Plant Physiol. (1968) 43, 515-521

Photosynthesis and Transpiration of Monterey Pine Seedlings as a Function of Soil Water Suction and Soil Temperature 0. Babalola, L. Boersma, and C. T. Youngberg Department of Soils. Oregon State University, Corvallis, Oregon 97331 Receive(d October 16, 1967.

A bstract. Rates of photosynthesis, respiration, and transpiration of Monterey pine (Pinus radiata D. Don) were measured under controlled conditions of soil water suotion and soil temperature. Air temperature, relative humidity, light intensity, and air movement were maintained oonstant. Rates of net photosynthesis, respiration, and transpiration decreased with increasing soil water suction. The decrease in the rates of net photosynthesis and transpiration as a function of the soil temperature at low soil water suctions may be attributed to changes in the viscosity of water. At soil water suctions larger than 0.70 bars rates of transpiration and net photosynthesis may be affected in the same proportion by changes in stomatal apertures.

A plant is constantly being influenced by its abilitv the literature is contradictory. Whereas environment. Soil temiperatture and soil water suc- large decreases in the rate of photosynthesis of tion are important environmental variaibles. It is leaves of apple trees du.ring the depletion of soil generallly accepted thait low soil temperature de- water were observed (18), no reduction in phato- creases waiter uptake by plants by the combined synthesis of Ladino clover occulrred until the avail- effects of a decreased permeability of the root able soil water was neairly depleted (19). Maxi- membranes and increased viscosity of the water mum rates of photosynithesis do not always occur (11). Leaf waster deficit of orange trees was when the water supply is plentiful. Balsam Fir higher at low soil temnperatures than at high soil and White Fir showed a maximum rate of pho-to- temperatures both in the field and in air conditioned synthesis after mu-ch water loss had taken place cham.bers (4). Watermelons and cotton absorbed (5) and a simil-ar observation was made for Pinus only 20 % as mutch water at 100 as at 250 and densiflora and Cryptomeria Japonica (16, 17). For loblod-ly and slash pine albsorbed only 40 % as much some pllants an initia;l increase in resp ration rate water at 100 as at 250, while a comiparable figure has been oibserved tupon a decrease in soil water for white and red pine was 60 % (9). Transpira- content, followed by an eventual sharp decrease, tion of sunflowers varied little with soil tempera- after continued waiter loss (3). Other plants how- ture between 12.80 and 37.80, btut dropped rapidly ever exhib,t an immediate and continued decrease below 12.80, was reduced to half at 3.30 and ap- in respiration rate when water availability is de- proached zero at 00. The wilted plants recovered creased. rapid!ly w1hen the soil temperature was raised (6). The specific objectives of the present study were Few studies have considered the influence of to (1) qutantitatively evaluate rates of photosyn- soil water avail1ability on photosynthesis and res- thesis, respiration, and transpiration at specified piration (2). Clear identific,ation of plant response values of soil water suction and soil temperatuire, to changes in soil water availatbility requires rig- with other environmentail parameters maintained orotus control of this variable. The transpiration constant, and (2) attempt to identify the mechanism ra,te of plants is at least in part linked to the soil by which the observed differences were broutght water availlabi,lity by means of the stomatal control about. mechanism (10, 15, 20). At constant soi,l water content stomatal dlosutre was olbserved even at low soi,l water suctions (7). Photosynthesi,s may be Materials and Methods limited by dehydration of the protoplasm which reduces its photosynthetic capacity (12), and be- Control of Soil Water Suction and Soil Tem- cause stomatal closture reduces the stupply of carbon peratuire. Control of soil water suction was ob- dioxide to the chloroplast. Under certain condi- tained by inserting thin slabs of soil, encased in tions the rate of photosynthesis is less affected by semi-permeable membranes, into osmotic solutions stomatal movement than transpiraition is, because (7, 21). The chambers were sturrotunded by a water the diffusion path for CO, is longer than that for jacket connected to a constant temperature bath H2O (1). On the dependency of the rates of (fig 1). The soil water suction in the soil slabs photosynthesis and respiration on soil water avail- was controlled by the concentration of the osmotic 515 516 PLANT PHYSIOLOGY

