Photosynthesis, productivity and environment

Transcription

1 Journal of Experimental Botany, Vol. 46, Special Issue, pp , September 1995 Journal of Experimental Botany Photosynthesis, productivity and environment David W. Lawlor 1 lacr-rothamsted, Harpenden, Herts AL5 2JQ, UK Received 2 March 1995; Accepted 12 June 1995 Abstract The relation between photosynthetic rate per unit leaf area (Pn), total photosynthesis by canopies and dry matter production {DMP) of crops is reviewed. Although Pn is the driving force for all plant growth, total DMP is determined by processes integrated over the canopy, primarily light interception and thus by leaf area index (LAI) and canopy architecture and leaf area duration [LAD). The processes are not linearly related so that effects on DMP of changes in the efficiency of conversion of energy of radiation to dry matter are smaller than those associated with LAI. Photosynthesis is much less sensitive to changing environmental conditions than development of leaf area. This explains the apparent anomaly that Pn does not determine the variation in productivity of a crop under normal agronomic practice, despite the role of photosynthesis in providing all the assimilates for DMP. Breeding and selection of crops for higher yield has not resulted in improvements in dry matter production. Indeed, potential photosynthetic rate has decreased under selection breeding, compensated by increased leaf area: the causes are considered. Crops growing at or near their potential rate use most of the available solar energy and there is a strong correlation between radiation absorbed and DMP and canopy photosynthesis is not light saturated. To increase production it will be necessary to extend either the growing season or to improve light conversion efficiency; the latter is best achieved by increasing Pn. The limiting factors in photosynthetic metabolism which determine Pn under different environmental conditions, are reviewed. Increased Pn is not likely to come from altering light harvesting, electron transport or ATP and NADPH synthesis which are potentially very flexible and have large capacity: there is large genetic variation. Synthesis of ribulose bisphosphate (RuBP) depends on activity of Calvin cycle enzymes which may be limiting due to environmental factors. Increasing the atmospheric C0 2 supply increases production of C 3 plants under current conditions: this is due to a decrease in the oxygenase function of ribulose bisphosphate carboxylase-oxygenase (Rubisco). Improving the specificity factor of Rubisco is a longterm goal to decrease photorespiration. Even if Pn is increased, evidence from theoretical and crop canopy studies suggest that the increase in biomass production will only be a small proportion of the increase in Pn, and DMP also depends on the crop's sink capacity. Crop production is a function of many processes, at the level of the chloroplast, the leaf and the canopy. To increase Pn and production of crops will require knowledge of processes at all levels in the plant-environment system. Key words: Photosynthesis, dry matter production, leaf area index, environment. Introduction The aims of this review are (1) to examine the relation between photosynthesis, plant productivity and yield and to clarify the roles of photosynthetic rate per unit leaf area (Pn) and total leaf area, in determining dry matter production (DMP): (2) to analyse the limitations to Pn, which it will be necessary to overcome to increase productivity. Examination of these wider aspects is necessary given the possibilities offered by genetic engineering (Gasser and Fraley, 1989) to modify Pn and other crop processes. This review specifically addresses the confusion over the links between Pn and DMP, arising because there is poor correlation between them in many situations (Elmore, 1980; Evans, 1983, 1984, 1993). This conflicts with the logical expectation that Pn, as the factor responsible for all dry matter production, should correlate very strongly with dry matter production and harvestable yield (Hesketh, 1963; Zelitch, 1982). Comparison of plants 1 Fax: Oxford University Press 1995

2 1450 Lawlor with C 4 and C 3 metabolism does indeed show a strong correlation between Pn and DMP: in warm, high radiation environments C 4 plants have greater Pn and accumulate more dry matter than do C 3 plants, although in cool, dim conditions the superiority of the C 4 syndrome may not be apparent (Gifford, 1974; Evans, 1993). Similarly, there is a good, positive correlation for crops grown with different amounts of fertilizer (Zelitch, 1975). Yet, surprisingly, breeding and selection for greater harvested yield in cereals and other crops has not resulted unequivocally in increased Pn or total dry matter production (Evans and Dunstone, 1970; Austin et al., 1980, 1982, 1986; Evans, 1993). Poor correlation between Pn, DMP and yield arises from the involvement of many processes in total production, not least the development of leaf area and yield bearing organs (Bingham, 1969; Evans, 1983). Although the driving force for dry matter production is photosynthesis, agronomic and physiological studies indicate that the variation in production under different conditions and in different seasons is more related to plant development and organ formation than to variation in Pn. The importance of the apparent contradiction is that it highlights the need for careful appraisal of the productive system the crop in a particular environment rather than assuming that one process, for example, photosynthesis or a single step in a complex metabolic sequence, will limit productivity over a wide range of conditions. The factors limiting Pn in different conditions have been analysed from many perspectives (Sharkey, 1985; Woodrow and Berry, 1988; Woodrow, 1994). Photosynthetic processes capture the physical energy of sunlight and convert it to chemical forms which are consumed in the biochemical reactions associated with organ development and growth which are required for resource capture (e.g. nutrient uptake and assimilation) and reproduction (Lawlor, 1993). The limitations to Pn may be environmental deficiency or excess of light, nutrients or water and sub- or supraoptimal temperatures while current atmospheric CO 2 concentration limits C 3 plants. They may also be inherent in the photosynthetic mechanism inadequate capacity or inefficiency of enzymes etc. These limiting environmental and plant factors interact strongly so the optima depend on species, the plant's previous history and conditions (Stitt, 1986; Woodrow and Berry, 1988). To achieve maximum rates of photosynthesis and maximum productivity, i.e. to approach the genetic potential of the individual plant in the context of the community (crop), requires that all the conditions approach the optimum (Rabbinge et al., 1990). If the environmental conditions are close to the optimum, and the efficiency with which they are used approaches the maximum possible for that level of production, then the way forward is to increase the genetic potential by altering the plant's genome (Evans, 1983; Gasser and Fraley, 1989; Connett and Barfoot, 1992). Alterations will be required both to the basic mechanisms of photosynthesis in order to increase Pn for given environmental conditions, and to partitioning in order to increase accumulation of assimilates and harvested yield. Understanding of the limitations to Pn inherent in the mechanism and the regulation imposed by peripheral, but vital, processes such as sink development (Gifford, 1986; Geiger, 1987), is essential if the major goals of agriculturally-related plant sciences are to be achieved. Such goals are: understanding the mechanisms of biomass production, prediction of production under a range of conditions, increasing production by modifying the plant environment with a minimum use of resources so as to avoid pollution, and improvement of both the quality of products and the efficiency of their production (related to specific requirements of agro-industrial application). Altering the plant's genome (Connett and Barfoot, 1992) has a role to play in all of these. Here, only some aspects of the problem of increasing DMP (and, by implication, yield) of crops are considered, specifically related to CO 2 assimilation, its efficiency and which of the underlying mechanisms must be modified to increase Pn. Crop photosynthesis and productivity Capture of solar radiation and use of the energy to drive the biophysical and biochemical processes which ultimately result in the synthesis of all components of plant structure, are the key processes in production of dry matter (Monteith, 1977; Lawlor, 1993). Net total (root plus shoot) DMP from emergence to harvest (time t 0 to H) of a crop is determined, (Monteith, 1977, 1981; Kiniry et al., 1989) by the total photosynthetically active radiation (PAR) intercepted (I { ), and the efficiency with which the energy is converted into dry matter (Pn/I { ), where Pn is the net CO 2 assimilation per unit leaf area. The fraction of photosynthate lost by respiration, root exudates etc. is expressed by F. DMP= (IPn/I)dtF. oj The net rate of photosynthesis is the difference between gross photosynthesis (P s ) and photorespiration (P T ) plus respiration (R d ) from the tricarboxylic cycle or related process in the light ('day respiration') not directly linked to photosynthesis: Radiation interception The value of / i5 (the difference between the incident radiation, I, and the radiation penetrating below the base

