LEAF DIFFUSIVE RESISTANCE AND WATER ECONOMY IN CARBON DIOXIDE-ENRICHED RICE PLANTS
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1 New Phytol. (1986) 104, ^ ^ 5 LEAF DIFFUSIVE RESISTANCE AND WATER ECONOMY IN CARBON DIOXIDE-ENRICHED RICE PLANTS BY M. A. H. KHAN* AND A. MADSEN Department of Plant Physiology and Anatomy, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Copenhagen V, Denmark {Accepted 10 June 1986) SUMMARY The leaf diffusive resistance to the transfer of water vapour and COj exchange in rice plants {Oryza sativa L., cv. IR-20) measured from the late vegetative stage to maturity, varied in response to differing CO^ enrichments. The leaf diffusive resistance of plants treated with 900 /tl r* CO2 ranged from one-half to twice that of the control plants (330//ll"'CO2).This difference was more pronounced during the heading and ripening stages. In plants treated with 600 /tl ri CO2, the diffusive resistances appeared to be smaller than in the control plants for most of the day. In the diurnal cycles, resistances were highest during the early morning and before sunset, the maximum again occurring in the plants treated with 900 fi\ T' CO^. The rate of transpiration was inversely related to the diffusive resistance, and was 20 to 100 % lower in the plants treated with 900 //I T' COj than in the controls, both in the seasonal and diurnal cycles. In plants treated with 600 //11"' CO^, the rate of transpiration was lower than in the controls in the morning but distinctly higher during the afternoon. However, the integrated total daily transpiration in 600 /il T' CO2 did not exceed that of the controls. In all cases, COa-treated plants, through their increased biomass production and economic yield, appeared to have a higher water use efficiency than the control plants. Key words: Rice, COj enrichment, diffusive resistance, transpiration. INTRODUCTION In the natural environment, the growth and development of plants are the integrated results of many interacting factors, but the limiting or regulatory effects of just some of these factors may determine the fitness of the plant in a cultivated ecosystem. Water economy and leaf diffusive resistance have been widely investigated in many cultivated crops, including rice (Kanemasu & Tanner, 1969; Turner &Begg, 1973; Imai & Murata, 1976; Turner & Heichel, 1977; Sandanam, Gee & Mapa, 1981). However, COg-induced changes in diffusive resistance (notably over long periods) have received very little attention in previous ecophysiological studies in rice plants. Stomatal conductance not only affects the loss of water but also growth, through its effects on COj exchange and plant water status (Rosenberg, 1974; Salisbury & Ross, 1978). It is therefore essential to understand how stomata behave in COa-enriched environments. The experiment described here investigated the leaf diffusive resistance and the release of water vapour to the atmosphere in rice plants grown in atmospheric COj (330/<1 T'), or atmospheres enriched to 600 or 900 //.I T^ COj from the late vegetative stage to maturity. * Present address: Department of Crop Botany, Bangladesh Agricultural University, Mymensingh, Bangladesh X/86/ $03.00/ The New Phytologist
2 2i6 M. A. H. KHAN AND A. MADSEN MATERIALS AND METHODS Seedlings of rice (Oryza sativa L., cv. IR 20) were grown in plastic containers (20x17x18 cm) under greenhouse conditions with supplementary light from 15 March At the late vegetative stage of growth, i.e. in late August, two pots containing uniform plants (which were selected previously) were placed in each of three growth cabinets, which were subjected to 330 (atmospheric), 600 and 900 ju,l 1"^ COj. Air containing the required level of COj entered the cabinets at a rate sufficient to replenish the air 15 times per hour. The desired concentrations of COg were achieved by adjusting the low-flow rotameter and by continuous monitoring of the air with an infrared gas analyzer (type URAS 1, Hartman & Braun AG, FRG). The COg concentrations in the enriched chambers were controlled to and //11"', and the atmospheric level was fil 1"\ When the door of the cabinet was opened for a short period for watering, measurement, etc., there was large but brief deviation from these CO2 concentrations. CO2 enrichment was maintained from 0600 to 1800 h each day. The growth cabinets were naturally illuminated through the glass roof of the greenhouse, but each cabinet had supplementary light from a Philips HPLR 700 W lamp suspended at a height of about 25 cm above the cabinet. This, in addition to the natural light, proved about 133/.