GAS OPEMNS TUK tions were used, correspondinig to the osmotic pressures of 0.35, 0.70, 1.50, and 2.50 bars (21). MIN PLANTW b seed- Leaf areas were estimated by a method base(d lug and connected toA the frared analy zer. on tihe assuimption that the nee(dle cross sections are triangutlar. Needles were divided into 18 length solultion anbd the 'soil temperasture was controlled h) classes, viz: 9.5 to 9.0, 9.0 -to 8.5, . 1.0 to 0.5 the temperaGtucre of the bath. and the average suirface area per need,le for eaclh The soil cells inwjhic h the plants were growne size class was multiplied by the nuimber o,f nee(dles consisted of a frame with removable covers (fig 2). in the class. Suimming these lprodllcts over all The soil slab was 0.8 cm thick, 10.0 cm wide, and classes gave the total surface area per seedlilg. 30 cm high. The soi,l used was a mrixtture of a Measuiren1icn t of' Photosynth esis, Respirationi, and loamy fine sand and a clay loam. A mechaniical Transpirationi. A constant-water level dlevice oper- analysis of the mixtture showed 39.0, 30.0, and ating on the principle of a mariotte bottle was 31.0 % sand, silt and clay respectively. Each cell connected to each osmotic chamber. Tihe device was filled with material passed throuigh a 2 mm was adjusted to maintain a frce water surface in sieve and packed to a bulk density of abouit l g the slits in the cover, about 0.5 cm below the upper per cm3. side of the 1.2 cm thick cover (fig 1). The rate Plants were grown from seed in the cells for of trainspirationl was obtained by reacling the wvater about 6 months, at wvhich time the removable sides levels in the graduated devices at the begiiir in1g wvere replaced with a visking membrane. The and end of a test period, 2 houirs lonig, duirinig v hich wd(ltll of the cells xv'as selected to fit loosely inlside photosynthesis measturements were taken. A reli- a flattened membrane cylinder with a diameter of able measurement was obtained by takinig several 13.5 cm. The membrane was sealed at the lower readings dturing a test period and(l plotting the en(I by folding it over several times and clamping amotunt o,f water tused as a fuinctioln of time. A it with a plastic looseleaf binder. The membrane straight line sldoiil(1 result if steady state conditions was held in place at the tipper end by 2 braces prevailed andl the device was flnctioniing properly. (fig 2). The cells were ini.erted into the osmotic Rates of net photosynthesis wN,ere measuired by solutioin by gently low erinig them through slits recording the rate of CO., consuimption with a (1.3 X 13 c,m) in the cover, and came to rest on Heath recor(ler co,nnected to an infra-red gas the braces. analyzer. A closed system was obtained by placing The o,smotic soluttion was made iip) of poly- a cuivette over the plants onto a slotted "flo,orplate" ethylene glycol 6000 (carbowax). Foulr coincentra- through which the plant stems passed (fig 1). Trhe slits were sealed with modeling c,lay. Rates of dark BRACE respiration were obtained by mea!suiring CO. evollu- tion in the dark. The period of measurement was usniallly about 5 minuttes. The lpulmp to the analyzer was rtunning at all times, making the CO,, concein- tration in the cuivette, at the time it was puit inI place equa,l to the CO. level in the growth room. To avoid raising the CO, level in the growth room by hu,man respiration, the operator was fitte(d with a mask and 'ho-ses leading to the otitside, providing a breathing sy,stem isolated from the growth room atmo,sphere. Proced-ure. Mionterey pine (Pinus radiata D. Don ) seeds we,re pregerminated, planted in soil cells and grown in the greenhouse at night tempera- tuires of 15° and day tem,peratuires of 260. TI'he plants were irrigated twice each week. The maxi- muim soil water suiction seldolm exceedekl 0.70 bars. This was established by determininig the amo,unt of FIG. 2. Schematic diagram of the soil cell used, water in the soil thronigh periodic weighing. The showing removable cov er and braces. soil was 'initially fertillized to conltainl abou"t 150 ppm BABALOLA ET AL.-WATER STRESS AND SOIL TEMPERATURE EFFECTS 517

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Insert BABALOLA ET AL.-WATER STRESS AND SOIL TEMPERATURE EFFECTS 519

