Plant Physiol. (1982) 70, 1508-15130032-0889/82/70/1508/06/$00.50/0

Stomatal Behavior and Water Relations of WaterloggedTomato Plants

Received for publication June 29, 1981 and in revised form July 19, 1982

KENT J. BRADFORD1 AND THEODORE C. HSIAOLaboratory ofPlant- Water Relations, Department of Land, Air and Water Resources, University of California,Davis, California 95616

ABSTRACT

The effects of waterlogging the soil on leaf water potential, leaf epider-mal conductance, transpiration, root conductance to water flow, and petioleepinasty have been examined in the tomato (Lycopersicon esculentumMill.). Stomatal conductance and transpiration are reduced by 30% to 40%after approximately 24 hours of soil flooding. This is not due to a transientwater deficit, as leaf water potential is unchanged, even though rootconductance is decreased by the stress. The stomatal response apparentlyprevents any reduction in leaf water potential. Experiments with variedtime of flooding, root excision, and stem girdling provide indirect evidencefor an influence of roots in maintaining stomatal opening potential. Thisroot-effect cannot be entirely accounted for by alterations in source-sinkrelationships. Although 1-aminocyclopropane-l-carboxylic acid, the im-mediate precursor of ethylene, is transported from the roots to the shootsof waterlogged tomato plants, it has no direct effect on stomatal conduct-ance. Ethylene-induced petiole epinasty develops coincident with partialstomatal closure in waterlogged plants. Leaf epinasty may have beneficialeffects on plant water balance by reducing light interception.

Paradoxically, physiological responses to waterlogging are oftenconsidered to be similar to those induced by drought. Since rootconductance can be decreased by sudden flooding, wilting canoccur, especially under conditions of high transpiration (12).However, wilting does not always accompany flooding injury, andleaf 422 may be unaffected or even increase in waterlogged plants(5, 10, 14). The maintenance of high 4 values in waterloggedplants is due to stomatal closure limiting water loss (10, 14, 18,22). Yet, it is unclear how the stomatal response is initiated. Thetime courses of leaf 4, ge, transpiration, and root conductanceduring waterlogging were determined to examine their causal andtemporal relationships.Two possible mechanisms were investigated by which waterlog-

ging might influence stomatal behavior without changes in leaf4,. Waterlogged tomato roots export ACC to the shoot where it isconverted to ethylene, promoting the characteristic epinasty of thepetioles (3-6). We therefore tested whether ACC has a direct effecton stomatal opening. Waterlogging also rapidly alters the source-sink relations of plants (24), and such changes in assimilateutilization can cause corresponding stomatal responses (11, 19,

' Supported by National Science Foundation and University of Califor-nia Graduate Fellowships.

2 Abbreviations: A, water potential; ACC, I-aminocyclopropane- 1-car-boxylic acid; ge, leaf epidermal conductance to water vapor; CK, cytoki-nin(s); GA, gibberellin(s).

20). That possibility was studied by using plants which had beensteam girdled around the lower stem.

MATERIALS AND METHODS

Plant Material and Treatments. Tomato plants (Lycopersiconesculentum Mill.) were grown in 10-cm pots in a potting soilmixture in a growth chamber for five weeks (six to seven leafstage). Three cultivars were used, VF 145B, VFN8, and RhinelandsRuhm, and all responded similarly to waterlogging stress. Envi-ronmental conditions were: temperature, 26°C day/21°C night;photo-period, 12.5 h (8:30 to 21:00); light intensity, 450 ,uE m s1PAR; RH, 55%. In some cases seedlings were grown in a green-house, but were transferred to the growth chamber at least 1 weekprior to use in experiments. The pots were irrigated once or twicedaily, and full-strength nutrient solution (4) was used once perweek in place of water.

Plants were flooded by placing their pots inside 13-cm pots andfilling with distilled H20 to the cotyledonary node. Excised shootswere used to study the effects of ACC. The pots were immersedin water and the stem was cut under water with a razor blade justbelow the cotyledonary node. After removing the cotyledons andlowest two leaves under water, the bases of the shoots wereimmersed in solutions with or without ACC in Erlenmeyer flasksand held in place with foam plugs. The solutions were changed tofresh solutions at the start of the second light period. To study theeffects of altered source-sink relationships, the stem was girdledby directing a jet of steam from a pipette at the cotyledonary nodefor 1.5 min. A segment 1 to 2 cm long was killed, and microscopicexamination confirmed that no living cells remained in the girdledregion. The xylem remained functional and the plants were turgidfor 3 d if flooded or about 1 week if drained.

