Plant Physiol. (1981) 67, 484 4880032-0889/81/67/0484/05/$00.50/0

Osmoregulation in Cotton in Response to Water Stress'I. ALTERATIONS IN PHOTOSYNTHESIS, LEAF CONDUCTANCE, TRANSLOCATION, ANDULTRASTRUCTURE

Received for publication June 13, 1980 and in revised form October 13, 1980

ROBERT C. ACKERSON AND RICHARD R. HEBERTCentral Research and Development Department, Experimental Station, E. L du Pont de Nemours andCompany, Wilmington, Delaware 19898

ABSTRACT

Cotton plants subjected to a series of water deficits exhibited stressadaptation In the form of osmoregulation when plants were subjected to asubsequent drying cycle. After adaptation, the leaf water potential coincid-ing with zero turgor was considerably lower than in plants that had neverexperienced a water stress. The relationship between leaf turgor and leafwater potential depnded O leaf age.

Nonstomatal factors severely limited photosynthesis in adapted plantsat high leaf water potential. Nonetheless, adapted plants maintained pho-tosyPnthesis to a much lower leaf water potential than did control plants, inpart because of increased stomatal conductance at low leaf water poten-tials. Furthermore, adapted plants continued to translocate recently derivedphotosynthate to lower leafwater potentials, compared with control plants.

Stress preconditioning modffied cellular ultrastructure. Chloroplasts offully turgid adapted leaves contained extremely large starch granules,seemed swollen, and had some breakdown of thylakoid membrane struc-ture. In addition, cells of adapted leaves appeared to have smaller vacuolesand greater nonosmotic cell volume than did control plants.

Osmoregulation enables plants to withstand temporary or sus-tained water deficits (19). Although cellular mechanisms thatinduce or promote osmoregulation are unknown, solute accumu-lation within the cell seems to play a central role in the adaptiveprocess (10-12, 19, 31, 32). In stress-adapted plants, lowering ofcellular osmotic potential through accumulation of osmotica per-mits turgor maintenance at relatively low leaf water potentials (1,10, 11, 14, 16, 19-21, 31, 32).Although many plants partially adapt to water deficits by

osmoregulation, thereby maintaining some growth duringdrought, adaptation is normally associated with reduced growthand productivity (9, 19). Two physiological processes necessaryfor growth and productivity are photosynthesis and translocation.Both are important in generation and distribution of osmoticallyactive solutes. In most plants, water stress reduces photosynthesis(6) and movement of assimilates out of the leaf (24, 28, 33, 34).The purpose of the present study was to examine the process ofosmoregulation in cotton focusing on photosynthesis, transloca-tion, and leaf carbohydrate status and their responses to leafwaterstatus.

In this paper we describe photosynthesis, translocation, andcellular ultrastructure in relation to osmoregulation. A companion

I Contribution 2803 from the Central Research and Development De-partment, E. I. du Pont de Nemours and Co.

paper in this series defines the role of specific cellular carbohy-drates in stress adaptation (2).

MATERIALS AND METHODS

Plant Material. Cotton (Gossypium hirsutum L. Tamcot SP37)plants were grown from seed in controlled environment facilitiesas described (3). When the fifth leaf above the cotyledons wasabout 75% expanded, one set of plants was subjected to repetitivewater stress cycles while another set was well watered. Each stresscycle consisted of allowing plants to dehydrate until midday leafwater potentials reached approximately -20 bars. Dehydrationrequired 24 to 48 h, depending on plant age. Five days ofrecovery(plants well watered) were interspersed between successive stresscycles. Plants were subjected to a total of five such cycles. Middayleaf water potentials of control plants ranged from -5 to -8 bars.Plants that had been subjected to the five stress cycles are referredto as "adapted" plants. This should be construed as referring to"phenotypic" adaptation, rather than genotypic. Control plantshad never been stressed.