*E m"^ s'^ photosynthetically active radiation (PAR) in the centre of the cabinet. The supplementary light was used daily during the period of COj enrichment and was autocontrolled. The minimum temperature in the chambers was controlled by blowing the air through thermostatically controlled heating wires. Although this procedure effectively controlled the day/night minimum temperatures to about 22/18 C in the early part of the experimental period, in June/July when the solar radiation was high, the day/night temperatures on some occasions exceeded 35/28 C. To avoid such excessive temperatures mist irrigation was applied at intervals. The pots were kept watered above fleld capacity so that water availability never became a limiting factor. All other environmental parameters in the three cabinets were identical except for COg concentration, which was the only experimental variable. After the plants had been allowed to acclimatize for 7 d in the growth cabinets, the flrst diffusive resistance measurements were made at the late vegetative stage using a steady state porometer (model LI-1600 from LI-COR, Nebraska). Measurements were subsequently made at intervals of 1 to 5 d depending on weather conditions, and continued until maturity. During the vegetative stage, diffusive resistance was measured on young fully expanded leaves. From ear emergence onwards, flag-leaves were used and sequential measurements were made on the same leaves. Five to six leaves (from the main culm and tillers) were included in each set of measurements for each of the growth cabinets. All measurements were carried out on the abaxial surface of the leaf starting at 1300 h local time. As the time required for each measurement was less than a minute, the measurement period never exceeded 6 min for a single cabinet. Leaf temperature, relative humidity, and PAR were also simultaneously recorded by the multifunction steady state porometer.
3 Responses of rice to CO^ enrichment 217 RESULTS AND DISCUSSION Seasonal trends in leaf diffusive resistance and transpiration The mean data obtained from two or three consecutive days of observations from the late vegetative stage to maturity are plotted in Figure 1. The leaf diffusive resistances clearly differed between the three treatments [Fig. l(a)]. Resistances were largest in 900 /il 1"^ CO^ and smallest in the plants in 600 /tl 1 ^ CO^. Diffusive resistances in 900 fil I'' CO^ increased from 0-7 s cm'^ at the late vegetative stage to about 1-6 s cm'i at ear formation and then gradually decreased to 0-8 s cm-i at the late grain filling stage. Diffusive resistances in 330 and 600 fil 1-1 CO, ranged between 0-5 and 0-8 s cm'i and 0-3 to 0-5 s cm ^ respectively during the late vegetative stage and the late grain filling stage. As ripening started, the resistances increased by more than three-fold in all treatments. Vegetative Booting Earing Late gram filling Early grain filling Yellowing Fig 1 Seasonal trends in leaf diffusive resistance (a) and rate of transpiration (b) in rice plants grown at atmospheric (O), 600 ( ) and 900 (D) /d I'' CO, enrichment. The vertical bars represent the standard errors of the means. The maximum rates of transpiration were found in the plants treated with 600 /tl 1-1 CO2, although the rates fiuctuated greatly during the observation period [Fig l(b)] In general, the rates of transpiration were about 10 to 60% higher in 600/tl 1-1 CO2 and 20 to 100% lower in 900/tl T^ CO, than in the controls at 330/tl 1-1. These differences were most pronounced between ear formation and grain filling. During the booting stage, however, the differences in diffusive