N, 100 ppm P, and 100 ppm K. At the time of the net photosynthesis are plotted as a functioni of the experiment the plants were approximately 6 months viscosity of water. At a given soil waiter suction olld and had developed good root systems (fig 3). the rate of net photosynthesis was a function of The celils were moved to the growth room, provided viscosity. At soil water suctions of 0.35, 0.70, with membranes ulpon removall o,f the sides and 1.50, and 2.50 bars the slopes are 0.95, 0.73, 0.70, immersed in the chambers, maintained at that time alnd 0.68 respectively. at a temperature of 100. It is assumed that the viscosity of water and in When the systems reached equtilibrium measture- particullar the temperature coefficient of the vis- ments were made of rates of transpiration, photo- cosity of water represents a reasonable approxima- synthesis, and respiration, and leaf temperatures. tion. of the magnitude of simiilar quantities for the Uipon completion of these measurements, the soil plant fluids. At a soil water suction oif 0.35 bars temperature was raised to 15.60. Two days were the change in rate of photosynthesis is inversely allowed for the system to come to equilibritum at prop}ortional to the change in viscosity, stuggesting this temiperature and measturements were folilowed that a laminar flow process controls the overall in time by measurements at 21.10 and 26.70. The relation. At higher soil water suctions the rate of seedlings were then harvested for leaf areai deter- decrease in the rate of photosynthesis is less ,than mination. that predicted by the inverse viscosity relationship. The effects of soil temperatu,re on photosynthesis Results suggest that a physical process with a low Q,o value and Discussion rather than a chemical process controls the overall reflation. Photosynthesis. Rates of net photosynthesis are Respiration. Resullts of the respiration measuire- showxn in fgutre 4 as a ftunction of soiil water stuctioni ments are shown in table I. The rate of respira- for 4 soil temperatures. The rate of net photo- tioIn decreased considerably as the soil water suction synthesis dropped sharply between soil water stuc- increased but soil temperature seems to have had tions of 0.35 and 0.70 bars. little effect on the rate of respiration of the shoots. Opening of stomates requiires a reducition of the Assuming that the products necessary for leaf CO, concentration in the mesophyll cells (8, 14). respiration were available in the shocts and that It was hypothesized th,at the meastured re(duction in physical changes in the above grounid environment the raite of photosynthesis at constanlt soiil water did not resuilt from a change in the soil1 tempera- stuction restulting from a decrease of the temniperature tture, no change in the rate of respiration should be of the root system could be mediated by a (lecrease expected. The rate of respiration of tihe total in the rate of translocationi of photosynthates re- plant system was not meastured. It is possible that sulItin,, from a change in viscosity. Stomatal the rate of respiration of the below groutind parts closing may occur duie to an increase in the CO.. of the plant were influenced considerably more l)y concentration, brouigh't about by slow removal of a change in soil temperature. photosynthates. In figulre 5 the measulredl ra-tes of Trmaspiration. Resuilts of the transpiration

Table 1. Measured Rat.s of 7Transpiration. iVet Photosyntthesis,. and Respirationz of Mloniterey Pinie Seedlings as a Fmicetion of Soil Temiperature antd Soil [Fater Suction Soil Soil water Net temlp suction Transpiration photosynthesis Respiration Bars 10-5 cn13 cmnr2 sec-1 10.0 0.35 0.172 2.90 1.43 0.70 0.164 2.56 1.31 1.50 0.150 2.00 0.97 2.50 0.139 1.66 0.87 15.6 0.35 0.381 3.46 1.59 0.70 0.330 2.70 1.49 1.50 0.264 2.30 1.07 2.50 0.197 1.99 0.86 21.1 0.35 0.52-0 4.06 1.42 0.70 0.392 3.03 1.29 1.50 0.278 2.44 0.97 2.50 0.217 2.23 0.87 26.7 0.35 0.606 4.28 1.34 0.70 0.450 3.22 1.30 1.50 0.300 2.64 1.09 2.50 0.236 2.36 0.97 520 PLANT PHYSIOLOGY'

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FIG. 4. (top, left) Rate of net photosynthesis as a function of soil water suction at 4 levels of soil temperature. FIG. 5. (top, right) Rate of net photosynthesis as a function of the viscosity of water, at 4 levels of soil water suction. The dotted line indicates that for laminar flow the flow rate is inversely proportional to the viscosity (m = 1). FIG. 6. (bottom, left) Rate of tranispiration as a function of soil water suctioIn at 4 levels of soil temperature. FIG. 7. (bottom, right) Ratio of rates of trainspiration and net photosynthesis as a funictioni of soil temperature, at 4 levels of soil water suction.

