Plant Physiol. (1984) 75, 364-3680032-0889/84/75/0364/05/$01.00/0

Photosynthetic Response and Adaptation to High Temperaturein Desert Plants'A COMPARISON OF GAS EXCHANGE AND FLUORESCENCE METHODS FOR STUDIES OFTHERMAL TOLERANCE

Received for publication November 15, 1983 and in revised form February 2, 1984

JEFFREY R. SEEMANN*, JOSEPH A. BERRY, AND W. JOHN S. DOWNTON2Department ofPlant Biology, Carnegie Institution of Washington, Stanford, California 94305

ABSTRACI

The temperature threshold for the onset of irreversible loss of photo-synthetic capacity of leaves was exmind in studies of net CO2 exch ead by chlorophyll fluorescence techniques. Close agreement was foundbetween the temperature threshold for a dramatic inreas in the fluores-cence of chlorophyll from intact leaves and the leaf temperature at whichthe capacity for photosynthetic CO2 fixation (measured at rte saturatinglight intensity by infrared gas analysis) began to be temperature unstable(i.e. decline with time ofexposure to a costant temprature). This declinein CO2 uptake was not a result of a stomatal response yieling a reducedintercellular CO2 concentration at high temperature, and it is interpretedas an indication of progressive damage to some essential component(s)of the leaf. The temperature-dependent change in chlorophyll fluores-cence apparently also indicated the onset ofthisdamage. The fluorescenceassay could be conducted with discs of leaves collected from remotelcations and kept moist while they were transported to a central location,allwing assessment of the high temperature tolerance of leaves whichdeveloped under natural field conditions. These assays were verified usinga mobile laboratory to study ps exchange of attached leaves in situ. Thehigh temperature sensitivity of leaves of plants growing under naturalconditions were similar to those of the same species grown in controlledenvironments of similar thermal regimes. High temperature in controlledenvironment studies brought about acclimation responses which increasedthe threshold for high temperature damage as measured by gas exchange.Studies of fluorescence versus temperature confirmed that this methodcould be used to quantify these responses, and permitted the kinetics ofthe acclimation response to be ex d. Gas exch e studies, whileproviding similar estimates of thermal stability, required more time, moreelaborate instrumentation, and are particularly difficult to conduct withfield plants growing in situ.

The photosynthetic reactions of plants are among the mostsensitive of plant processes to heat damage, and damage causedby excessively high leaf temperatures may pose significant limi-tations for the growth and survival ofplants. For example, studieshave shown that summer temperatures in Death Valley exceed

' Supported by the Science and Education Administration of theUnited States Department of Agriculture under Grant No. 78-59-21 15-0-128 from the Competitive Research Grants Office. CIW-DPB Publi-cation No. 775.

2 Present Address: CSIRO Division of Horticultural Research, Box350 GPO, Adelaide, S.A. 5001, Australia.

the temperature limits of all but a few plants native to hot desertregions (6). Plants may differ in heat tolerance, and studies haveshown that some plants are capable of physiological acclimationto increase both their heat tolerance and their temperature opti-mum for net CO2 uptake of leaves in response to increasedgrowth temperature (3). Physiological studies of responses ofphotosynthesis to temperature and the limits for heat toleranceare important aids to understanding the productivity and survivalof plants in hot desert regions such as Death Valley. For themost part these studies have concentrated on laboratory meas-urements of a few plants grown in controlled environmentchambers. Few studies have yet examined plants growing undernatural conditions. Such studies are important in order to con-firm that plants growing under natural conditions respond tothis stress as they do in controlled environment studies. Fieldstudies would permit larger populations ofplants to be examined,permit more meaningful comparisons to be made between dif-ferent species and life forms, and enable a more complete eval-uation ofthe extent and the significance ofacclimation responsesto seasonal changes in environmental temperature.Gas exchange studies of net CO2 uptake by attached intact

leaves has been the method of choice for studies of thermalresponses. Effects of temperature on the productivity of plantscan be estimated from studies of the rate of CO2 uptake versustemperature, and thermal tolerance may be estimated fromstudies which examine the ability of a leaf to recover photosyn-thetic capacity after exposure to a high temperature or by ex-amining the time stability ofthe rate ofC02 uptake. Such studiesrequire sophisticated equipment to control leaf temperature andmeasure C02 and H20 exchange. Such studies can be conductedunder field conditions using a mobile laboratory (5, 9). However,the experiments require several hours per plant, and the equip-ment is not generally available. An assay which could be rapidlyapplied to plant material brought to a central location wouldgreatly facilitate field studies of heat tolerance.