4 2i8 M. A. H. KHAN AND A. MADSEN resistance and transpiration between plants in 330 and 600/y,l 1"'COj were negligible. Imai & Murata (1976) subjected rice seedlings with five to seven leaves to 350, 1050 and 3500 /A 1"' CO2 in transparent growth chambers under natural conditions and observed a differential response pattern in the rates of transpiration. The Table 1. Effect of CO^ enrichment from the late vegetative stage to maturity on growth and reproductive attributes of rice plants Treatments (/*! 1"' CO2) Attribute Atmospheric Plant height (cm) 2. Fertile tillers 3. Ear length (cm) 4. Kar density (florets cm~') 5. Grain number ear"' 6. Grain fertility ("/ ) 7. Weight grain"' (mg) 8. Grain weight (g plant"') 9. Main shoots DM (g plant-') 10. Regrowth DM (g plant"') 11. Biological yield (g plant"') 12. Harvest index O + 2-O ± ± ± ± ± ± ±O O-27±O ± diffusive resistances calculated from leaf to air temperature differences and water vapour and CO.^ concentration (Imai & Murata, 1978b) revealed that the aftereffects of CO2 enrichment, which persisted for 8 to 10 d, resulted from reductions in mesophyll resistance with increasing COj concentration up to about 500 /il 1~'. With further increase in COj content, the mesophyll resistance together with the boundary and stomatal resistances were greatly increased. Akita & Tanaka (1973) and Akita (1980) also reported reduced rates of transpiration at COj levels above 1000//I 1~', which were associated with high diffusive resistances. However, the references cited above, although confirming the general response pattern for stomatal behaviour in COg-enriched rice plants, did not explain the ontogenetic progression because the treatments were applied only for a few days. However, seasonal changes in leaf diffusive resistance have been widely used as an indicator of stomatal responses to environmental variables and water stress in many species (Kanemasu & Tanner, 1969; Brown & Rosenberg, 1970; Gee & Federer, 1972; Turner & Begg, 1973; Jordan, Brown & Thomas, 1975; Turner & Heichel, 1977; Sandanam et al., 1981). In most of these studies, an effect of leaf age on stomatal response has been demonstrated. Generally, low atmospheric CO2 concentrations cause stomata to open more widely irrespective of the level of irradiance, and high COj contents tend to inhibit stomatal opening partially, thus increasing resistance to the diffusion of COj and water vapour (Harper, 1977; Salisbury & Ross, 1978). This general principle was reflected by the results for plants treated with 900 fix 1 ' CO.^ but confounded by
5 Responses of rice to CO^ enrichment 219 those for the plants in 600 //I T^ CO,,. The explanation for these difterential responses in leaf diffusive resistance remains obscure. However, it is evident from Table 1 that all the plant attributes responded positively to CO.^ enrichment, particularly with respect to ear capacity and biological yield. Even the late-formed tillers that appear after maturation of the main culm and tillers tended to accumulate more biomass in CO.^-enriched plants. The trend of the present data (Table 1) and the findings of other workers (Yosida, 1976; Tanaka, 1976; Imai & Murata, 1978a; Akita, 1980) suggest that growth in rice plants is favoured by increasing concentrations of CO^, even though the leaf diffusive resistances were different at different levels of COj (Fig. 1). Although the growth suppression observed during the early vegetative stages in plants treated with 900/il 1 ^ CO^ in previous studies (M.A.H.Khan, unpublished Ph.D. thesis) did not suggest any increase in the rate of photosynthesis, the subsequent growth promotion at the late vegetative stage indicated a two-phase responsiveness in rice plants to high CO^. Such a growth reduction at the early vegetative stage, and growth promotion at subsequent stages, were also reported by Imai & Murata (1978a). This promotory effect was more likely to have originated from reduced photorespiration at CO,, concentrations above 600 /il T^ (Akita, 1980) rather than increased photosynthesis, since diffusive resistances remained high, even at that stage of plant growth (Fig. 