3 of the canopy) between emergence and harvest depends on the leaf area of the crop (the leaf area index, LAI) and its duration (LAD, i.e. LAI over time, dt) and on crop structure, s, which is a function of factors such as leaf angle (Legg et al., 1979; Monteith, 1981). The total radiation intercepted over the season is given by: 4>tai= Idt(LAIxs). oj Only a fraction of the radiation intercepted is used in photosynthesis as some is reflected and some absorbed in the tissues. Interception of radiation by crops well supplied with water and nutrients, and protected from pests etc., increases from zero at sowing to almost 100% as LAI exceeds c. 3 or 4, when the canopy covers the ground, and decreases as the crop senesces and LAI falls (Irvine, 1975; Monteith, 1977). The LAI is a function of the number and size of leaves and both, but particularly the latter, are decreased by cool temperatures, water deficits, nutrient deficiency etc. giving smaller LAI and LAD. The rate of canopy development has marked effects on the interception of radiation early in crop growth and thus greatly affects yield in many crops. For example, in cool springs in Britain sugar beet grows slowly so that the rapidly increasing incident radiation is not used and subsequent yield is poor compared to that resulting from warmer springs (Milford et al., 1980). Differences in I { due to LAI, s and leaf spectral characteristics of crops may play a role in differences between species and in variations in productivity with changing conditions. Canopy architecture, particularly leaf angle and morphology, has an effect on the amount of energy intercepted in different layers of the canopy (Legg et al., 1979). Canopy photosynthesis Simulation models suggest that erect and dissected leaves allow greater penetration of radiation into the canopy and also reduce the energy load on the uppermost leaves whilst increasing it for the lower leaves, thus allowing photosynthesis at low light where it is most efficient (in terms of CO 2 assimilated per unit of intercepted radiation). Young leaves have greater Pn in bright light than old leaves, so optimizing the efficiency of light use. Old leaves senesce, reducing the respiratory burden on the crop, and nutrients etc., are remobilized to the growing organs, thus improving the efficiency of nutrient use, but decreasing leaf area (Lawlor et al., 1989). The marked inefficiency of Pn at large photon flux in most C 3 leaves is not seen in canopy photosynthesis, which is generally not saturated even in very bright light (Bugbee and Salisbury, 1988; McCree and Troughton, 1966; Vietor and Musgrave, 1979; Sinclair and Horie, 1989; Mahon, 1990a; Sinclair, 1994). With very large photon flux, Photosynthesis, productivity and environment 1451 particularly under stress conditions, the upper, but not the lower, leaves in the canopy may become photoinhibited without major decrease in canopy photosynthesis (see reviews in Baker and Bowyer, 1994). Some studies with wheat and rice have shown greater production in varieties with erect leaves (Gale and Youssefian, 1985; Le Cain et al., 1989; Fischer and Quail, 1989; Morgan et al., 1990). Also, under very large radiant energy fluxes, some of the advantage of C 4 crops over C 3 crops, is from better radiation penetration to lower leaves (Kanemasu and Hiebsch, 1975). However, the expected advantages of canopy architecture and other traits are not generally large, in part, because too little attention has been paid to diffuse radiation conditions (Goudriaan and van Laar, 1978; Feil, 1992; Evans, 1993). Simulation modelling of photosynthesis in canopies, based on the light response of photosynthesis by individual leaves and the attenuation of PAR in the canopy, shows that the apparent quantum yield is of greater importance to productivity than the maximum rate of photosynthesis (P max ) in environments with relatively low, diffuse radiation. Integrated over time, a 10% increase in apparent quantum yield was calculated to have more effect than an equivalent change in P max. However, in brightly lit canopies, increasing P max would be an advantage (Day and Chalaby, 1988). Theoretical analysis shows that crop radiation use efficiency increased as a function of leaf Pn but reached a plateau well before the maximum rate of Pn was reached, as observed experimentally (Sinclair, 1994). The photosynthetic mechanism and Pn are apparently optimized in canopies, but the importance to production and the mechanisms of optimization are poorly understood (R.A.C. Mitchell, personal communication) and have not been targeted for improvement. Canopy architecture interacts with many other factors so the complexity of the system decreases the supposed advantage of a single factor. Probably the scope for increasing productivity in crops with large LAI and LAD by modifying these characteristics is small, but current agriculture world-wide is substantially limited by inadequate LAI and light interception and, to a smaller extent, by direct effects of stresses on Pn. Total net photosynthesis depends on the integrated activities of all photosynthetically active organs and the response of Pn of individual leaves to radiation. Respiration Respiration is an important factor in crop production. In C 3 crops P r may be 15-45% of P n but it is almost zero in C 4 crops: respiration from 'day' respiration is poorly quantified under field conditions, but may be 70-80% of dark respiration, which itself is perhaps 10-15% of Pn under normal photosynthetic conditions. Thus, Pn depends not only on photosynthesis but on other pro-

4 1452 Lawlor cesses, principally photorespiration (Amthor, 1989, 1994). Respiration during darkness is a factor of great importance for biomass production. In C 3 crops it is about 50% of the carbon assimilated, a large demand and one substantially reducing DMP compared to the total photosynthetic potential of the canopy. If respiration is changed to even a small extent, it may cause large variation in DMP (Amthor, 1989). The rate of dark respiration per unit DM varies according to conditions, particularly temperature, generally increasing linearly with a g io of 2 to 3. Total net productivity and efficiency of radiation use depend on environmental conditions, for photosynthesis and respiration and growth processes are not affected in the same way over the range of conditions, so the balance between them varies (Heichel, 1971). The ratio of respiration to photosynthesis is probably a major factor in production despite adjustment of dark respiration to changes in Pn so that the processes are, in part, optimized (Amthor, 1994). Grain yields of wheat in the UK are generally greater in the (cooler but long-day) north than (warmer, short-day) south, possibly due to reduced respiration relative to photosynthesis (Russel and Wilson, 1994). Respiration has been separated, functionally, into growth and maintenance components. These are related to the synthesis of new tissue and the turnover of existing tissue, respectively. Growth respiration is large (80% of total respiration) in the phase of vegetative growth, decreasing during reproductive growth (e.g. grain filling, 20%) with maintenance respiration changing reciprocally. Growth respiration is relatively independent of the environment and, as it is a small component of respiration in mature canopies, is not regarded as a major target for modification. Reduction in maintenance respiration is the process which has probably been modified in cases where selection for low respiration rates has increased productivity (Amthor, 1989). Although respiration consumes assimilates it should not be considered wasteful for it is essential to production, providing the energy and substrates for growth and maintenance of the existing plant structures. However, decreased rates of respiration per unit of plant dry matter can be selected for and do contribute to increased productivity (Wilson, 1975; Eagles and Wilson, 1982; Medrano et al, 1995). Production and radiation use efficiency There is very strong correlation between canopy dry matter production, crop growth rate (CGR) and I { over a very wide range of / for C 3 and C 4 crops in many different environments (Monteith, 1977; Christy and Porter, 1982; Kiniry et al., 1989; Evans, 1993), including very large photon fluxes (Bugbee and Salisbury, 1988). Efficiency of energy conversion is generally greater in C 4 than C 3 plants, but similar within each group, although the superior performance depends on the environment (Evans, 1993). For C 3 plants the maximum efficiency is about 3 g of dry matter per megajoule (DM MJ" 1 ) of PAR intercepted or an efficiency of c. 5%. C 4 plants achieve efficiencies of 4-5 g MJ 1 PAR. This implies that in many environments with different temperatures and incident radiation, but with water, nutrients etc., approaching optimal, the physiological and metabolic processes determining dry matter production are very similar for a wide range of C 3 crops and that their metabolism is less