Several studies have used changes in Chl fluorescence withheating of leaves as an indicator ofdamage to the photosyntheticmembranes (1, 11, 15, 17). It is thought that heat damage to thePSII reaction centers or associated pigment-protein complexesresults in a corresponding increase in the probability that ab-sorbed light is re-emitted as fluorescence (14). Schreiber andBerry (15) found that the temperature at which fluorescencebegan to increase sharply with temperature corresponded to thethreshold temperature for a detectable decline in the quantumyield for CO2 fixation. Further, they used Chl F-T3 studies torank species in terms of their heat tolerance and to show accli-mation of a species to different growth temperatures. This tech-

' Abbreviation: F-T, fluorescence versus temperature.

364 www.plantphysiol.orgon May 17, 2020 - Published by Downloaded from

Copyright © 1984 American Society of Plant Biologists. All rights reserved.

PHOTOSYNTHETIC TEMPERATURE TOLERANCE: METHODS

nique could have many advantages for ecological studies of heattolerance. However, only a limited number of species have beenexamined for agreement between heat tolerance as assessed bythe fluorescence procedure and more direct measures of wholeleaf photosynthetic performance, and such comparisons havenever been conducted with plants growing in natural environ-ments.

This paper presents laboratory and field studies of the heattolerance of some species of the winter annual flora of DeathValley, CA. The results demonstrate that the fluorescence pro-cedure can be used to obtain an accurate assessment of plantsgrowing under field conditions.

MATERIALS AND METHODSPlant Material. Field plants used for this study had been grown

either within an experimental garden in Death Valley NationalMonument, CA, during spring where they received periodicwatering or under natural conditions in Death Valley. Plantsused in laboratory studies were germinated from seed collectedin Death Valley and grown hydroponically with a completenutrient solution on a solid support of vermiculite and perlite(1:1) in controlled-environment chambers with temperature re-gimes as indicated in the results.Gas Exchange Measurements. Photosynthesis studies were

conducted with attached leaves using a mobile laboratory systemas described (5, 8). All measurements were conducted at anirradiance of 1800 to 2000 Mmol m-2 s-' quanta (400-700 nm)provided from a high-pressure metal-arc lamp. The concentra-tion of CO2 was (except as indicated) 900 to 1000 WA/l, nearlyrate-saturating for these C3 species. Leaf temperature was in-creased in steps from near 20C to near 50°C, and the photosyn-thetic rate and time stability of that rate was noted.

Fluorescence Versus Temperature Measurements. Fluores-cence studies used 0.3 cm2 discs punched from the leaf to beassayed. The leaf disc was placed in an appropriately machinedindentation in a brass block (-500 g) and enclosed with a glassmicroscope coverslip. The disc was illuminated with a very stableexciting light through an interference filter (X,,,, = 480 nm, 0.1Mmol quanta m-2 s-'), and fluorescence was collected through afiber optic and interference filter (X,,,, = 690 nm, 12 nm band-pass) and monitored with a photomultiplier tube. The blockcontaining the leaf disc was slowly heated at a rate of -1.5°Cmin-', and the temperature of the leaf disc was monitored usinga thermocouple. The fluorescence and temperature signals wererecorded on an X-Y recorder yielding a plot of F-T. Some earlierexperiments were conducted using whole attached leaves en-closed in a water-jacketed cuvette of design similar to that usedfor gas exchange studies. Discs punched from the leaves weresubsequently found to yield results identical to those from theattached leaves. Preliminary experiments (data not shown) dem-onstrated that leaves could be detached in the field, placed insmall plastic bags with moist filter paper, and stored in the darkin an insulated chest at 25 to 30°C for several hours beforeconducting fluorescence measurements without affecting the ap-parent heat tolerance. Changes in apparent heat tolerance couldoccur if the tissue was allowed to dry or kept longer than 24 h.The equipment used for these fluorescence studies was portable,could be operated from normal line current, and under normalindoor levels of light. In Death Valley, the measurements wereconducted in a house trailer. Leaf material was usually collectedin the afternoon and assayed within 4 to 6 h. Possible influencesof leaf age and plant age were explored and shown to have onlya small effect on thermal stability (see also 17), provided leaveswere fully expanded. Developing leaves had reduced thermalstabilities. There was no indication of physiological adjustmentsin thermal tolerance of leaf samples during the storage or assayprocedures.