1). However, the possibility of increased photosynthesis in 900 //11"' CO^ cannot be entirely eliminated since the diflfusion of COj depends on the concentration gradient (Salisbury & Ross, 1978), and stomatal resistance exerts relatively greater effects on transpiration than on photosynthesis (Gaastra, 1963). Nevertheless, in all cases, CO^ concentration of the atmosphere appeared to be the dominant force controlling the yieldcontributing characters of rice (Table 1). Higher diffusive resistances and reduced rates of transpiration during ripening were obvious in all the treatments as the leaves aged. The age-dependent response of diffusive resistance and transpiration seemed to be related to partial loss of stomatal activity due to aging. Although diffusive resistance and transpiration measurements could not be carried out from the seedling stage because of unavailability of the instrument, a knowledge of the changes which occur between the seedling stage and maturity is essential for a full understanding of plant reactions to CO^ enrichment. In wheat, whole-season CO^ enrichment in growth cabinets showed that as the degree of water limitation increased, the relative enhancement of yield by CO^ enrichment increased (Gifford, 1979). Such a wholeseason CO2 enrichment in association with water stress may signiflcantly assist the assessment of future water requirements in rice plants as global CO., concentration of the atmosphere increases. Diurnal changes in diffusive resistance and transpiration The effect of CO^ enrichment on the diurnal pattern of variation in leaf diffusive resistance and transpiration in rice was measured at hourly intervals from 0800 h to sunset on a clear sunny day (3 October 1980) during the grain filling stage. The results are presented in Figure 2 and the corresponding micrometeorological parameters are shown in Table 2. Early in the day (0800 h), diffusive resistance was high in all treatments, especially in atmospheric (3 s cm i) and 900/ill"iCO2 (4-5scm-i) [pig 2(a)]. By 0900 h, diffusive resistances in both atmospheric and 900 //I U^ CO^ had sharply decreased to about 1 and 2 2 s cm ^ respectively, and the difference between the plants in atmospheric and
6 22O M. A. H. KHAN AND A. MADSEN 600/il 1"^ COj was negligible. After 1000 h, the decrease in diffusive resistance was gradual and small in all the treatments until late afternoon. However, the resistances in 900 /tl 1"^ COg remained more than double those in the plants in atmospheric and 600/tl 1"' CO^. Shortly before 1600 h, the supplementary light Local time (h) Fig. 2. Diurnal changes in leaf diffusive resistance (a) and rate of transpiration (b) at atmospheric (O), 600 ( ) and 900 (D) /*' '"' CO2 content in rice plants. The vertical bars represent the standard errors of the means. was discontinued to monitor the stomatal response in the falling PAR. After 1600 h, as the PAR dropped (Table 2), leaf diffusive resistances increased sharply from less than 0-5 s cm"^ to more than 5 s cm"i in both atmospheric and 900/tl r^ CO2; in 600/^1 1"^ COg, the increase was only from 0-3 s cm"i to less than 1 s cm"i. With a further decrease in PAR, the highest resistance of about 15scm"i was achieved by the plants in 900/ilT^ CO^, with small increases being observed in atmospheric and 600 /tl 1"^ CO^. The rate of transpiration was very low during the morning, gradually increasing from less than 4 /tg cm"^ s~i by noon in atmospheric and 600 /i\ 1"^ COj, respectively [Fig. 2(b)]. From noon until 1400 h, the rate of transpiration in control plants was relatively constant, while in 600 ja'^ CO2 a further increase to about 30 jig cm"^ s"^ occurred. The rate of transpiration in 900/^r^ CO2 increased gradually from a very low value in the early morning until afternoon, but remained less than half that of the plants in atmospheric CO^ for most of the day. As PAR dropped during the late afternoon, transpiration decreased sharply to its lowest level and eventually ceased entirely at sunset at 1800 h. However, the plants treated with 600 /*1 1"^ COg still continued to transpire slowly for about 1 h after sunset.