Measurements. Leafepidermal conductance was estimated witha Licor (Lambda Instruments Corp., Lincoln, NB) model LI-65autoporometer with a LI-205 sensor, calibrated before each ex-periment for the range of temperatures encountered. An aspiratedmask was worn by the experimenter at all times inside the growthchamber to prevent the accumulation of expired CO2. Measure-ments were made on both surfaces of a leaflet on the third orfourth oldest leaf. Adaxial ge averaged between 50%o and 55% ofthe abaxial ge, and this relationship was not altered by flooding.Therefore, data are expressed as the total conductance of the twoleaf surfaces in parallel. Since adaxial and abaxial ge exhibitedsimilar changes, only abaxial ge was measured in the experimentswith excised shoots. Leaf conductance of wilted leaves (stomatapresumably completely closed) was 0.04 cm s-1, or less than 10%oof the maximum daytime values.

Leaf 4 was determined by isopiestic thermocouple psychrometry(2) using a single leaflet per determination. No more than fiveleaflets were removed from any individual plant. The samplingwas arranged to minimize the effect of progressive defoliation.Measurements of 4, on whole leaves in a pressure bomb gave

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WATER RELATIONS OF WATERLOGGED TOMATO

comparable results.The surfaces of the pots (both control and flooded) were covered

with black plastic held in place by a rubber band. Tests showedthat this effectively prevented evaporation from the soil or watersurface. Transpiration was therefore equated with weight lossbetween measurements.The angle between the petiole of the third oldest leaf and the

stem was measured with a transparent protractor. Epinasty isdefined as the change in petiole angle from zero time.

Statistical Analysis. A randomized complete block design wasused with five to eight replicates per treatment. Data were sub-jected to analysis of variance. All experiments except the one inFigure 3C were performed at least two times with similar results.

RESULTS

Stomatal Behavior in Waterlogged Plants. Flooding in themorning (at the start of the light period) had no significant effecton ge or transpiration during the first day (Fig. 1). On the secondand subsequent days, however, ge of waterlogged plants averagedonly 72% of the control value. Measured values of ge indicate thatstomata of flooded plants did not open as wide initially as the

FLOODED IN MORNING

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FIG. 1. Epinasty, ge, and transpiration of VF 145flooded at start of light period. Black bars on abscissa idarkness. Arrows indicate time of initiation of floodingences between treatments are marked by asterisks: *,:0.01.

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KFIG. 2. Epinasty, ge, and transpiration of VF 145B tomato plants

flooded at end of light period. Symbols as in Figure 1.

control plants and closed progressively during the day. Transpir-ation was reduced in close proportion to the changes in ge, showing

'..b- no effect on the first day of flooding and averaging 68% of thecontrol values on subsequent days. Epinasty began 24 h after thestart of flooding and continued to increase thereafter (Fig. 1). Nosignificant difference in leaf 4 was detected between control andwaterlogged plants at any time during the stress period (Fig. 3A).

* .' \ This was confirmed by pressure bomb measurements with whole*l/ leaves. Psychrometric determinations of the osmotic potential of

frozen and thawed leaves revealed no treatment differences. Bulkturgor potential was calculated to be between 5 and 6 bars in bothflooded and control leaves (data not shown). Consequently, the

. marked stomatal closure is not the result of a decrease in bulk 4or turgor pressure of the leaf.When plants were flooded in the evening (at the end of the light

period), the stomatal response was different. Both ge and transpir-ation were reduced during the first light period following flooding,

60 72 84 as well as on subsequent days (Fig. 2). In this experiment, ge wasmeasured during the first 0.5 h of illumination, which led to a

5B tomato plants large variance since the stomata were opening during this period.indicate periods of However, the data show that stomata of flooded plants begin toStatistical differ- open on illumination, but close progressively during the day. In

P s 0.05; **, P - all other experiments reported here, the initial ge measurementswere taken between 0.5 and 1 h after illumination, after stomatal

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BRADFORD AND HSIAO

-24 -12 0 12 24 36 48 60

B FLOODED IN EVENING C BRIEFLY WILTED IN MORNING

FIa t

HOURS

FIG. 3. Epinasty, ge, and leaf as influenced by time of flooding or by brief wilting. Symbols as in Figure 1.