efficient than C 4 crops. Efficiency depends on the products being made, for example, it may decrease during formation of yield (particularly of oil or protein yielding crops), when energy demand for biochemical syntheses increases. Correlation between radiation interception and harvested yield, for example, of grain in cereals, is generally poorer than that with dry matter (Kiniry et ah, 1989; Evans, 1993). The explanation is in the many, variable processes contributing to the formation of storage and particularly reproductive organs (Bingham, 1969), their greater sensitivity to conditions during particular stages of growth (e.g. pollen formation and flowering) compared to vegetative organs and to the varying source of assimilates, for example, current photosynthesis or stored (Bonnett and Incoll, 1992). The more steps occurring between photosynthesis and the end products, the poorer the coupling and the weaker the correlation. The relative importance of LAI, light interception and photosynthesis in DMP in crops is illustrated by the response of winter wheat (Triticum aestivum L. cv. Avalon) as a function of nitrogen and water supply in a field experiment at IACR-Rothamsted. Briefly, wheat was grown in replicated small plots with standard non-limiting applications of phosphorus and potassium. Three different amounts of N were applied to achieve a very wide range of crop production and yield; (1) no N, the crop growing on soil containing about 40 kg Nha" 1 ; (2) 75 kg ha" 1 N as nitrate; (3) 300 kg ha" 1 N as nitrate. Ten per cent of the fertilizer was applied in autumn, and the remainder in two equal proportions in March and in April. Each N treatment was combined with either full irrigation to minimize soil water deficits or a continuously developing drought after emergence to harvest. Plots were protected from rain by a mobile rain shelter. Rates of photosynthesis were measured on the flag leaves shortly after attaining maximum size. Leaf area and dry matter of the crops was measured regularly and straw and grain dry matter at maturity, together with components of yield. Throughout crop growth, PAR incident on and below the canopy was measured by tube solarimeters; intercepted energy and radiation conversion efficiency (net total DMP per unit /j over the crop's life) were calculated. Nitrogen and water deficiency decreased the maximum LAI and LAD (Fig. la), and radiation interception (Fig. lb). The decrease in DMP is related to total inter-

5 B 5 x Irrigated Draughted 300N,. / '. kgn 75N April May June July Aug Fig. 1. Effects of different amounts of nitrogen fertilizer and of irrigation on winter wheat grown in the field with three N fertilizer applications, 0, 75 and 300 kg ha" 1 at Rothamsted. (A) Development of leaf area index during the growing season and (B) the interception of total PAR radiation (total, solid line): interception for the droughted crops is omitted for clarity. cepted PAR in Fig. 2 and Table 1: both N deficiency and drought decreased radiation interception and conversion efficiency. The effects on grain yield were similar to those on total dry matter so harvest index was unaffected. The changes in yield were largely caused by variation in grain number not individual grain mass. Comparison of the 24H C.16 I 8 (0 S irrigated 0 kg N drought drought irrigated 300 kg N irrigated 75 kg N drought Total photosynthetically active radiation absorbed (MJ m~ 2 ) Fig. 2. Total above-ground dry matter as a function of the total PAR intercepted by the crops during their growing season. The irrigated crop with 300 kg N provides a measure of total potential production (solid line). Deficient N decreases DMP at a particular radiation absorption and drought decreases it yet further. Photosynthesis, productivity and environment 1453 relative reductions in the components of productivity as a function of N supply (Fig. 3) shows the progressively greater decreases in P max of young, mature flag leaves, conversion efficiency, light interception, dry matter production, and LAI as N supply decreased. The DMP was, therefore, not only a function of radiation intercepted, but of plant metabolism. The effect of the N deficiency (and water deficit data not given) was to decrease the maximum Pn (Fig. 4). The smaller LAI is caused by decreased tillering, fewer, smaller leaves and increased senescence (Pearman et al, 1979); nitrogen and waterstressed crops mature earlier thus decreasing the duration of photosynthesis. The decrease in radiation use efficiency with deficient nitrogen and water supply is a consequence of less efficient metabolism, particularly decreased net photosynthesis: respiration per unit of dry matter was not affected by the treatments (Mitchell et al., 1991). The decrease in Pn in response to nitrogen deficiency (Fig. 4) results from decreased content of photosynthetic (and other) components per unit leaf area, as is well established. There is less chlorophyll and Rubisco, reducing, respectively, energy capture by thylakoids and carboxylation capacity (Evans, 1986; Makino et al, 1988; Lawlor et al, 1989). The change in radiation use efficiency is relatively small, suggesting that photosynthetic and respiratory metabolism are affected much less than organ number and size. Thus, variation in dry matter production in wheat is due primarily to variation in leaf area production (Feil, 1992) and Pn and other metabolic processes are conserved: whilst they are not invariant they change much less than organ growth. Analysis of the complete production system shows the limitations more clearly than an analysis of separate processes. For existing crops under good husbandry, radiation is almost fully used. Decreased production due to nutrient and water deficiencies is primarily due to poor development of leaf area decreasing light interception. Reduced photosynthesis and light conversion efficiency have smaller effects on production. World-wide, growth conditions are inadequate for exploitation of available radiation to achieve existing genetic potential. However, when environmental conditions are not limiting, further increase in production will require greater rates of canopy photosynthesis or reduced respiration or longer duration of crop and photosynthesis. Characteristics of the crop and the biochemical and physiological mechanisms of the plant must be altered to increase the genetic potential for production and yield. Photosynthetic rate and productivity Correlation between the rate of photosynthesis and productivity has been analysed in several reviews (Evans, 1993, 1994; Sinclair, 1994), coming to the general conclu-

6 1454 Lawlor Table 1. Production of dry matter and grain by winter wheat (cv. Avalon) with nitrogen and irrigation treatments Nitrogen (kg ha" 1 ) Grain (gm" 2 ) Total dry matter LAI Total PAR (MJirT 2 season" 1 ) Conversion efficiency (gmj" 1 ) Irrigated Dry <0 V 0) CA S.E * CM tt^ S E Leaf N (g m 2 ) Fig. 3. Maximum rates of photosynthesis of wheat leaves as a function of leaf nitrogen content for the crops grown with 0 (open circles) and 300 (solid circles) kg ha" 1 applied N, as described in Fig. 1.,, photosynthetic rate conversion efficiency PAR interception dry matter production LAI max Applied N (kg ha~ 1 ) Fig. 4. Relative effects of the amount of N fertilizer applied on processes in the wheat crop: photosynthetic rate measured at saturating light and 350 /urnol mol" 1 CO 2 on young, fully mature flag leaves was much less affected by N deficiency than conversion efficiency, PAR interception, dry matter production or leaf area index at its maximum (LAI max). sion that the correlation is, at best, weak (Bunce, 1989) and usually negative for crops in the field (Evans, 1993; Sinclair, 1994). However, there is considerable conflict in the results for different crops. Measurement of Pn was expected to provide a direct measure of plant production (Elmore, 1980; Zelitch, 1982; Evans, 1993), based on the argument (Cannell et al, 1969; Zelitch, 1975) that photosynthesis underpins the whole complex mechanism ultimately leading to dry matter production, so knowledge of Pn should allow prediction of productivity (Natr, 1966; Nelson et al, 1975; Peterson and Zelitch, 1982). A corollary was that DMP could be increased by selection of genotypes for large Pn or by altering the photosynthetic mechanisms (Austin, 1989). Also, there is substantial inherent quantitative variability in photosynthesis (Natr, 1966; Cannell et al, 1969; Byrne et al, 1981; Johnson et al, 1987; Austin, 1989). Some studies do show good correlation between Pn and productivity, for example, in grain sorghum (Peng et al, 1991); increased Pn was found in maize following cycles of selection for the trait (Crosbie and Pearce, 1982) and there is heritability for canopy photosynthesis and seed yield in soybean (Harrison et al, 1981). However, total biomass has not increased with recent selection of wheat for high yield: comparison of old and new wheat varieties on Broadbalk field at Rothamsted shows the old to have slightly greater DMP (Austin et al, 1993) as reported earlier (Austin et al, 1980). In contrast, Waddington et al. (1987) observed a 30% increase in biomass of durum wheats over 25 years. The failure to select for larger Pn, despite increased wheat yield, has been apparent. Indeed, there is frequently a negative correlation between photosynthetic rate and size of the leaf in wheat (Evans and Dunstone, 1970; Dunstone et al, 1973; Austin et al, 1982, 1986) and rice (Cook and Evans, 1983) when wild progenitors, old cultivars and high yielding modern varieties are compared (Khan and Tsunoda, 1970). Zelitch (1982) identified the apparent 'paradox' that increasing the rate of photosynthesis (e.g. by fertilizer application) does increase biomass and, generally, yield of most crops but genetic selection does not. As Evans (1993) says '... the very crux of the paradox, [is] that yield is favoured by environmental improvement of [photosynthetic rate per unit area] but not, so far, (Evans' italics) by genetic improvement of the individual leaf rates'. This suggests that selection during breeding, for yield presumably, has decreased the components responsible for photosynthesis ('dilution hypothesis', see Evans, 1993). However, there is evidence for selection increasing Pn (but decreasing electron transport) with date of culti-