RESULTS AND DISCUSSION

The temperature response of photosynthesis of an attachedleafofthe desert winter annual, Camissonia brevipes, determinedat rate-saturating irradiance is shown (Fig. 1C). At normal at-mospheric CO2 concentration (330 Ml/1), the effect of changes intemperature were small, yielding a broad temperature optimumat about 20C. More pronounced effects of temperature wereobserved at high (about three times atmospheric) CO2 concentra-tion. At temperatures in excess of 30C, there was a gradualdecline in photosynthetic rate. At 44C, the rate had declined toapproximately one-half of the optimum rate and began to beunstable with time as indicated by a downward arrow (Fig. IC).A time course of chankes in photosynthesis and temperaturefrom a similar experiment (Fig. 2) shows that, as temperature

(DLc-

a)0

0ea)L-0

n

(I

(NJI

E

0E

a)

0

011

D(\J

cE)

-,I I I I

A Camissonia brevipes

2

0 A

0

8 1000 p6bar CO2

6

330 pbar CO2

2

010 20 30 40 50 60

Leaf temperature, OCFIG. 1. A, Fluorescence versus temperature course obtained directly

from an X-Y plotter fora leaf disc of Camissonia brevipes (see "Materialsand Methods" and "Results" for details). B, F-T course of a disc punchedfrom the leaf used for the 1000 1l/l CO2 temperature response shown inC after completion of that measurement. C, Rate of net CO2 exchangeas a function of temperature for two separate leaves measured at eitherhigh (1000 ul/1) or ambient (330 Ad/l) CO2 concentrations. Downwardarrows indicate the temperature at which the rate ofCO2 fixation becameunstable with time. Similar aged leaves from a single individual of C.brevipes grown under 20/15C (day/night) growth conditions were usedin all experiments shown here.

365

www.plantphysiol.orgon May 17, 2020 - Published by Downloaded from Copyright © 1984 American Society of Plant Biologists. All rights reserved.

50 they demonstrated that loss of photosynthetic capacity was as-

Mo/vastrum rotundofo/lum sociated with a reduction in the capacity of chloroplasts isolated

------ 45 from those leaves for PSII electron transport. Bauer (2) reported-, o * that high temperature inhibition of CO2 uptake by Hedera helix

leaves was not reversible once the temperature exceeded that at

40 O which CO2 uptake had fallen to half of its optimum rate. In our

_ experiments, the threshold for time instability occurred whenE the rate had fallen to about half its optimum value (Fig. IC) and

) ,_,'with most other species examined.

Photosynthesis & A F-T course from a disc of the opposite leaf of the same plant)_'-Leaf temperature 30 as used for the gas exchange studies is shown in Figure IA. As

the temperature was increased, the fluorescence from the discwas relatively constant until about 43C. Above this threshold

() 10 20 30 40 50 60 70 25 fluorescence increased sharply with temperature until it reached2030 60 70a peak near 49°C. We estimated the threshold for this fluores-

cence increase by extrapolating the linear portions of the F-T2. The time course of the rate of photosynthetic CO2 fixation course above and below the threshold to a point of intersection,af of Malvastrum rotundifolium as the leaf is heated (-). The T2, as suggested by Schreiber and Berry (15). This point proved

surse of leaf temperature is indicated by the dashed line, to be quite reproducible, with variation ofabout ±1°C for similar

icreased in steps, the rate of photosynthesis at first re- leaves of the same plant and +0.5%C for replicate discs from theed rapidly, reaching stable values at each new temperature. same leaf. The break point of this F-T course correspondedver, when the temperature was increased above about 44C, closely to the temperature at which irreversible damage began tote began to decline continuously at constant temperature. be evident in the gas exchange studies (Fig. IC).the CO2 concentration was nearly saturating for these C3 Irreversible damage to photosynthetic capacity occurred whens, it is unlikely that this decline could be caused by a leaves were held at temperatures in excess of 43C in the gasion in stomatal conductance, and in measurements where exchange cuvette (Fig. IC) as evidenced by a time-dependental conductance was monitored continuously, we found decline in photosynthetic capacity at high temperature and aLe intercellular CO2 concentration usually increased while failure to recover previous capacity at optimal temperatures (datacline was occurring. Other experiments (data not shown) not shown). Fluorescence studies ofsuch damaged leaves showedDd that once a leaf had been exposed to temperatures above a reduced fluorescence transient in the F-T course (Fig. IB).reshold for a time-dependent decline, the rate of photosyn- Presumably such attenuation reflects damage to the chloroplastcould not be fully recovered upon returning to a lower membranes caused by heat. This result provides a further indi-rature. Provided the leaf had not exceeded this threshold, cation that these two phenomena (loss of photosynthesis and the,er, the response to temperature was generally reversible. increase of fluorescence) are linked, but also indicates that ther instability was observed by Pearcy et aL ( 11) in their fluorescence assay should not be conducted on previously heat-of the temperature responses of Atriplex lentiformis, and damaged tissue.