opening was nearly complete. At this time, ge of evening-floodedplants was notably depressed on day 1 compared to control plants,then recovered somewhat during the afternoon (Fig. 3B). Tran-spiration was also reduced on the first day, in contrast to themorning-flooded treatment (Fig. 2). Immediately following illu-mination, leaf decreased to -12 bars and then soon recoveredto the control value (-6 bars) (Fig. 3B). The stomata also reopenedafter turgor was restored, but ge remained lower than the controlvalues. On subsequent days, the pattem was similar to that seenin moming-flooded plants (Figs. 1 and 3A). Thus, evening-floodedplants experience a brief water deficit on the morning followingflooding which is not observed in moming-flooded plants. Ineither case, stomatal closure on days 2, 3, and 4 after flooding isnot associated with low leaf A.Whether a brief water deficit could cause such a long-term

effect was tested by inducing a short period of water stress inotherwise unstressed plants. Pots were immersed in ice water anda stream ofwarm (40°C) air was directed over the shoots, resultingin a slight wilt within 5 min. Samples were immediately taken for

measurement, and the plants were returned to the growthchamber. Even with these rather severe measures, leaf decreasedonly to -8.5 bars. Nonetheless, this was sufficient to cause apattern of stomatal closure and reopening similar to that in theevening-flooded plants (Fig. 3C). After reopening, however, sto-mata behaved as the control plants both on the afternoon of dayI and on subsequent days. Hence, it is concluded that the persistentstomatal closure seen in the evening-flooded plants is not due toan after-effect of the brief water deficit.

Epinasty also occurred in the evening-flooded plants, and itappeared to be initiated somewhat sooner than in the morning-flooded plants (compare Figs. 1 and 3A with 2 and 3B). The shortwilting treatment did not induce epinasty (Fig. 3C).Changes in Root Conductance Due to Flooding. Numerous

studies have found that apparent root conductance to water uptakedecreases under waterlogged or anaerobic conditions (5). Our owndata on this point are taken from experiments where a suctionwas used to collect xylem sap from flooded and control plants (seeRef. 6 for details). Since a constant pressure gradient (0.9 bar) wasused to induce flow, changes in the rate of sap collection corre-

spond to changes in root conductance. Within 8 h of flooding,

there was a 50%o reduction in sap flow, indicating a halving of rootconductance (Fig. 4). After 48 h, root conductance increasedrapidly as the roots became severely injured. Root weight in-creased steadily in the control plants, but declined in the floodedplants due to deterioration and loss of most of the smaller roots(Fig. 4). These data suggest that in the evening-flooded plants,root conductance was decreased by the 12 h flooding stress. Whenstomatal opening occurred on illumination the next morning (Fig.2), water uptake lagged behind water loss, resulting in the decreasein leaf (Fig. 3B). The continued partial stomatal closure after 48h in both flooding treatments, even though root conductance isnow high, emphasizes that stomatal behavior in flooded plants iscontrolled by factors other than the leaf water balance.

Role of Ethylene in Stomatal Behavior of Flooded Plants. Thelag time between the imposition of flooding and the initiation ofepinasty represents the time required for root stress to occur, fora signal (ACC) to be transported, and for the shoot tissues torespond (4-6). Stomatal closure and epinasty have similar lagtimes (Figs. 1 and 3). Further, the stomata close and prevent adecrease in leaf 4, only if a period of transpiration intervenesbetween the imposition of flooding and the next photoperiod(compare Fig. 3, A and B). Since a vigorous transpirational streammarkedly facilitates movement of substances in the xylem fromroots to shoot, this implicates the roots as a source of factors whichmodify stomatal behavior. Since ACC is transported from theroots of waterlogged tomato plants (6), we tested the effect ofACC on ge. When ACC is supplied to excised shoots via thetranspiration stream, epinasty is promoted within a few hours(Fig. 5) due to the conversion of ACC to ethylene (6). Leafconductance, however, was not significantly different between thetreatments (Fig. 5). Thus, ethylene or ACC does not have a directeffect on stomatal aperture. Excision itself, on the other hand, didinfluence stomatal behavior. Leaf conductance of the excisedshoots was somewhat lower than that of intact plants on the firstday of excision, and ge was greatly reduced in the cuttings on thenext day (Fig. 6). The presence of ACC in the uptake solutionshad no additional effect. Leaf 4, was not measured, but the plantsremained turgid to the touch, and epinasty, a growth reponserequiring turgor, continued to develop during the second day(data not shown). Although the timing of stomatal closure during

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1510 Plant Physiol. Vol. 70, 1982

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WATER RELATIONS OF WATERLOGGED TOMATO

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FIG. 4. Rate of sap collection under 0.9-bar suction and changes inroot weight during waterlogging ofVFN8 tomato plants. Sap was collectedfor 3 h from detopped root systems, then roots were carefully washed fromsoil, blotted dry, and weighed. Control curves are linear regression lines.Flooded curves were eye fitted. In this experiment, photoperiod was 16 hrather than 12.5 h. Symbols as in Figure 1.

waterlogging is consistent with the transmission of a factor be-tween the stressed roots and shoot, that factor is apparently notACC. The ability of root excision to reproduce the stomatalbehavior seen in flooded plants (i.e. little effect on the first dayfollowed by partial closure on the second) suggests that the rootsnormally play a role in plant water balance in addition to that ofwater uptake.