7 Responses of rice to CO^ enrichment 221 s 2 K 1 o S o i OO ooooooooooo O ooooooooooo ^
8 222 M. A. H. KHAN AND A. MADSEN The stomatal pores, through which gaseous transfer occurs, are known to be affected by photosynthetic quantum fiux, ambient COj concentration, leaf to air vapour pressure difference, leaf water status and leaf temperature (Hall, Schulze & Lange, 1976; Jarvis, 1976). The rice plants tested here were grown under conditions of non-limiting water supply, where all other climatic factors except COj concentration were essentially identical. Leaf temperature and relative humidity were inversely related to each other (Table 2), thus allowing more transpiration to occur as PAR increased to a maximum around noon. Leaf temperature is one of the most important factors determining energy exchange between the leaf and its environment and is strongly correlated with the physiological reactions of the plant (Gates, 1965). Therefore, increases in transpiration with increasing PAR and leaf temperature are predictable (provided the stomata remain open). However, mean leaf temperature was at least 1 C lower in COj-enriched plants, irrespective of the level of PAR, for most of the day (Table 2). Imai & Murata (1976), in contrast, observed that leaf temperature was increased by 1 C in soybean and maize seedlings exposed to 1050 and 3500/il 1-1 COg. This difference in the response of leaf temperature probably originated from differences in stomatal resistance, radiation loading, leaf orientation, ventilation within the enclosure, plant age, cultivar and growing conditions. These plants were tested in plastic enclosures in the field where the radiation load on the leaf surface was high. Transpiration was limited by high diffusive resistance at 1050 and 3500/tl l-i COg and thus the excess energy could not be freely dissipated from the leaf surface. The amount of water transpired by rice plants exposed to 600 /tl I"! COg was lower in the morning and higher in the afternoon than in control plants [Fig. 2(b)], although the diurnal trends in diffusive resistance were similar [Fig. 2(a)]. The mean hourly rate of transpiration for any one day, therefore, might not be as high as in 600 //I \~^ COg as the data for seasonal variation support, where the measurements were made only at 1300 h. Thus it can be predicted that the amount of water transpired by the plants in 600 /tl l^i COj during their whole ontogeny may have little adverse consequence on the efficiency of water use. This has also been indicated by the increased biomass production and grain yield (Table 1). The rapidity with which the stomata closed at the approach of darkness, as indicated by the cessation of transpiration, accomplished a high diffusive resistance in the plants in 900/il L' COj (Fig. 2). The importance of night-time partial stomatal opening, which is uncommon in most plant species, has been demonstrated by Muchow et al. (1980) in kenaf at both high and low soil moisture status with varying temperatures. The partial stomatal opening, as indicated by dark transpiration in 600 /A l^i CO^-treated plants [Fig. 2(b)] occurred, however, only for a short duration of about one hour (not shown in Fig. 2), probably because COg enrichment was also simultaneously discontinued with the onset of darkness at 1800 h. Further studies of night-time stomatal opening at various levels of COj enrichment are required to confirm the results presented here. ACKNOWLEDGEMENTS We thank the Danish International Development Agency (DANIDA) for financial support, and Professor R. Rajagopal and Dr A. S. Anderson of the Royal Veterinary and Agricultural University, Copenhagen for their criticism of this paper.