EnU)a 10oo

>s 90U)

800

70

E 60

E 50_(0 40E

300

- 20u 10

a)o

FIG.for a le

time co

was inspondeHowe)the ratSince Ispeciesreductistomatthat ththe derevealethis ththesistempehowevSimila:study 4

Table I. Comparison ofthe Fluorescence Rise Temperature to the Heat Tolerance ofPhotosynthesis asMeasured by Gas Exchange

Species Growth Photosynthesis FluorescenceA

Conditions Heat Stability Rise Temperature A°C

A. Time Stability of Net CO2 ExchangeAbronia villosa (field') 46.5 47.6 -1.1Camissonia brevipes (20/15) 43.5 43.1 +0.4Camissonia brevipes (20/15) 44.0 44.0 0.0Camissonia brevipes (43/32) 47.0 47.5 -0.5Curcurbita palmata (field') 47.5 44.5 +3.0Geraea canescens (fieldb) 48 (50%)c 46.2 +1.8Geraea canescens (field') 40.0 40.5 -0.5Geraea canescens (20/15) 44.2 44.6 -0.4Geraea canescens (40/32) 46.6 46.8 -0.2Gossypium hirsutum (20/15) 45.0 45.2 -0.2Gossypium hirsutum (40/32) 46.7 48.6 -1.9Lupinus arizonicus (field") 44.0 44.7 -0.7Malvastrum rotundifolium (fiueld) 45.0 44.0 -1.0Phacelia crenulata (fieldb) 41.5 (50%)c 42.6 -1.1

B. Quantum Yield Studies"Atriplexglabriuscula (20/15) 42.0 42.0 0.0Atriplex subulosa (20/15) 40.3 41.0 -0.7Tidestromia oblongifolia (45/31) 48.8 49.0 -0.2

Plants were growing in an experimental garden in Death Valley and received occasional waterings.b Plants had germinated and grown under natural conditions in Death Valley.Leaf temperature at which the photosynthetic rate had fallen to 50% of its maximum value.

I Data of Schreiber and Berry (15).

366 SEEMANN ET AL. Plant Physiol. Vol. 75,,1984

www.plantphysiol.orgon May 17, 2020 - Published by Downloaded from Copyright © 1984 American Society of Plant Biologists. All rights reserved.

PHOTOSYNTHETIC TEMPERATURE TOLERANCE: METHODS

LL

0-

U)

0

x

'-

0

c0C

00

0;

-C

40

0

aC

10 20 30 40Leaf temperature, °C

50

FIG. 3. Fluorescence versus temperature course (A) and temperatureresponse of photosynthesis (B) for Geraea canescens grown under eitherlow (20/15'C) or high (40/32C) temperature regimes. Photosynthesisand fluorescence measurements were conducted on opposite leaves ofthe same plant.

48Camissonia brevipes

47

= 46

0~~~~~~~~

0~~~~~~~

445u

o Transfer from 20° to 400C

43-

42 .o 8 16 24 32Hours after transfer

FIG. 4. Time course of the fluorescence rise temperature followingtransfer of an individual of C. brevipes from 20°C to 40°C growthconditions. Several similar-aged leaves were used and the plant was well-watered throughout the course of the experiment.

We have conducted similar comparisons of fluorescence andgas exchange for a number of other species (Table I). The plantsexamined had been grown under a variety of conditions; inlaboratory growth cabinets at low and high temperature, in anexperimental garden in Death Valley where the plants wereirrigated but otherwise in a natural setting, and in natural habitatsin Death Valley where they had germinated and grown. The

fluorescence rise temperature was generally very close to thetemperature at which irreversible inhibition of photosynthesiswas observed (mean difference was 0.9C). Data from anotherstudy (15) is also included in Table I and shows similar closeagreement.