Effect of Girdling on Stomatal Behavior. Although the abovedata are consistent with the transmission of a factor from theflooded roots which affects stomatal behavior, an alternativeexplanation is equally viable. Blocking assimilate transport orreducing sink strength often results in stomatal closure and re-duced photosynthetic rates (11, 19, 20). Both flooding and rootexcision could affect stomata by reducing phloem transport fromleaves to roots. This hypothesis was tested by girdling plants ingreenhouse experiments. Transpiration of intact flooded plantswas unaffected on the first day of flooding, but decreased to 53%of the control value on the second day, in good agreement withthe growth chamber data (Fig. 7). Girdled but unflooded plantsalready showed an 18% reduction in transpiration on the first day(girdling had occurred the previous evening), and the effect

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FIG. 5. Epinasty and ge of excised shoots as influenced by presence ofACC in uptake solution. Shoots of VFN8 tomato plants were excised at8:00 and measurements were begun at 10:00. Symbols as in Figure 1.Effect of ACC on ge was not statistically significant.

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plants on consecutive days. The uptake solutions contained I mM KCI and0.2 mm CaSO4. ACC at 1 im is sufficient to cause petiole epinasty (datanot shown). Effect of ACC on g. was not significant, so asterisks refer todifferences between intact and excised treatments. Symbols as in Figure 1.

reached a maximum (40% reduction) approximately 24 h aftergirdling. When plants were both flooded and girdled, only thegirdling effect was apparent during the first day and night, but onthe second day an additional reduction in transpiration occurred.This effect of flooding on the second day was significant (P c0.001) regardless of whether the plants had been girdled. Meas-urements ofge in the growth chamber confirmed that the reductionin transpiration was correlated with stomatal closure (3). Thus,elimination of roots as a sink for phloem transport rapidly leads

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BRADFORD AND HSIAO

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TIME INTERVAL

FIG. 7. Flooding and girdling effects on transpiration. Plants (VFN8)were girdled in evening and flooded next morning (15 h later). Transpir-ation was measured twice a day as weight loss from pots. Data are

presented as percent of control values due to environmental variation in

greenhouse. Average values (g plant-) for control treatment are: day 1,58.9; night 1, 9.4; day 2, 82.8; night 2, 12.6. Data are averages from two

separate experiments with a total of nine replicates. On day 1, only girdlingtreatment was significant, whereas on day 2, both girdling and floodingwere significant (P c 0.001). Girdling x flooding interaction was not

significant, indicating that both intact and girdled plants responded simi-

larly to flooding.

to partial stomatal closure. However, there is an additional effect

of the anaerobic roots which is not accounted for by this mecha-

nism.

DISCUSSION

Curiously, waterlogging is often considered to be a stress anal-

ogous to drought, and certainly wilting can occur if plants are

suddenly exposed to anaerobic root conditions when transpira-tional demand is high. Many plants, however, including those not

particularly adapted to the wetland condition, can respond to

stress by closing stomata to restrict water loss. Stomatal conduct-

ance is reduced in tomato leaves following waterlogging, without

the intervention of a transient wilting and recovery cycle (Figs. Iand 3A). Moreover, stomatal closure is one of the earliest shoot

responses to waterlogging, coinciding with the development of

petiole epinasty. Jackson and co-workers (10) also found that

transpiration decreased on the secohd day of waterlogging, but

detailed measurements of stomatal behavior were not presented.A review by Sojka and Stolzy (22) concluded that for a variety of

crop plants, ge decreases as the 02 diffusion rate in the soil

declines. Similar behavior also occurs in woody species (14, 16,

18). Thus, partial stomatal closure is a widespread response to

waterlogging. However, in all of the studies cited, and as reportedhere (Fig. 3A), leaf of flooded plants remained equal to or

greater than that of the control plants. Stomatal closure appearsto prevent a decrease in leaf 4, rather than being the result of a