7 var introduction of Australian wheats, probably related to the introduction of dwarfing genes (Watanabe et al., 1994). The tendency to increase leaf area and to decrease the photosynthetic components (Dunstone and Evans, 1974) is related to increasing ploidy and increasing cell size, which affect the leaf anatomy and gas exchange (Dornhoff and Shibles, 1976; Le Cain et al., 1989; Byrne et al., 1981). The result of selecting larger leaves has been to increase the light interception (Gent and Kiyomoto, 1985; Mahon, 19906) and perhaps reduce weed competition. Large biomass production was desirable as straw is valuable in many rural economies for animal feed etc. (but not in industrialized agriculture). Similarly, increasing N supply, for example, increases leaf area by increasing cell size and number, but generally stimulates production of components of the photosynthetic system and photosynthetic rate (Lawlor et al., 1989). Not only has selection not resulted in greater Pn, neither has more specific selection aimed at apparently wasteful processes. Attempts to select individuals with small rates of photorespiration within populations of C 3 plants (Zelitch, 1975; Zelitch and Day, 1973; Evans, 1983) have generally not had the desired effect, with the ratio of photorespiration to photosynthesis remaining stubbornly constant, although the selection methods employed appear to have selected for reduced rates of dark respiration (Medrano et al., 1995). The assumption that altering photorespiration of C 3 crops will confer long-term advantages, particularly in changing or stressful environments, such as under water stress where photorespiration may have a protective role (Lawlor, 1979) against photoinhibition (Baker and Bowyer, 1994) has been questioned by Evans (1993). Why is it that selection for high productivity (possibly) and yield (certainly) has not increased photosynthetic rate? Explanation of why breeding selection should have resulted in the converse relation of Pn to other characteristics have not been given. Perhaps the genetic changes required for greater numbers of cells or, more likely, for larger cells (related to wall growth perhaps) are relatively more easily achieved than those related to increasing the number of genes for photosynthetic components or to increasing the copies. Advances in plant genetic engineering open the prospect of modifying photosynthesis and decreasing photorespiration (Bainbridge et al., 1995) although there is still uncertainty about the potential to modify complex multigenic traits expressed in 'systems* such as photosynthesis. Evans (1993) suggests the need for better evaluation of how changes at the cellular level of organization are transferred directly through to the crop. Often the effects are attenuated (Gifford, 1974). To this end it is legitimate to ask is there a 'proper view' of the events in plant production to direct genetic engineering towards effective targets within photosynthesis and the use of assimilates? With respect to photosynthesis the questions are: Photosynthesis, productivity and environment What parts of the photosynthetic mechanism must be altered to improve the rate of CO 2 assimilation: NO3" metabolism is ignored here although very important (Foyer et al., 1995)? 2. What must be done to increase the ability of the mechanisms to function efficiently over a wide range of environmental conditions and to avoid damage? 3. How do the various sub-processes link to achieve the productivity obtained in particular environments? 4. Can alterations in biochemistry, which increase photosynthesis under laboratory conditions, increase production in the field? Factors limiting photosynthetic rate Photosynthetic rate is determined by the interaction of several processes and systems (Lawlor, 1993): (1) light harvesting, electron transport and NADPH and ATP synthesis associated with the thylakoid membranes, (2) the capacity of the enzymes of the photosynthetic carbon reduction (Calvin) cycle in the chloroplast stroma for ribulose bisphosphate (RuBP) regeneration and of ribulose bisphosphate carboxylase-oxygenase (Rubisco) for CO 2 assimilation, (3) consumption of the assimilates to avoid feedback inhibition of photosynthesis by its products or shortage of inorganic phosphate in the stroma. Light capture, electron transport and ATP and NADPH synthesis There are substantial differences in the ability of different species to capture solar radiation and use the energy for electron transport and NADPH and ATP synthesis. Similarly, there are great differences between species in their ability to adapt to the light environment during growth. Many are very adaptable in their capacity to capture photons, to transport electrons and to form the ph gradient across the thylakoids for ATP synthesis. Others, however, are obligate (genetically adapted) sun or shade plants. Obligate shade plants are unable to increase their performance effectively in bright light. Obligate sun plants are similarly unable to adjust to dim light (Evans et al., 1988). Some C 3 plants achieve large maximum rates of CO 2 assimilation in bright light, comparable to C 4 plants which are virtually never saturated even at the highest terrestrial photon fluxes, yet their photosystems, electron transport and photophosphorylation and NADP + reduction mechanisms appear not to differ fundamentally in components, but do in system organization, from those of plants less effective at large rates of assimilation. Generally, plants are able to intercept radiation and convert energy into ATP and NADPH very efficiently (Stitt, 1986), this is so in crops at high irradiance even if the processes in individual leaves are saturated. Indeed,

8 1456 Lawlor for many environments and crops, light availability limits photosynthesis over much of the growing period. Energy transduction in the photosystem reaction centres is efficient and similar in different plants. The quantum yields of C 3 plants approach the theoretical limit of efficiency given by the mechanism requiring 8 quanta per oxygen evolved and the apparent quantum yields (slope of the response of Pn to incident PAR) of a range of species, even for obligate sun and shade plants (see papers in Evans et al., 1988) are similar and determined by the characteristics of Rubisco. Therefore, the possibilities of improving the basic processes energy capture and transfer in the chlorophyll T protein complexes and reaction centres are limited (Ehleringer and Pearcy, 1983). Only by radical change to the mechanism could major advances be made: how it could be done is unclear. Increasing the efficiency of energy captured, for example, in the green wavelengths or extending capture towards unexploited parts of the spectrum are probably not options given the current understanding of the mechanisms. As PAR incident on the crop may be insufficient to saturate photosynthesis for much of the growing season, energy must be used more effectively for assimilation of CO 2, NO 3 ~ etc. Calvin cycle limitations Limitations in the cycle may be analysed in terms of the synthesis of ATP (by chloroplast coupling factor, CF1-0), NADPH and RuBP and their relation to Rubisco activity and to whole leaf photosynthesis (von Caemmerer and Farquhar, 1981; Farquhar and von Caemmerer, 1982). Low light limits ATP, NADPH and RuBP synthesis and therefore Pn: electron and proton transport are simply insufficient. As illumination increases, so does synthesis of ATP, etc. until, in the normal atmosphere, the (low) concentration of CO 2 then limits Pn. However, with increasing CO 2 Pn rises and eventually saturates. At this point it is probable that Rubisco is the limiting factor. It is, however, unclear if ATP also becomes limiting or Rubisco and CF1-0 'co-limit' (Sharkey, 1985; Woodrow, 1994): it is unlikely that NADPH would limit as plants adapted to large irradiance have a large capacity for electron transport. However, complex feedback regulation of enzymes serves to maintain relatively stable metabolism. Photosynthesis and DMP of C 3 plants, grown as crops, increases when atmospheric CO 2 is raised. Winter wheat, grown with ample nutrition and water in 700 jixmol mol ~ x CO 2 compared to 