9 Responses of rice to CO^ enrichment 223 REFERENCES AKITA, S. (1980). Studies on the differences in photosynthesis and photorespiration among crops. II. The differential response of photosynthesis and photorespiration and dry matter production to carhon dioxide concentration among species. Bulletin of the National Institute of Agricultural Sciences. Scries D {Physiological Genetics), 31, AKITA, S. & TANAKA, I. (1973). Studies on the mechanism of differences in photosynthesis among species. IV. The differential response in dry matter production hetween C3 and C4 species to atmospheric carhon dioxide enrichment. Proceedings of the Crop Science Society of Japan, 42, BROWN, K. W. & ROSENBERG, N. J. (1970). Influence of leaf age, illumination and upper and lower surface differences on stomatal resistance of sugarbeet {Beta vulgaris) leaves. Agronomy Journal, 62, CHANG, H. T. & LOOMIS, W. W. (1945). Effect of carbon dioxide on absorption of water and nutrients hy roots. Plant Physiology, 20, GAASTRA, P. (1963). Climatic control of photosynthesis and respiration. In: Environmental Control of Plant Growth (Ed. hy L. T. Evans), pp Academic Press, London. GATES, D. M. (1965). Energy, plants and ecology. Ecology, 46, GEE, G. W. & FEDERER, A. (1972). Stomatal resistance during senescence of hardwood leaves. Water Resource Research, 8, GiFFORD, R. M. (1979). Growth and yield of CO^ enriched wheat under water-limited conditions. Australian Journal of Plant Physiology, 6, HALL, A. E., SCHUI.ZE, E. D. & LANGE, O. L. (1976). Current perspective of steady-state stomatal response to environment. In: Ecological Studies, vol. 19 (Ed. by O. L. Lange et al.), pp Springer- Verlag, Berlin. HARPER, J, L. (1977). The limiting resources of the environment. In: Population Biology of Plants, pp Academic Press, London. IMAI, K & MURATA, Y. (1976). Effect of carbon dioxide concentration on growth and dry matter production of crop plants. I. Effects on leaf area, dry matter, tillering, dry matter distribution ratio, and transpiration. Proceedings of the Crop Science Society of Japan, 54, IMAI, K. & MURATA, Y. (1978a). Effect of carbon dioxide concentration on growth and dry matter production of crop plants. IV. After-effects of carbon dioxide treatments on the apparent photosynthesis, dark respiration and dry matter production. Japanese Journal of Crop Science, 47, IMAI, K. & MURATA, Y. (1978b). Effect of carbon dioxide concentration on growth and dry matter production of crop plants. V. Analysis of after-effect of carhon dioxide treatment on apparent photosynthesis. Japanese Journal of Crop Science, 47, JARVIS, P. G. (1976). The interpretation of variations in leaf water potential and stomatal conductance found in canopies in the field. Philosophical Transactions of the Royal Society of London, 273 B, JORDAN, W. R., BROWN, K. W. & THOMAS, J. C. (1975). Leaf age as a determinant in stomatal control of water loss from cotton during water stress. Physiologia Plantarum, 56, KANEMASU, E. T. & TANNER, C. B. (1969). Stomatal diffusion resistance of snap beans. 1. Influence of leaf water potential. P/iys!o/og;a P/an<ar«m, 44, ,,. n c MucHow R C ElSHER M. J., LUDLOW, M. M. & MYERS, R. J. K. (1980). Stomatal behaviour of kenaf and sorghum in a semi-arid tropical environment. I. During the night. Australian Journal of Plant Physiology, 7, RosnNBFRG N J {\974). Microclimate: The Biological Environment. John W\ley,Ne^v York. SALISBURY, F. B. & Ross, C. W. (1978). The photosynthesis-transpiration compromise. In: Plant Physiology, pp Wadsworth Publishing Company, California. SANDANAM, S., GEE, G. W. & MAPA, R. W. (1981). Leaf water diffusion resistance in clonal tea {Camellia sinensis L.): effects of water stress, leafage and clones. Annals of Botany, 47, TANAKA, I. (1976). Climatic influence on photosynthesis and respiration in rice. In: Climate and Rice, pp International Rice Research Institute, Los Banos, Philippines. TURNER, N. C. & BEGG, J. E. (1973). Stomatal behaviour and water status of maize, sorghum and tobacco under fleid conditions. I. At high soil water potential. Plant Physiology, 51, TURNER N C &HEICHEL G. H. (1977). Stomatal development and seasonal changes in diffusive resistance of primary and regrowth foliage of red oak {Quercus rubra L.) and red maple {Acer rubrum L.). New Phytologist, 7»,7l-Sl. HiDA, S. (1976). Carbon dioxide and yield of rice. In: Climate and Rice, pp International Rice Research Institute, Los Banos, Philippines.
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