leaf water deficit.Experiments with differential times of flooding permit certain

inferences to be made. Plants flooded in the morning showed no

changes in any measured parameter during the first 12 h (Figs. 1

and 3A). On the following morning, however, stomata open less

widely, and geremains below the control level on subsequent days.A brief water deficit can produce stomatal closure on day 1, but

has no long-term effects (Fig. 3C). The pattern of stomatal behav-

ior seen in evening-flooded plants can be viewed as a combination

of the effects induced by the other two treatments (Fig. 3B). That

is, there is an initial stomatal closure as the result of a decrease in

leaf 4. This occurs because the light comes on 12 h after flooding,and root conductance has decreased by this time (Fig. 4). Waterloss exceeds uptake, leaf decreases and leaves wilt, causingstomatal closure. Subsequently, there is a persistent partial sto-

matal closure unrelated to leaf 4,. It can be concluded that partialstomatal closure can prevent a decrease in leaf if a period of

transpiration follows the imposition of flooding. There is, however,the possibility that light might have modifying effects on the

response to root anaerobiosis other than that related to the flow of

the transpiration stream.

Interestingly, the early observations (17) on leaf scorching or

'white-spot disease' in irrigated alfalfa (Medicago sativa L.) maybe explained by our results on the time of flooding relative to

photoperiod. Flood irrigation of the field during the night resulted

in severe symptom development the following day, whereas irri-

gation only during the day was not injurious. As the leaf scorchingis due to water deficits in the leaves (23), the pattern observed in

the field bears a striking resemblance to that reported here.

At least three hypotheses are consistent with the observations:

(a) that waterlogged roots export some factor which causes closure

of stomata; (b) that waterlogged roots fail to export sufficient

quantities of some factor normally present in xylem sap which

promotes stomatal opening; or (c) that a reduction in phloemtransport to the anaerobic roots leads to a/buildup of assimilates

or growth regulators in the leaves which causes stomatal closure.

The delayed effect on stomata would be due to the time requiredfor transport and accumulation. Of course, some or all of these

mechanisms may be involved simultaneously.In waterlogged tomato plants, ACC export from the roots and

its conversion to ethylene in the shoot has been shown to cause

petiole epinasty (4, 6). The time courses for the initiation of

epinasty and stomatal closure during waterlogging are coincident

(Figs. 1; 2; and 3, A and B). However, we found no stomatal

response to ACC supplied in the transpiration stream (Figs. 5 and

6). This is in agreement with the lack of ethylene effects on

stomata of other species (13). Thus, one physiologically active

compound known to be transported in the xylem of waterloggedplants is not the causal agent.Root excision largely reproduced the effects of flooding on ge

(Fig. 6). This is in contrast to epinasty, where anaerobic roots

must be present for the response (10). Possibly the roots supplyfactors which promote stomatal opening or serve as a sink for

factors inhibitory of opening. This hypothesis is supported by the

work of Xu and Lou (26) with sweet potato (Ipomoea batatas)stem segments with a single leaf attached. Within 2 d after

excision, transpiration and g. were reduced to 10%o of the control

levels. If no adventitious roots were allowed to develop, ge re-

mained at the low level for many days. With the appearance of

adventitious roots, the stomata began to resume normal function

and transpiration increased. Excision of the adventitious roots

resulted in stomatal closure within I d. The role played by the

Nass ________intact

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Plant Physiol. Vol. 70, 19821512

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WATER RELATIONS OF WATERLOGGED TOMATO

roots was not water absorption, for they had an identical promo-tive effect when simply enclosed in a moist chamber, with wateruptake occurring through a lower portion of the stem lackingroots. Stomata of Fraxinus pennsylvanica also begin to reopen

during waterlogging coincident with the appearance of adventi-tious roots on the stem (18). Removing the roots as a sink bygirdling (Fig. 7) did cause stomatal closure with a time coursesimilar to that observed during flooding. Yet, flooding resulted infurther reductions in ge and transpiration beyond that caused bygirdling.ABA is the growth regulator most closely associated with sto-

matal closure, and waterlogging caused a 6 to 8-fold increase inABA content of tomato leaves (7). The accumulation of ABAassociated with stomatal closure during drought stress is triggeredby the loss of leaf turgor (15). As stomatal closure in waterloggedplants can occur without a decrease in leaf turgor, either some