355 ^mol mol" 1 under simulated field conditions at Rothamsted, has 15-40% greater biomass and 18-23% greater grain yield in different experiments (Lawlor et al., 1993; Mitchell et al, 1993), similar to the response in many studies (Cure and Acock, 1986). Note that this is when interception of radiation by the crop canopy is maximal, showing that yield potential at that radiation is not achieved with the current atmospheric CO 2. As the response of C 4 crops to elevated CO 2 is very much smaller or negligeable (Cure and Acock, 1986) this shows the need for improvement of photosynthetic potential in C 3 crops to exploit the current CO 2 concentration and radiation fully. Plants exposed to elevated CO 2 have, initially, very substantially increased Pn, but there is good evidence that the high rates are often not maintained over long periods, even with ample nutrients, water etc. Photosynthetic rates and capacity often decrease substantially with time (Cure and Acock, 1986; Yelle et al., 1989; Lawlor and Keys, 1993), due to accumulation of carbohydrates related to limited sink capacity (Rowland- Bamford et al., 1990). However, the effects are variable: Delgado et al. (1994) found no evidence of acclimation in winter wheat grown with elevated CO 2 in one experiment, but in another (Delgado et al., unpublished) there was progressive 'down-regulation' and acclimation in the same cultivar. Possibly such differences are related to differences in assimilate storage and sink development. The effect of elevated CO 2 is to increase Pn and to decrease photorespiration, so clearly there would be benefits to DMP and yield of wheat and other C 3 crops if this could be achieved by altering the photosynthetic characteristics rather than by attempting to alter the environment (although anthropogenic CO 2 release to the atmosphere may achieve the same ends!). The response of Pn to CO 2 supply at less than saturating radiation is analogous to the light response: at limiting CO 2, ATP, NADPH and RuBP synthesis are in excess and Rubisco capacity as well. As CO 2 increases so eventually RuBP becomes limiting, but Rubisco may not limit. However, further increase in radiation increases RuBP synthesis so that increasing the CO 2 results in saturation of Pn, again with Rubisco the likely limiting factor (Woodrow, 1994). Although Rubisco has been identified as the enzyme limiting Pn in C 3 plants, other enzymes in the Calvin cycle may also, under some conditions be expected to be limiting, namely phosphoribulosekinase (PRK; Gray et al., 1995) and sedoheptulose bisphosphatase and fructose bisphosphatase (Sharkey, 1989). In the current atmosphere, the CO 2 concentration is too small to achieve saturation of Rubisco and oxygen competes for the reaction sites. Indeed, there is evidence that the CO 2 concentration at the reaction sites of Rubisco in the chloroplast is substantially below that in the intercellular spaces (Evans et al., 1994). Increasing atmospheric CO 2 increases the intercellular CO 2 concentration and CO 2 /O 2 ratio at the reaction sites of the Rubisco, thus decreasing oxygenation and hence photorespiration (Andrews et al., 1995; Bainbridge et al., 1995). Under warm conditions in bright light Pn may be increased substantially (20-50%) by increasing the atmospheric CO 2 concentration from 350 to 700 ^mol mol" 1 (Cure and Acock, 1986). Also, in

9 dim light the quantum efficiency is increased by elevated CO 2, so that there is a positive response to increasing CO 2 concentration under most conditions, particularly very warm. Factors such as nutrient deficiency which decrease growth and assimilate consumption reduce or prevent the response. In the current atmosphere C 3 photosynthesis is not saturated with CO 2 so production increases with elevated CO 2 (Lawlor and Keys, 1993). This is due to the oxygenase function of Rubisco: elimination of this has long been a goal of biochemists (Zelitch and Day, 1973) and is feasible based on the evidence. There has been improvement in the specificity factor (Bainbridge et al, 1995) during evolution of Rubisco and this parameter varies in higher plant Rubiscos suggesting that there is potential for further improvement of the enzyme. Selection for decreased photorespiration may increase Pn by 20-50%, productivity by 15-30% and yield by about the same depending on species, conditions etc. However, this assessment is based on physiological information (elevated CO 2 studies). The failure to select low photorespiration plants means that a direct test of the consequences of eliminating the oxygenase function of Rubisco has not been possible. If Rubisco can be modified, why then was the route taken by C 4 plants not to improve the Rubisco specificity factor, but to modify leaf anatomy and also metabolism by using phosphoenolpyruvate carboxylase as a CO 2 'pump'? Organic acids are transported from the mesophyll to the bundle sheath and decarboxylated, providing CO 2 to Rubisco. Also, O 2 generation in the bundle sheath is much decreased, so the CO 2 /O 2 ratio under which Rubisco operates in C 4 plants is greater than in C 3 plants, decreasing photorespiration (Dever et al, 1995). Perhaps surprisingly, Rubisco in C 4 plants is less efficient than in many C 3 plants (lower specificity factor) yet net photosynthesis is greater due to the CO 2 'pump'. This suggests that, even if Rubisco can be modified, the time-scale is long, so that it has proved easier in evolutionary terms to adapt multi-gene processes ancillary to Rubisco, involving more complex and larger carbon fluxes between cells of different types. If genetic alteration of Rubisco requires many, co-ordinated steps then this may be very difficult via mutation in vivo whilst maintaining a viable photosynthetic system, but genetic engineering may be able to achieve the changes in vitro and then incorporate the changes into the plant (Andrews et al, 1995). The enzyme capacity of the Calvin cycle appears adequate to match the energy available under the illumination experienced during growth, but may be inadequate in bright light, as shown by studies with reduced Rubisco and PRK activity produced by antisense gene techniques (Stitt, 1986; Paul et al, 1995). The apparent excess activity of Rubisco (Krapp et al, 1994) and phosphoribulokinase (Paul et al., 1995) in leaves grown in relatively dim light is required for maximum photosyn- Photosynthesis, productivity and environment 1457 thesis when leaves are placed in bright light. Increasing the amount of Rubisco above the current concentrations in leaves of many plants would seem not to be the best way to improve Pn and productivity. Large nitrogen supply greatly increases concentrations of Rubisco, but does not improve CO 2 assimilation in normal environmental conditions, but does under bright light and elevated CO 2 (Lawlor et al, 1989; Krapp et al, 1994). Little attention has been directed to whether over-expression of the limiting enzymes results in greater Pn. If, for example, over-expression of Rubisco resulted in increased Pn then clearly other photosynthetic processes would not be limiting (as indeed is shown by the increase in Pn with elevated CO 2 ). If no stimulation resulted from over-expression then increasing other components (e.g. CF1 or PRK if possible) would show if they limit Pn. With current knowledge the real improvement in Pn of C 3 plants is expected to come from avoiding the intrinsic inefficiency of Rubisco. The adverse effects of low atmospheric concentration of CO 2 (despite its rapid rise over the last century) and the limitations of CO 2 (Evans et al, 1994) and metabolite diffusion to Rubisco in the stroma (Lawlor et al, 1989) would be avoided or substantially decreased if the oxygenase activity of Rubisco could be eliminated. Less Rubisco would be needed, decreasing the requirement for nitrogen used in its synthesis. However, if an improved Rubisco were achieved it might become necessary to alter Calvin cycle regulation to improve the synthesis of RuBP. Nitrogen assimilation Photosynthetic N assimilation by the reduction of nitrate ions and synthesis of amino acids is well understood (Lawlor, 1993), but the links to C assimilation are less so, particularly the partitioning of energy in the chloroplast and regulation of the combined processes of C and N metabolism. A consequence of increasing Pn by elevated CO 2 is to decrease the N content of tissues, both vegetative and reproductive (e.g. cereal grain). This arises from accumulation of carbohydrates, mainly soluble sugars, fructans and starch without increased accumulation of N-containing components, nitrate ions, amino acids and, particularly, proteins. However, as total DMP increases with increased Pn so total N uptake may be the same or increases. To overcome the decrease in N content will require accumulation (increased synthesis of) N-containing components of the system and in the same proportions to avoid alterations to the machinery. This may also be necessary in future if Rubisco characteristics are improved and other limitations (e.g. Calvin cycle enzyme activity) become important. Mechanisms for and consequences of making such alterations have yet to be evaluated but it is likely that control resides in protein synthesis rather than nitrate reduction.