Infiequently the assay protocols gave anomalous resultswhich should be noted. On two occasions we failed to observetime instability of the photosynthetic rate at superoptimal tem-peratures even as complete inhibition was approached (Table I,footnote c). When the temperature was lowered, however, therate failed to recover the previous values, indicating that irre-versible damage had occurred. This may indicate a difference inthe kinetics of damage occurring at high temperature in theseindividuals. A more elaborate experimental protocol would berequired to precisely specify the threshold for damage in thesecases. In these two cases, we assumed (following Bauer [2]) thatthe threshold was reached when the rate declined to 50% of theoptimum rate. Since the decline of the rate in this temperaturerange is very steep, errors introduced by this assumption arerather small. With another species (Curcurbita palmata), thefluorescence assay yielded a significantly lower thermal stabilitythan indicated by gas exchange. Schreiber and Berry (15) notedthat leaves generally had a slightly higher thermal stability atmoderate than low light intensity. Since the fluorescence assayis conducted at very low light intensity and the gas exchange athigh light intensity, this discrepancy might indicate that thisspecies has an unusually strong response to light intensity. Themost extreme difference was only 3C. Overall the studies indi-cate very good agreement between the two procedures, but theexceptions emphasize the need for careful controls if a high

precision is to be achieved.Determination of Photosynthetic Acclimation. Photosynthetic

temperature responses of net CO2 uptake by similar leaves ofGeraea canescens, grown under contrasting temperature regimes(20/15C and 40/32C day/night), are shown in Figure 3B. Thehigh-temperature-grown plant could continue active photosyn-thesis to temperatures nearly 5°C above that at which thermaldestruction of some components of the photosynthetic systemoccurred in the low-temperature-grown plant. The temperaturelimits of photosynthesis for these plants was also indicated bythe F-T courses from similar leaves of these plants (Fig. 3A).Similar prallel changes in Chl fluorescence and photosyntheticphysiology have also been observed during acclimation of desertperennials (1, 4, 11).Chl fluorescence could also be used to determine the time

course of this acclimation response. The fluorescence rise tem-perature was determined at -4 to 8 h intervals for an individualof C. brevipes after transfer from 20C to 40C growth conditions(Fig. 4). The 6°C adjustment of thermal stability is seen to havereached the midpoint in 10 h and was essentially completewithin 32 h. The extremely rapid capacity for adjustment ofthermal tolerance may be an important factor in allowing theseannual species to cope with large fluctuations in leaftemperatureas a result of rapid changes in environmental conditions. Thekinetics of this acclimation process closely resemble that foundfor Nerium oleander by Raison et al. (13). These workers foundthat during acclimation of this species to high temperature, thefluidity of chloroplast membrane lipids (measured at a constanttemperature) decreased, apparently by modification of lipidproperties. This change was accompanied by an increase in theheat tolerance ofthe photosynthetic apparatus, as determined bythe F-T assay. Pike (12) has also shown a change in the physicalproperties of membrane lipids from desert annuals grown atcontrasting temperatures.

CONCLUSIONSThis study has focused upon the use of Chl fluorescence to

study the photosynthetic responses ofplants to high temperature.

A Geraeo canescens

, 2

lI

:~~~~IIN24.d

B100 00

60

40

20

o , .

367

www.plantphysiol.orgon May 17, 2020 - Published by Downloaded from Copyright © 1984 American Society of Plant Biologists. All rights reserved.

368 SEEMANN ET AL.

One of the major factors limiting such research, particularly asit concerns plants under natural growth conditions, has been alack of methods which allow quantitative yet rapid assessmentof the temperature sensitivity of the photosynthetic apparatus.Using the fluorescence procedure described here, a quantitativeassessment of the high temperature tolerance of a leaf can bemade within -20 min. In a number of studies, the fluorescenceassay indicated a thermal stability similar to that measured byexamining the temperature dependence and time stability of netCO2 uptake using similar leaves of the same plant. Changes inthe fluorescence rise temperature were found to predict accli-mation-induced shifts in the high temperature sensitivity to CO2fixation processes. Since leaves may be killed by high temperaturedamage or recover only slowly in instances of moderate damage(2), and since damage may be aggravated by high light intensities(10), we are confident that differences among plants in theirfluorescence rise temperature indicates ecologically and physio-logically significant differences in their capacity to tolerate hightemperature.The ease and rapidity of this technique allows measurements

to be made of the temperature acclimation response of plantpopulations under field conditions. We have used the techniqueto study the capacity of phenologically and physiognomicallydistinct groups of desert plants to tolerate high temperatures andhave examined their capacity to acclimate to changing temper-ature (7). This technique has also been used to study the accli-mation ofdesert winter annuals to seasonally increasing environ-mental temperature in Death Valley (16).