other mechanism triggers the accumulation ofABA in the leaf, orABA is imported from other parts of the plant. Anaerobic stressmight promote the synthesis and export of ABA from roots as isthe case for ACC. However, this is inconsistent with the observa-tion that root excision produces effects similar to flooding (Fig. 6,Ref. 26). On the other hand, petiole girdling or sink removalresults in an accumulation of ABA in soybean (Glycine max L.)leaves (19, 21). A similar situation may occur during waterloggingdue to root anaerobiosis.The plant growth regulators generally considered to be synthe-

sized in the roots and transported in the xylem sap are GA andCK. These hormones can often promote stomatal opening (9), andtheir concentrations in xylem sap decline rapidly in waterloggedplants (25). Data on endogenous levels of GA and CK in associ-ation with alterations in stomatal behavior are badly needed (8).The possible adaptive significance of epinastic response to

waterlogging has been neglected. In tomato, not only does themain petiole change in angle, but each leaflet also assumes a morevertical orientation. This reduces the horizontal surface area forlight interception (Bradford, K. J., unpublished results) and theheat load (1, 5). Epinasty and partial stomatal closure may acttogether to restrict water loss soon after waterlogging, when rootconductance has decreased. The maintenance of high leafpermits some stomatal opening and the accompanying photosyn-thesis. In our own work (Figs. I and 2), changes in ge can largelyaccount for the reduction in transpiration, and the data are notprecise enough to distinguish an additional effect of epinasty. Thismay be due to the relatively low intensity and diffuse illuminationin the growth chamber. A larger influence of epinasty on waterloss would be expected under the intense and unidirectionalradiation in the field around midday.

Acknowledgment-The excellent technical assistance of Ms. Wendy Hall is grate-fully acknowledged.

LITERATURE CITED

1. BEGG JE 1980 Morphological adaptations of leaves to water stress. In NC Turner,PJ Kramer, eds, Adaptation of Plants to Water and High Temperature Stress.

John Wiley and Sons, New York, pp 33-422. BOYER JS 1972 Use of isopiestic technique in thermocouple psychrometry. I.

Theory. InRW Brown, BP van Haveren, eds, Psychrometry in Water RelationsResearch. Utah Agricultural Experiment Station, Utah State University, pp51-55

3. BRADFORD KJ 1981 Ethylene physiology and water relations of waterloggedtomato plants. PhD thesis. University of California, Davis

4. BRADFORD KJ, TC HSIAO, SF YANG 1982 Inhibition of ethylene synthesis intomato plants subjected to anaerobic root stress. Plant Physiol 70: 1503-1507

5. BRADFORD KJ, SF YANG 1981 Physiological responses of plants to waterlogging.HortScience 16: 25-30

6. BRADFORD KJ, SF YANG 1980 Xylem transport of I-aminocyclopropane-l-carboxylic acid, an ethylene precursor, in waterlogged tomato plants. PlantPhysiol 65: 322-326

7. HIRON RW, STC WRuGHT 1973 The role of endogenous abscisic acid in theresponse of plants to stress. J Exp Bot 24: 769-781

8. HsIAo TC, KJ BRADFORD 1983 Physiological consequences of cellular waterdeficits: an overview. In H Taylor, W Jordan, T Sinclair, eds, Limitations toEfficient Water Use in Crop Production. American Society of AgrqpomyMadison, WI In press

9. JACKSON MB, DJ CAMPBELL 1979 Effects of benzyladenine and gibberellic acidon the responses of tomato plants to anaerobic root enviroments and toethylene. New Phytol 82: 331-340

10. JACKSON MB, K GALEs, DJ CAMPBELL 1978 Effect ofwaterlogged soil conditionson the production of ethylene and on water relationships in tomato plants. JExp Bot 29: 183-193

11. Koller HR, JH Thorne 1978 Soybean pod removal alters leaf diffusion resistanceand leaflet orientation. Crop Sci 18: 305-307

12. KRAMER PJ, WT JACKSON 1954 Causes of injury to flooded tobacco plants. PlantPhysiol 29: 241-245

13. Pallaghy CK, K Raschke 1972 No stomatal response to ethylene. Plant Physiol49: 275-276

14. PEREIRA JS, TT KoZLOWSKI 1977 Variations among woody angiosperms inresponse to flooding. Physiol Plant 41: 184-192

15. PIERCE M, K RAscHKE 1980 Correlation between loss of turgor and accumulationof abscisic acid in detached leaves. Planta 148: 174-182

16. REGEHR DL, FA BAZZAZ, WR BOGGESS 1975 Photosynthesis, transpiration, andleaf conductance of Populus deltoides in relation to flooding and drought.Photosynthetica 9: 52-61

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