Five days after the last stress cycle, all plants were subjected tostress. Data were obtained during this dehydration period fromleaves at nodes 5 and 8. Leaves at node 5 were 75% expanded atthe time of the first stress cycle, whereas the leaves at node 8 werejust emerging. After completion of the last stress cycle, the areasof the leaves at node 5 were similar in adapted and nonadaptedplants. In adapted plants, the leaves at node 8 were approximatelyone-half the size of equivalent leaves in control plants.Water Potential, Leaf Conductance, and Photosynthesis. Leaf

water potentials and leaf conductances were obtained using iso-piestic thermocouple psychometry and diffusion porometry aspreviously described (3). Osmotic potentials were determinedpsychometrically on leaf discs (1.0 cm diameter), frozen in liquidN2, and thawed. Turgor pressure was calculated as the differencebetween total leaf water potential and osmotic potential. Osmoticpotentials were not corrected for the dilution of cell sap withapoplastic water that occurs during freezing (22). Leaf resistanceswere converted to conductances by taking the reciprocal of totalleaf resistance obtained by assuming individual surface resistancesact in parallel.Apparent photosynthetic rates were determined using the CO2

pulse-labeling technique described by Naylor and Teare (26).Translocation. Sections of intact plants consisting of the vege-

tative apex and four to five monopodial and two to three sympo-dial branches were excised under water and the stems were placedin distilled H20. The plants were enclosed in a Plexiglas chambercontaining a fan to facilitate mixing, and air containing about 320PI 1-' CO2 was passed through the chamber (open system). Dewpoint of the air was adjusted to between 24 and 26 C. Plants wereallowed to photosynthesize for 1 h at 27 C with PAR of 850 ,IE

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WATER STRESS ADAPTATION IN COTTON

m-2 s-' provided by a Xenon arc lamp. This PAR was equivalentto that during the growth period in the controlled environmentchamber (3). After 1 h, the chamber was sealed and 5 to 10 ,uCi"CO2 were injected into the chamber. The pulse period was 15 to20 min, followed by 15 to 20 min chase with air (320,d 1-1). Afterthe chase period, discs from leaves at node 6 or 7 were removedand their radioactivity was counted. The percentage of radioactiv-ity remaining in the leaves after selected time intervals was deter-mined. In each experiment, translocation was determined in afully turgid plant (stems in H20) and a wilting plant (stems in 0.7M mannitol after the pulse and chase periods). Excised, ratherthan intact plants, were used to dehydrate the control and adaptedplants at about the same rate.Leaf and Cellular Ultrastructure. Leaf samples were fixed in

phosphate-buffered 5% glutaraldehyde (pH 7.0) for 2 h. Sampleswere rinsed with buffer and treated with phosphate-bufferedosmium tetroxide (2%) for 1.5 h. Tissue was dehydrated by agraded series of ethanol and embedded in Spurr. Thin sectionswere cut and stained with lead citrate and uranyl acetate. Sectionswere examined on a Zeiss EM 10 at 60 kv.

RESULTS AND DISCUSSIONA series of brief water deficits reduced growth of cotton (Fig.

1). After each successive stress cycle the lead conductances of fullyturgid control and adapted plants were similar (Fig. 1). Followingthe first three stress cycles, photosynthetic rates of adapted plantswere lower than those of control plants. However, immediatelyafter the last two stress cycles, adapted leaves photosynthesizedmore rapidly than control leaves. This increase in photosynthesisappeared to be transient inasmuch as fully turgid adapted leavesconsistently had lower rates of photosynthesis than control plants5 days after the last stress cycle (Fig. 5). Even though stressinhibited growth, plants subjected to water stress preconditioningexhibited signs of adaptation when subjected to a subsequent

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CYCLE OF STRESSFIG. 1. Influence of repetitive stress cycles on photosynthesis (A), plant

height (B), and leaf conductance (C) on stress-adapted (0) and controlcotton plants (0). Data were obtained from leaves at node 5 2 days afterplants had recovered from each period of water stress. Each data pointrepresents the mean ± SD of four determinations. Data are from well-watered plants with soil at about "field capacity" in all cases.

