 DelftBromus inermis a Oshlo

/ / I TromsoCU 1E 1~ Poa pratensis05CU

-5 0 6 12 18 24Photoperiod (h)Figure 5. Climate-phototherms for Tromsd5(690 39' N)and Oslo, Norway (590 5 5' N) and Deift, The Netherlands(520 N), together with optimum areas for primary in-duction of flowering of Bromus inermisand a high-latitudePoa pratensis. Mean monthly temperatures and daylengthsat day 21 of each month of the year.

in the LD of the short and cool arctic summer.However, when moved to lower latitudes suchspecies may form advanced inflorescences in theautumn which may be vulnerable to frost damageduring the winter (Hodgson, 1966; Heide, 1980;Niemelainen, 1991).

The LD requirement for heading and inflorescencedevelopment (secondary induction) is important forthe prevention of precocious heading and flowering,especially in areas with relatively mild and variablewinter temperatures. While both the critical photo-period and the critical number of LD cycles generallyincrease with increasing latitude of origin of thespecies or ecotypes (e.g. Heide, 1984), some arctic-alpine species show an opposite response and mayflower even in 8-h SD (see above). Since these plantsare adapted to stable winter conditions where LDand even continuous light prevail long beforesnowmelt in the spring, they have no need for astrong LD barrier to prevent precocious heading.Hence, an obligatory LD requirement has noadaptive advantage under such conditions. One ofthese species, Phleum alpinum, which has a bipolardistribution flowers rather freely in SD conditions(Heide, 1990a). Interestingly, this ability to flowerin both LD and SD conditions would be oneprerequisite for a plant's ability to migrate alongmountain ranges across the tropics from one polarregion to the other. Comparative experiments withother such bipolar species would be interesting inthis perspective.

Through the dual floral induction control system,

flowering and reproduction of temperate perennialgrasses are well adapted to and synchronized withthe seasonal changes of temperature and daylength atthe higher latitudes where they grow. The primaryinduction requirements are met by the decreasingdaylength and temperature of autumn and winter,while the increasing daylength and temperature ofspring and early summer satisfy the secondaryinduction requirements. The ability of the temperategrasses to respond to such seasonally determinedenvironmental signals represents an effective andcrucially important mechanism for fitting their lifecycles to the dramatic seasonal changes of the high-latitude environment.

ACKNOWLEDGEMENTSI thank Dr L. T. Evans for his helpful comments on themanuscript and Ms L.-A. Eriksen for typing assistance.

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control of flowering and reproduction in temperate grasses

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