10 1458 Lawlor End product regulation of photosynthesis and sink limitation If the capacity of the sinks for assimilates (Bonnett and Incoll, 1992) is too small then accumulation of carbohydrates in source tissue frequently reduces Pn by feedback processes (Blechschmidt-Schneider et al., 1989; see Evans, 1993, for a compilation of many experiments). Translocation of assimilates does not limit assimilate movement and accumulation in sink organs except in extreme conditions (Gifford, 1986; Wardlaw, 1990). The physical size of the phloem and the rates of assimilate transport increase in proportion to the photosynthetic potential and the sink: rather it is the capacity of the sinks which is important (Wardlaw, 1990). The advantages accruing in crops as a consequence of selection breeding relate more to the utilization of assimilates, altering the sink distribution, including increasing harvest index which has so influenced yield (Austin et al., 1980) and changing the time over which the crop grows, rather than increasing photosynthesis (see Evans, 1993, for discussion and literature). Increasing the capacity to utilize assimilates should ensure that inhibition of the photosynthetic system, especially decreased rates of enzyme activity ('downregulation') and possibly inhibition of the synthesis of and thereby decreased content of photosynthetic components ('acclimation'; Lawlor and Keys, 1993) do not occur and, therefore, allow the maximum photosynthesis possible for the light and CO 2 available. The occurrence of acclimation is demonstrated regularly in some species, for example, tomato (Yelle et al., 1989) but in others, for example, winter wheat, it may not occur in some experiments (Delgado et al., 1994), but do so in others which are very similar (Delgado et al., unpublished). Suggested mechanisms of feedback reduction of activity are inadequate rates of recycling of inorganic phosphate due to end-product accumulation and slower Calvin cycle turnover and direct allosteric control of metabolites on enzymes (Sharkey, 1985, 1989). Acclimation is related to the inhibition by carbohydrates of gene transcription and translation of RNA into protein (Sheen, 1994). By ensuring that sink demand for photosynthetic products is maintained over a wide range of conditions, limitations to photosynthesis should be minimized (Humphries and Thorne, 1964; Geiger, 1987); for example, reduced temperatures of growing organs may decrease Pn, in the long term, by preventing the consumption of carbohydrates (Paul et ah, 1991). Plants grown under elevated CO 2 may show down-regulation and acclimation because, presumably, the storage pools can not accommodate the excessive carbohydrate production, allowing metabolism to be affected. By increasing the capacity of the sinks and by extending the periods over which those sinks fill, total photosynthesis might well be increased and total biomass and yield production improved. As sink size (e.g. the tillering capacity and stem length of cereals) seem to be under the control of relatively few genes (Gale and Youssefian, 1985) then increasing sink capacity under adverse conditions might, in the long run, be more feasible to maintain photosynthesis and increase productivity, than genetically altering the photosynthetic system. Alteration of sink capacity by genetic engineering appears feasible. Recently, increasing the expression of the enzyme sucrose phosphate synthase (SPS) from maize in all tissues of tomato under the control of the 35S promoter from cauliflower mosaic virus, was shown (Foyer et al., 1995) to increase the flux of carbon to sucrose rather than starch and increased biomass production substantially. This was achieved with only a 10% increase in Pn above the untransformed plant. Clearly, these changes increased the use of assimilates and suggests that altered sink behaviour is of great importance for maximizing Pn and productivity. Conclusions 1. Photosynthesis is the ultimate determinant of dry matter production, but Pn is only one aspect and the LAI and LAD are important aspects of crop production. 2. Losses of assimilate by dark respiration and the ratio of respiration to photosynthesis are important determinants of production. 3. The main limitation to Pn in C 3 plants is the oxygenase function of Rubisco; overcoming that and reducing or eliminating P r or increasing the affinity of the enzyme for CO 2 are long-term goals to increasing productivity. 4. Increasing Pn and productivity in low light would require increasing the apparent quantum yield rather than the maximum Pn: decreasing photorespiration would be advantageous in these conditions. 5. If Pn is increased by overcoming the Rubisco limitation, or by elevated CO 2 then full expression of dry matter production will require development of sinks for assimilate to be optimized to particular environmental conditions. Acknowledgement IACR receives grant-aided support from the Biotechnology and Biological Sciences Research Council of the UK. References Amthor JS Respiration and crop productivity. Berlin: Springer-Verlag. Amthor JS Respiration and carbon assimilate use. In: Boote KJ, Bennett JM, Sinclair JR, Paulsen GM, eds Physiology and determination of crop yield. Madison, Wisconsin: American Society of Agronomy, Inc.,

11 Andrews TJ, Hudson GS, Mate CJ, von Caemmerer S, Evans JR, Arvidsson YBC Rubisco: the consequences of altering its expression and activation in transgenic plants. Journal of Experimental Botany 46, Austin RB Genetic variation in photosynthesis. Journal of Agricultural Science (Cambridge) 112, Austin RB, Bingham J, Blackwell RD, Evans LT, Ford MA, Morgan CL, Taylor M Genetic improvements in winter wheat yields since 1900 and associated physiological changes. Journal of Agricultural Science (Cambridge) 94, Austin RB, Ford MA, Morgan CL, Yeoman D Old and modern wheat cultivars compared on the Broadbalk wheat experiment. European Journal of Agronomy 2, Austin RB, Morgan CL, Ford MA Flag leaf photosynthesis of Triticum aestivum and related diploid and tetraploid species. Annals of Botany 49, Austin RB, Morgan CL, Ford MA Dry matter yields and photosynthesis rates of diploid and hexaploid Triticum species. Annals of Botany 57, Bainbridge G, Madgwick P, Parmar S, Mitchell R, Paul M, Pitts J, Keys AJ, Parry MAJ Engineering Rubisco to change its catalytic properties. Journal of Experimental Botany 46, Baker NR, Bowyer J (eds) Photoinhibition of photosynthesis. Oxford: BIOS Scientific Publishers. Bingham, J The physiological determinants of grain yield in cereals. Agricultural Progress 44, Blechschmidt-Schneider S, Ferrar P, Osmond CB Control of photosynthesis by the carbohydrate level in leaves of the C 4 plant Amaranthus edulis L. Planta 111, Bonnett GD, Incoll LD The potential pre-anthesis and post-anthesis contributions of stem internodes to grain yield in crops of winter barley. Annals of Botany 69, Bugbee BG, Salisbury FB Exploring the limits of crop productivity. I. Photosynthetic efficiency of wheat in high irradiance environments. Plant Physiology 88, Bunce JA Growth rate, photosynthesis and respiration in relation to leaf area index. Annals of Botany 63, Byrne