LITERATURE CITED

1. ARMOND PA, U SCHREIBER, 0 BJiRKMAN 1975 Photosynthetic acclimation totemperature in the desert shrub, Larrea divaricata II. Light-harvestingefficiency and electron transport. Plant Physiol 61: 411-415

2. BAUER H 1978 Photosynthesis of ivy leaves (Hedera helix) after heat stress. 1.CO2 exchange and diffusion resistances. Physiol Plant 44: 400-406

Plant Physiol. Vol. 75, 1984

3. BERRY JA, 0 BJORKMAN 1980 Photosynthetic response and adaptation totemperature in higher plants. Annu Rev Plant Physiol 31: 491-543

4. BJORKMAN 0, M BADGER 1979 Time course of thermal acclimation of thephotosynthetic apparatus in Nerium oleander. Carnegie Inst Wash Yearbook78: 145-148

5. BJORKMAN 0, M NoBs, J BERRY, H MOONEY, F NICHOLSON, B CATANZERO1973 Physiological adaptation to diverse environments: approaches andfacilities to study plant responses to contrasting thermal and water regimes.Carnegie Inst Wash Yearbook 72: 393-403

6. BJORKMAN 0, M NoBs, H MOONEY, J TROUGHTON, J BERRY, F NICHOLSON,W WARD 1974 Growth responses of plants from habitats with contrastingthermal environments: transplant studies in the Death Valley and BodegaHead experimental gardens. Carnegie Inst Wash Yearbook 73: 748-757

7. DOWNTON WJS, JA BERRY, JR SEEMANN 1984 Tolerance of photosynthesis tohigh temperature in desert plants. Plant Physiol 74: 786-790

8. EHLERINGER JR, 0 BJORKMAN 1977 Quantum yield for CO2 uptake in C3 andC4 plants. Dependence on temperature, CO2 and 02 concentration. PlantPhysiol 59: 86-90

9. MOONEY HA, 0 BJORKMAN, GJ COLLATZ 1978 Photosynthetic acclimation totemperature in the desert shrub, Larrea divaricata. I. Carbon dioxide ex-change characteristics of intact leaves. Plant Physiol 66: 406-410

10. LOMAGIN AG, TA ANTROPOVA 1966 Photodynamic injury to heated leaves.Planta 68: 297-309

1 1. PEARCY RW, JA BERRY, DC FoRK 1977 Effect of growth temperature on thethermal stability of the photosynthetic apparatus of Atriplex lentiformis(Torr.) Wats. Plant Physiol 59: 873-878

12. PIKE CS 1982 Membrane lipid physical properties in annuals grown undercontrasting thermal regimes. Plant Physiol 70: 1764-1766

13. RAIsON JK, JA BERRY, PA ARMOND, CS PIKE 1980 Membrane properties inrelation to the adaptation of plants to high and low temperature stress. In:NC Turner, PJ Kramer, eds, Adaptations of Plants to Water and HighTemperature Stress. Wiley-Interscience, New York, pp 261-273

14. SCHREIBER U, PA ARMOND 1978 Heat induced changes ofchlorophyll fluores-cence in isolated chloroplasts and related heat-damage at the pigment level.Biochim Biophys Acta 502: 138-151

15. SCHREIBER U, JA BERRY 1977 Heat-induced changes of chlorophyli fluores-cence in intact leaves, correlated with damage of the photosynthetic appa-ratus. Planta 136: 233-238

16. SEEMANN JR, JA BERRY, WJS DowNToN 1977 Seasonal changes in high-temperature acclimation of desert winter annuals. Carnegie Inst Wash Year-book 79: 141-143

17. SMILLIE RM, R NonT 1979 Heat injury in leaves of alpine, temperate andtropical plants. Aust J Plant Physiol 6: 135-141

www.plantphysiol.orgon May 17, 2020 - Published by Downloaded from Copyright © 1984 American Society of Plant Biologists. All rights reserved.