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-4 -8 -12 -16 -20LEAF WATER POTENTIAL, bars

FIG. 2. Relationship between leaf water potential and leaf pressurepotential of cotton leaves at the eighth (upper) and fifth (lower) nodeabove the cotyledonary node. Each data point is the mean of two mea-surements and data from two independent experiments were pooled toderive the relationships. (0), control plants; (0), adapted plants. Asterisksindicate significance at the 0.01 level.

water stress. Similarly, Cutler and Rains (9) demonstrated greaterdrought tolerance in cotton subjected to limited irrigation than infrequently irrigated cotton, even though limited water availabilityreduced growth.The adaptation exhibited by stressed plants appeared to be due

to osmoregulation, at least with respect to leaves at node 8. Thiswas inferred from the leaf turgor-leaf water potential relationshipsin adapted and control leaves (Fig. 2). Adapted, young leaves(node 8) exhibited greater leaf pressure potentials than did controlleaves at all leaf water potentials, prior to complete loss of turgor(Fig. 2). Accordingly, adapted, younger leaves must have accu-mulated solutes during the preconditioning phase of the experi-ment. Osmoregulation in these young leaves was similar to thatobserved in slowly adapted sorghum (21). In older leaves (node5), approximately the same turgor was observed in control andadapted plants at high leaf water potentials (2-5 bars). Duringdehydration, adapted plants sustained greater pressure potentialsthan did control plants as leaf water potentials declined (Fig. 2).Consequently, adapted leaves approached zero turgor at lowerleaf water potentials than did control leaves. The pressure poten-tial-leafwater potential relationships in these fully expanded olderleaves resembled those observed in fully expanded sorghum leavesthat had undergone moderate stress in the field (5). At least twoexplanations account for the adaptation response in older leaves.First, solutes could accumulate when adapted leaves undergowater stress, even though the solute status of adapted and controlleaves are similar when leaves are fully turgid. Alternatively,solutes in adapted leaves may be concentrated to a greater extentif adapted leaves have larger nonosmotic cell volumes, as com-pared with control leaves. This is typical in drought-adaptedcotton (11). Electron micrographs of fully turgid control andadapted leaves (node 5) indicate that starch accumulated inadapted leaves (Fig. 3). Based on measurements of 75 to 100 cells,adapted leaves at node 5 had about 30 to 40o less osmotic volume

I

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ACKERSON AND HEBERT Plant Physiol. Vol. 67, 1981

05

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FIG. 4. Relationship between leafwater potential and leafconductanceof adapted (0) and control (0) cotton leaves at the eighth (upper) andfifth (lower) node above the cotyledonary node. Each conductance valuerepresents the mean of five to six measurements obtained from twoexperiments. Asterisks indicate significance at the 0.01 (**) or 0.05 (*)level.

FIG. 3. Transmission electron micrographs of control (upper) andadapted (lower) cotton leaves. Micrographs are from paradermal sections.Magnification is x 11,250. Vac, vacuole; C, chloroplast; SG, starch granule.

per cell than control leaves (based on total cell volume and vacuolevolume). A substantial portion of the nonosmotic volume maywell have been occupied by starch granules inasmuch as estimatesfrom electron micrographs indicated that the volume of starchgranules increased 65-fold during adaptation. Consequently, theadaptation response observed in leaves at node 5 may well havebeen due to concentration of solutes as a result of starch-induceddecreases in cellular osmotic volume. In a subsequent paper (2),kinetics of starch and soluble sugar accumulation are discussed indetail and data will be presented suggesting that both activeaccumulation and concentration of solutes are important mecha-nisms in the type of adaptation observed in older cotton leaves.Similarly, osmoregulation in younger leaves (node 8) is primarilydue to solute accumulation, whereas concentrating effects attrib-utable to starch are minimal (2). These data suggest that themanner in which osmoregulation or adaptation is expressed de-pends on leaf age and perhaps the degree of expansion at the timeof stress.

Stomata of adapted leaves became less sensitive to low leafwater potentials (Fig. 4). This response is typical of many speciesthat have been conditioned to water stress in growth chambers or

the field (5, 7, 9, 21, 23, 27). In both adapted and control leaves,stomatal closure was essentially complete when leaves approachedzero turgor (Figs. 2 and 4). Because adapted leaves maintained a

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LEAF WATER POTENTIAL, bars

FIG. 5. Relationship between leaf photosynthesis and leaf water poten-tial of leaves at the eighth (upper) and fifth (lower) node above thecotyledonary node. Each Zvalue represents the mean of five to six deter-minations from two expernments. (0), control leaves; (0), adapted leaves.