MC, Nelson CJ, Randall DD Ploidy effects on anatomy and gas exchange of tall fescue leaves. Plant Physiology 68, Cannell RQ, Brun WA, Moss DN A search for high net photosynthetic rate among soybean genotypes. Crop Science 9, Christy AL, Porter CA Canopy photosynthesis and yield in soybean. In: Govindjee, ed. Photosynthesis, development, carbon metabolism and plant productivity. New York: Academic Press, Connett Raj, Barfoot PD The development of genetically modified varieties of agricultural crops by the seed industry. In: Gatehouse AMR, Hilder VA, Boulter D, eds. Plant genetic manipulation for crop protection. Biotechnology in Agriculture No. 7. CAB International, Cook MG, Evans LT The roles of sink size and location in the partitioning of assimilates in wheat ears. Australian Journal of Plant Physiology 10, Crosbie TM, Pearce RB Effects of recurrent phenotypic selection for high and low photosynthesis on agronomic traits in two maize populations. Crop Science 22, Cure JD, Acock B Crop responses to carbon dioxide doubling: a literature survey. Agriculture and Forest Meteorology 38, Day W, Chalaby Z Use of models to investigate the link between modification of photosynthetic characteristics and improved crop yields. Plant Physiology and Biochemistry 26, Photosynthesis, productivity and environment 1459 Delgado E, Mitchell RAC, Parry MAJ, Driscoll SP, Mitchell VJ, Lawlor DW Interacting effects of CO 2 concentration, temperature and nitrogen supply on the photosynthesis and composition of winter wheat leaves. Plant, Cell and Environment 17, Dever LV, Blackwell RD, Fullwood NJ, Lacuesta M, Leegood RC, Onek LA, Pearson M, Lea PJ The isolation and characterization of mutants of the C 4 photosynthetic pathway. Journal of Experimental Botany 46, Dornhoff GM, Shibles R Leaf morphology and anatomy in relation to CO 2 exchange rate of soybean leaves. Crop Science 16, Dunstone RL, Evans LT Role of changes in cell size in the evolution of wheat. Australian Journal of Plant Physiology 1, Dunstone RL, Gifford RM, Evans LT Photosynthetic characteristics of modern and primitive wheat species in relation to ontogeny and adaptation to light. Australian Journal of Biological Science 26, Eagles CF, Wilson D Photosynthetic efficiency and plant productivity. In: Rechcigl M, ed. Handbook of agricultural productivity, Vol. 1. Boca Raton, Florida: CRC Press, Ehleringer J, Pearcy RW Variation in quantum yield for CO 2 uptake among C 3 and C 4 plants. Plant Physiology 73, Elmore CD The paradox of no correlation between leaf photosynthesis rates and crop yields. In: Hesketh JD, Jones JW, eds. Predicting photosynthesis for ecosystem models, Vol. 2. Boca Raton, Florida: CRC Press, Evans LT Raising the yield potential: by selection or design? In: Kosuge T, Meredith CP, Hollaender A, eds. Genetic engineering of plants. New York: Plenum Press, Evans LT Physiological aspects of varietal improvement. In: Gustafson JP, ed. Genetic manipulation in plant improvement. New York: Plenum Press, Evans LT Crop evolution, adaptation and yield. Cambridge University Press. Evans LT Crop physiology: prospects for the retrospective science. In: Boote KJ, Bennett JM, Sinclair TR, Paulsen GM, eds. Physiology and determination of crop yield. Madison, Wisconsin: American Society of Agronomy, Inc., Evans LT, Dunstone RL Some physiological aspects of evolution in wheat. Australian Journal of Biological Sciences 23, Evans JR The relationship between CO 2 -limited photosynthetic rate and ribulose-l,5-bisphosphate carboxylase content in two nuclear-cytoplasm substitution lines of wheat, and the co-ordination of ribulose-bisphosphate-carboxylation and electron-transport capacities. Planta 167, Evans JR, von Caemmerer S, Adams, WW Ecology of photosynthesis in sun and shade. Australian Journal of Plant Physiology 15, Evans JR, von Caemmerer S, Setchell BA, Hudson GS The relation between CO 2 conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Australian Journal of Plant Physiology 21, Farquhar GD, von Caemmerer S Modelling of photosynthetic response to environmental conditions. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Encyclopedia of plant physiology, New series, Vol. 12B. Berlin: Springer, Feil B Breeding progress in small grain cereals a comparison of old and modern cultivars. Plant Breeding 108, Fischer RA, Quail KJ The effect of major dwarfing genes on yield potential in spring wheats. Euphytica 46, 51-6.

12 1460 Lawlor Foyer CH, Valadier MH, Ferrario S Co-regulation of nitrogen and carbon assimilation in leaves. In: Smirnoff N, ed. Environment and plant metabolism. Oxford: BIOS Scientific Publishers, Gale MD, Youssefian S Dwarfing genes in wheat. In: Russell GE, ed. Progress in plant breeding, Vol. 1. London: Butterworths, Gasser CS, Fraley R Genetically engineering plants for crop improvement. Science 244, Geiger DR Understanding interactions of source and sink regions of plants. Plant Physiology and Biochemistry 25, Gent MPN, Kiyomoto RK Comparison of canopy and flag leaf net carbon dioxide exchange of 1920 and 1977 New York winter wheats. Crop Science 25, Gifford RM A comparison of potential photosynthesis, productivity and yield of plant species with differing photosynthetic metabolism. Australian Journal of Plant Physiology 1, Gifford RM Partitioning of photoassimilate in the development of crop yield. In: Cronshaw J, Lucas WJ, Giaquinta R, eds. Plant biology, Vol. 1. Phloem transport. New York: Alan R. Liss, Goudriaan J, van Laar HH Calculations of daily totals of the gross CO 2 assimilation of leaf canopies. Netherlands Journal of Agricultural Science 26, Gray JC, Paul MJ, Barnes SA, Knight JS, Loynes A, Habash D, Parry MAJ, Lawlor DW Manipulation of phosphoribulokinase and phosphate translocator activities in transgenic tobacco plants. Journal of Experimental Botany 46, Harrison SA, Boersma HR, Ashley DA Heritability of canopy apparent photosynthesis and its relationship to seed yield in soybeans. Crop Science 21, Heichel GH Confirming measurements of respiration and photosynthesis with dry matter accumulation. Photosynthetica 5, Hesketh JD Limitations to photosynthesis responsible for differences among species. Crop Science 3, Humphries EC, Thorne GN The effect of root formation on photosynthesis of detached leaves. Annals of Botany 28, Irvine JE Relations of photo synthetic rates and leaf and canopy characters to sugar cane yield. Crop Science 15, Johnson RC, Kebede H, Mornhinweg DW, Carver BF, Rayburn AL, Nguyen HT Photosynthetic differences among Triticum accessions at tillering. Crop Science 27, Kanemasu ET, Hiebsch CK Net carbon dioxide exchange of wheat, sorghum and soybean. Canadian Journal of Botany 53, Khan MA, Tsunoda S Evolutionary trends in leaf photosynthesis and related leaf characters among cultivated wheat species and its wild relatives. Japanese Journal of Breeding 2Q, Kiniry JR, Jones CA, O'Toole JC, Blanchet R, Cabelguenne M, Spanel DA Radiation-use efficiency in biomass accumulation prior to grain-filling for five grain-crop species. Field Crops Research 20, Krapp A, Chaves MM, David MM, Rodriques ML, Pereira JS, Stitt M Decreased ribulose-l,5-bisphosphate carboxylase/oxygenase in transgenic