measurements are shown in figutre 6 whe,re the sists of a high temperature part (15.6°-26.70) and rate of transpiration is plotted as a function o.f the a low temperature part (10.0°-15.6°) . When the Soill water suction for 4 soill temperatures. soil temperature was increased from 10.00 to 15.60 The rates of transpiration decreasedl with in- the rate oif transpiration inicreased much faster than crealsin,g soil water suction. Alt a given soil walter the rate of photosynthesis. At the low soi,l tem- suction, the rate of transpi,rajtion decreased witlh peratures the rate of water uiptake was limiited by decreasing soil temiperature. Figure 7 shows the the permeability of the membranes. This phenom- ratio oif transpiration to net phlotosynthesis a,s a enon was described by Kuiiper (13). The transition function of !soil Itemperatture. The relationsh,ip con- between the high temperatulre range and the low BABALOLA ET AL.-WNATER STRESS AND SOIL TEMPERATURE EFFECTS 521 temperature range seems to be ajbrupt at about 7. Cox, L. MI. AND L. BOERSMA. 1967. Transpiration anld soil water 150. The water permeabillity of the root cels as a function of soil temperature stress. Plant Physiol. 42: 550-56. reached its saturation 'level at a temperature between 15.60 8. KETELLAPPER, H. J. 1963. Stomatal physiology. 10.00 and 15.60. At soil temperatures above Ann. Rev. Plant Physiol. 14: 249-67. and a soi,l water suction of 0.35 bars, the rate of 9. KRAMER, P. J. 1942. Species differences with re- transpiration increased faster than the rate of net spect to water absorption at low soil temperatures. photosynthesis, when the soil temperature was in- Am. J. Botany 29: 828-32. cireased. At soi;l temperatures above 15.60 and soil 10. KRAMER, P. J. 1949. Plant anid Soil Water Re- water suctions of 1.50 and 2.50 bars the ratio was lationships. MIcGraw-Hill. New York. 347 p. These resullts indicate that at high soil 11. KRAMER. P. J. 1956. Physical aind physiological constant. of water suctions the rates of transpiration and net aspects of water absorption. Ini: Encyclopedia Plant Physiology. Vol. 3. Springer-Verlag, Ber- were conitrolled by the same mecha- photosynthesis lin. 124-29. ni,sm, while at low soi,l water suctions the rate of 12. KRAMER, P. J. 1963. \Vater stress and plant transpiration was controlled by a separate mecha- growth. Agron. J. 55: 31-3'5. nism. 13. KUlPER, P. J. C. 1964. Water uptake of higher It is suggested that at high soil water suctions plants as affected by root temperature. MIededel. the rates of transpiration and net photosynthesis are Landbouwhoge,school Wageningen 64: 1-11. controlled by stomatal aperture. At low soil water 14. LEVITT, J. 1967. The mechanism of stomatal ac- suction,s the rates of transpiration are controlled, at tion. Planta 74: 101-18. F. L. AND E. J. SPENCER. 1957. Ex- a presumably viscosity, 15. IMILTHORPE, lea,st in part, by parameter, perimental studies of the factors controlling tranis- which regulates the waiter supply to the leaves. piration. III. The interrelations between trans- piration rate, stornatal movement anid leaf water Literature Cited content. J. Exptl. Botany 8: 413-37. 16. NEGISI, K. AND T. SATOO. 1954. The effect of drying of soil on apparent photosynthesis, tranis- 1. BIERHUIZEN, J. F. AND R. D. SLATYER. 1965. Ef- piration, carbohydrate reserves, and growth of feot of atmospheric concentration of water vapor seedlings of Akamatu (Piniiis densiflora). J. Ja- and CO., in determining transpiration-photosyn- pan Forestry Soc. 36: 66-71. thesis relationships of cotton leaves. Agr. Meteor. 17. SATOO, T. AND K. NEGISI. 1961. Experiments on 2: 259-70. the effects of soil moisture oil photosynthesis of 2. BOERSMA, L. 1967. Respiration rates and water conifer seedlings. In: Recent Advances in Bot- availability: plants. In: Environmental Biology. any. University of Toronto Press, Toronto. p Philip L. Altman and D. S. Dittmer, eds. Fed 1317-21. Am, Soc. Exptl. Biol. Bethesda, Maryland. p 18. SCHNEIDER, G. WT. AND N. F. CHILDERS. 1941. In- 477-79. fluence of soil moisture onl photosynthesis, respira- 3. BRIx, H. 1962. The effect of water stress ol1 the tion and transpiration of apple leaves. Plant rate of photosynthesis and respiration in tomato Physiol. 16: 565-83. planit and loblolly pine seedlings. Phvsiol. Plan- 19. UPCHURCH, R. P., M. L. PETERSON, AND R. M. tarum 15: 10-20. HAGAN. 1955. Effect of soil moisture content 4. CAMERON, S. H. 1941. The influence of soil tenii- on the rate of photosynthesis aild respiration in perature oii the rate of transpiration of young ladino clover (Trifoliuint rpepCns L.). Plant Phy- orange trees. Am. Soc. Hort. Sci. Proc. 38: siol. 30: 297-303. 75-79. and respiration in 20. Woo, K. B., L. BOERSMA. AND L. N. STONE. 1966. 5. CLARK, J. 1961. Photosynthesis model of the transpiration wvhite spruce and balsam fir. New York State Dynamic simulation University, College of Forestry, Technical Publi- process. Water Resources Research 2: 85-97. cation No. 85. Syracuse, New York. 72 p. 21. ZUR, B. 1961. The influence of controlled soil 6. CLEMENTS, F. E. AND E. V. MARTIN. 1934. T(he moisture suction, relative humiiidity and initial salt effect of soil temperature on transpiration in status on chloride uptake by sunflower plants. Helian thuts aiinuuiis. Plant Physiol. 9: 619-30. Ph.D. thesis. University of California, Davis.