greater degree of turgor to lower leaf water potentials than didcontrol leaves, stomata of adapted leaves remained partially openat low leaf water potentials. Older, fully expanded leaves hadlower leaf conductances than younger leaves at the same waterpotentials. Jordan et al. (22) demonstrated that stomatal responseof cotton to leaf water potential depended uniquely on leaf age.Older adapted leaves exhibited leaf conductances somewhathigher than did nonadapted counterparts (Fig. 3). Although leafconductance tends to decline with leaf age even without waterstress (15), the higher leaf conductances of adapted leaves at node5 (relative to control leaves) suggest that adaptation partiallyovercame the effect of age. Young leaves (node 8) had approxi-mately the same leaf conductance at high leaf water potentials inadapted and control plants (Fig. 4).Adapted leaves exhibited lower rates ofphotosynthesis than did

control leaves at relatively high leaf water potentials (Fig. 5). Thisoccurred in young and old leaves even though leaf conductances

486

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WATER STRESS ADAPTATION IN COTTON

6O[0

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FIG. 6. Relationship between retention of 14C activity and time forcontrol (A) and adapted (B) cotton plants, that were turgid or water-stressed; leaf water potentials are given in C. Data were obtained fromfour different pairs ofplants for control and adapted plants. Data representthe mean + SD from four plants.

were similar or slightly higher in adapted leaves (Fig. 4). Thesedata strongly imply that nonstomatal processes limited photosyn-thesis in adapted leaves. Photosynthesis can be inhibited throughstress-induced perturbations of photosynthetic partial processesthat are not directly linked to CO2 diffusion (6). Decreases in leafmesophyll conductance are commonly observed when leaf waterpotentials decline (7, 8). Furthermore, the accumulation of pho-tosynthetic end products may act to reduce photosynthetic rates,perhaps by metabolic regulation or by altering internal CO2diffusion (25, 30). Large starch granules were observed in chloro-plasts of fully turgid, stress-adapted plants (Fig. 3). Chloroplaststructure is often disrupted by water stress (13, 17, 18). Althoughsome breakdown of thylakoid structure was noted in chloroplastsof adapted leaves, this seemed to be minimal (Fig. 3). However,accumulation of starch in chloroplasts of adapted leaves may haveinduced physical changes in the chloroplasts, thus accounting forlower rates of photosynthesis in adapted leaves at high waterpotentials (Fig. 3).

Retention of photosynthetically derived assimilates (predomi-nantly sugars) would be an effective way of accumulating solutes,thereby facilitating turgor maintenance. In control plants, declin-ing leaf water potentials strongly inhibited translocation of re-cently synthesized assimilates (Fig. 6). Several studies have dem-onstrated that water stress inhibits loading of assimilates intoconducting tissue (24, 27, 33, 34). In contrast, adapted leavescontinued to export recently derived photosynthate rapidly evenas leaf water potentials declined (Fig. 6). Because turgor mainte-nance in adapted plants was associated with maintenance ofphotosynthesis at low leaf water potentials (Figs. 2 and 5), thesupply ofphotosynthetic assimilates may explain continued exportof sugars in adapted leaves even as leaf water potentials declined.In adapted leaves, sugars (sucrose) of photosynthetic origin couldnot act as osmotically active constituents in situ, at least in ex-panding leaves. Translocation ofphotosynthate occurred in cottonat leaf water potentials approaching -33 bars, whereas photosyn-thesis declined to a more significant extent as plants became

stressed (29). In essence, adapted plants utilized in this studymimic closely responses that moderately stressed field-grownplants exhibit with respect to photosynthesis, translocation, andleaf conductance in relation to leaf water potential (4, 29).

Acknowledgments-The technical assistance of W. Hartenstine and M. Ferrarithroughout the course of this study is gratefully acknowledged. We thank Drs. V.Wittenbach, D. Krieg, and J. Radin for helpful suggestions. We thank E. Sparre forassistance in preparation of this manuscript.

LITERATURE CITED

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24. MuNNs R, CJ PEARSON 1974 Effect of water deficit on translocation of carbo-hydrate in Solanum tuberosum Aust J Plant Physiol 1: 529-537

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29. SUNG FJM, DR KRIEG 1979 Relative sensitivity of photosynthetic assimilation

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ACKERSON AND HEBERT

and translocation of "4C to water stress. Plant Physiol 64: 852-85630. THORNE JH, HR KoLLER 1974 Influence ofassimilate demand on photosynthesis,

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