tobacco transformed with 'antisense' rbcs. VIII. Impact on photosynthesis and growth in tobacco growing under extreme high irradiance and high temperature. Plant, Cell and Environment 17, Lawlor DW Effects of water and heat stress on carbon metabolism of plants with C 3 and C 4 photosynthesis. In: Mussell H, Staples RC, eds. Stress physiology in crop plants. New York: Wiley, Lawlor DW Photosynthesis: molecular, physiological and environmental processes, 2nd edn. Burnt Mill, Harlow: Longman Scientific and Technical. Lawlor DW, Keys AJ Understanding photosynthetic adaptation to changing climate. In: Fowden L, Mansfield T, Stoddart J, eds. Plant adaptation to environmental stress. London: Chapman and Hall, Lawlor DW, Kontturi M, Young AT Photosynthesis by flag leaves of wheat in relation to protein, ribulose bisphosphate carboxylase activity and nitrogen supply. Journal of Experimental Botany 40, Lawlor DW, Mitchell RAC, Franklin J, Driscoll SP, Delgado E Facility for studying the effects of elevated carbon dioxide concentration and increased temperature on crops. Plant, Cell and Environment 16, Le Cain DR, Morgan JA, Zerbi G Leaf anatomy and gas exchange in nearly isogenic semi-dwarf and tall winter wheat. Crop Science 29, Legg BJ, Day W, Lawlor DW, Parkinson KJ The effects of drought on barley growth: models and measurements showing the relative importance of leaf area and photosynthetic rate. Journal of Agricultural Science, Cambridge 92, Mahon JD. 1990a. Photosynthesis and crop productivity. In: Zelitch I, ed. Perspectives in biochemical and genetic regulation of photosynthesis. New York: Alan R. Liss, Inc., Mahon JD Photosynthetic carbon dioxide exchange, leaf area, and growth of field-grown pea genotypes. Crop Science 30, Makino A, Mae T, Ohira K Differences between wheat and rice in the enzymatic properties of ribulose -1,5-bisphosphate carboxylase/oxygenase and the relationship to photosynthetic gas exchange. Planta 174, McCree KJ, Troughton JH Prediction of growth rate at different light levels from measured photosynthesis and respiration rates. Plant Physiology 41, Medrano H, Keys AJ, Lawlor DW, Parry MAJ, Azcon-Bieto J, Delgado E Improving plant production by selection for survival at low CO 2 concentrations. Journal of Experimental Botany 46, Mitchell RAC, Lawlor DW, Young AT Dark respiration of winter wheat crops in relation to temperature and simulated photosynthesis. Annals of Botany 67, Mitchell RAC, Mitchell V, Driscoll SP, Franklin J, Lawlor DW Effects of increasing CO 2 concentration and temperature on growth and yield of winter wheat at two levels of nitrogen application. Plant, Cell and Environment 16, Milford GFJ, Biscoe PV, Jaggard KW, Scott RK, Draycott AP Physiological potential for increasing yields of sugar beet. In: Hurd RG, Biscoe PV, Dennis C, eds. Opportunities for increasing crop yields. Boston: Pitman, Monteith JL Climate and the efficiency of crop production in Britain. Philosophical Transactions of the Royal Society of London B281, Monteith JL Does light limit crop production? In: Johnson CB, ed. Physiological processes limiting plant productivity. London: Butterworths, Morgan JA, Le Cain DR, Wells R Semi-dwarfing genes concentrate photosynthetic machinery and affect leaf gas exchange of wheat. Crop Science 30, Natr L Varietal differences in the intensity of photosynthesis. Rostlinna Vyroba 12, (In Czech). Nelson CJ, Asay KH, Horst GL Relationship of leaf

13 photosynthesis to forage yield of tall fescue. Crop Science 15, Paul MJ, Driscoll SD, Lawlor DW The effects of cooling on photosynthesis, amounts of carbohydrate and assimilate export in sunflower. Journal of Experimental Botany 42, Paul MJ, Knight JS, Habash D, Parry MAJ, Lawlor DW, Barnes SA, Loynes A, Gray JC Reduction in phosphoribulokinase activity by antisense RNA in transgenic tobacco: effect on CO 2 assimilation and growth in low irradiance. The Plant Journal 7, Pearman I, Thomas SM, Thome GN Effect of nitrogen fertilizer on photosynthesis of several varieties of winter wheat. Annals of Botany 43, Peng S, Krieg DR, Girma FS Leaf photosynthetic rate is correlated with biomass and grain production in grain sorghum lines. Photosynthesis Research 28, 1-7. Peterson RB, Zelitch I Relationship between net carbon dioxide assimilation and dry weight accumulation in fieldgrown tobacco. Plant Physiology 70, Rabbinge R, Goudriaan J, van Keulen H, Penning de Vries FWT, van Laar HH (eds) Theoretical production ecology: reflections and prospects. Wageningen: Pudoc. Russel G. Wilson GW An agro-pedo-climatological knowledge base of wheat in Europe. JAC 158. Rowland-Bamford AJ, Allen LH, Baker JT, Boote KJ Carbon dioxide effects on carbohydrate status and partitioning in rice. Journal of Experimental Botany 41, Sharkey TD Photosynthesis in intact leaves of C 3 plants: physics, physiology and rate limitations. Botanical Review 51, Sharkey TD Evaluating the role of Rubisco regulation in photosynthesis of C 3 plants. Philosophical Transactions of the Royal Society of London B323, Sheen J Feedback control of gene expression. Photosynthesis Research 39, Sinclair TR Limits to crop yield? In: Boote KJ, Bennett JM, Sinclair TR, Paulsen GM, eds. Physiology and determination of crop yield. Madison, Wisconsin: American Society of Agronomy, Inc., Sinclair TR, Horie T Leaf nitrogen, photosynthesis, and crop radiation use efficiency: a review. Crop Science 29, Photosynthesis, productivity and environment 1461 Stitt M Limitation of photosynthesis by carbon metabolism. I. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO 2. Plant Physiology 81, Vietor DM, Musgrave RB Photosynthetic selection of Zea mays L. II. The relationship between CO 2 exchange and dry matter accumulation of canopies of two hybrids. Crop Science 19, von Caemmerer S, Farquhar GD Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, Waddington SR, Osmanzai M, Yoshida M, Ransom JK The yield of durum wheats released in Mexico between 1960 and Journal of Agricultural Sciences, Cambridge 108, Wardlaw IF The control of carbon partitioning in plants. New Phytologist 116, Watanabe N, Evans JR, Chow WS Changes in the photosynthetic properties of Australian wheat cultivars over the last century. Australian Journal of Plant Physiology 21, Wilson D Variation in leaf respiration in relation to growth and photosynthesis of Lolium. Annals of Applied Biology 80, Woodrow IE Control of steady-state photosynthesis in sunflowers growing in enhanced CO 2. Plant, Cell and Environment 17, Woodrow IE, Berry JA Enzymatic regulation of photosynthetic CO 2 fixation in C 3 plants. Annual Review of Plant Physiology and Plant Molecular Biology 36, Yelle S, Beeson RC, Trudel MJ, Gosselin A Acclimation of two tomato species to high atmospheric CO 2. II. Ribulose-l,5-bisphosphate carboxylase/oxygenase and phosphoenol-pyruvate carboxylase. Plant Physiology 90, Zelitch I Improving the efficiency of photosynthesis. Science 188, Zelitch I The close relationship between net photosynthesis and crop yield. BioScience 32, Zelitch I, Day PR The effect on net photosynthesis of pedigree selection for low and high rates of photorespiration in tobacco. Plant Physiology 52, 33-7.