Photosynthesis — is it limiting to biomass production?

Biomass 8 (1985) 119-168

P h o t o s y n t h e s i s - is it L i m i t i n g to B i o m a s s P r o d u c t i o n ? C.L. Beadle 47 Davies Avenue, Leeds LS8 1JZ, UK a

and S.P. Long Department of Biology, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, UK (Received: 7 April, 1985)

A BS TRA CT While it is recognized that photosynthesis is the ultimate source o f biomass production in plants, little attempt has been made to exploit the considerable knowledge o f the light and dark reactions o f the process to increase the production o f biomass. The question therefore arises as to whether photosynthesis limits production. One o f the major problems in assessing the conversion efficiency o f solar energy to biomass has been the use o f techniques which inevitably underestimate this efficiency. Nevertheless, short-term measurements o f production suggest that conversion efficiencies are close to the theoretical photochemical efficiency o f photosynthesis (3.5-4%). C4 plants are ultimately more productive than C3 plants as they are able to concentrate C02 inside the leaf and so eliminate photorespiration. It is suggested that improved adaptation o f the photosynthetic process to sub- and supra-optimal conditions and more effective exploitation o f leaf area index for increased light interception will lead to increased biomass production rather than any attempts to improve the efficiency o f the process per se. Key words: Photosynthesis, limits to production, biomass, conversion efficiency of solar radiation. a Present address: Tasmanian Regional Group, CS1RO Division of Forest Research. 'Stowell', Stowell Avenue, Hobart, Tasmania, Australia 7000. 119 Biomass 0144-4565/85/$03.30- © Elsevier Applied Science Publishers Ltd, England, 1985. Printed in Great Britain

120

C. L. Beadle, S. P. Long

1. I N T R O D U C T I O N Whilst other factors m a y determine actual productivity, photosynthesis sets the potential upper limit on the efficiency with which solar radiation may be converted into stored chemical energy, i.e. biomass. Photosynthesis is the ultimate source of all biomass production. At this level, therefore, it is reasonable to argue that factors limiting photosynthesis limit potential production. Photosynthesis also provides us with a fundamental unit o f productivity, viz. that of carbon (C) gain. It follows that the total net primary production of the world is the total p h o t o s y n t h e t i c gain of C (photosynthesis) less the respiratory losses of C. Present estimates suggest that net annual primary production (NAPP) amounts to 8 × 10 l° t carbon which is fixed into 1.7 X l011 t of organic matter (Table 1). NAPP is therefore 10% of existing stored biomass (8 × 1011t C) within which forests are clearly the most important resource (90%). Carbon stored as atmospheric CO2, or CO2 in ocean surface layers and in soil and ocean organic matter complete the carbon balance, and each is of similar order to that stored in biomass. Terrestrial NAPP (4.8 × 1010 t C) is more than half total NAPP, and the annual input from cultivated land (0.4 × 101°t C), 8.3% of the total. As the terrestrial surface area of the earth is 13.1 Gha (= 1.31 × 10 s km 2) and cultivated land accounts for 1-5 Gha (arable only) i.e. > 11%, the loss o f land to cultivation has on average led to a loss of primary production 1 and of potential photosynthesis. The basic substrates o f photosynthesis are water (H20) and carbon dioxide (CO2) and the source of energy for their conversion to organic matter is light. If the annual incorporation of light energy into biomass (NAPP) is compared with the total incoming short-wave radiation at the earth's surface, the light conversion efficiency is, approximately, a mere 0.1%. The energy content equivalent to NAPP (3 X l021 k J) however, is still 10 × the world's annual energy use and 200 × our food energy consumption. 2 The p h o t o s y n t h e t i c process At the physico-chemical level photosynthesis represents the conversion of light energy into stored chemical energy through the reduction of CO2 to triose phosphate. For convenience the process can be divided into three phases: light t r a p p i n g ~ CO2 reduction ~ biomass production.

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Photosynthesis - is it limiting to biomass production?

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There have been many recent reviews of current knowledge of this complex of processes? The following is a brief summary of the essential features o f photosynthesis. In all eukaryotes, the basic steps in photosynthesis occur within the chloroplast. Light trapping occurs on the chloroplast internal membranes. Light energy absorbed by chlorophyll and other photosynthetic pigments, e.g. carotenoids, is channelled to one of two types of reaction centre molecules, P68o or PToo. At P68othe energy of one photon is used to eject an electron through a series of intermediates to PT00, where the energy of a further p h o t o n is used to pass the electron on to ferredoxin and finally to reduce NADP. The electron hole created at P68o is filled by water-splitting which results in the evolution of oxygen and production of protons. One intermediate between P680 and Pvoo, plastoquinone (PQ), is reduced on the membrane outer surface, where it binds protons, and reoxidized on the inner surface where it releases its protons. The passage of PQ across the membrane, combined with water-splitting, creates a proton gradient across the membrane and the energy of this gradient is utilized in ADP phosphorylation via an ATPase (CF) in the membrane. A cyclic electron transport pathway around PT00 involving PQ, may also occur and ensure that a proton gradient can be maintained even when there is no terminal aceeptor for the non-cyclic pathway. The reduced NADP and ATP are used primarily to reduce CO 2. CO2 is assimilated by reaction with the 5-carbon sugar, ribulose-l,5b i s p h o s p h a t e (RubP). This reaction is catalysed by RubP carboxylase/ oxygenase ( R u b i s C O ) and the products are two molecules of the three carbon carboxylate, phospho-glycerate (PGA). The PGA is first phosphorylated and then reduced, consuming ATP and reduced NADP, to yield glyceraldehyde 3-phosphate, a triose phosphate. It is this conversion of the carboxylate to an aldehyde which transfers the energy gained in electron transport to the plant's long-term chemical energy s t o r e - - c a r b o h y d r a t e . The triose phosphate may then be recycled to synthesize more RubP, so completing a cycle, termed the Calvin or RPP cycle, or used for synthesis of carbohydrates, fats or proteins. Besides carboxylation, R u b i s C O will also catalyse the oxygenation of RubP to yield PGA and one molecule of the 2-carbon c o m p o u n d phosphoglycollate. Phosphoglycollate may be metabolized in photosynthetic cells to PGA via the C2 or glycollate pathway, but this will cause the loss of CO2 and consumption of ATP and reduced NADP produced in the light reactions. Physiologically, this process is a light-dependent

124

C. L. Beadle, S. P. Long

consumption o f oxygen and evolution of CO2, termed photorespiration. Since CO2 and 02 compete for RubP, photorespiration may be prom o t e d or inhibited by varying the CO2 concentration. A number of mechanisms have evolved for the concentration of CO2 at the site of R u b i s C O to eliminate photorespiration. The best known o f these are the three types of C4 photosynthesis. In C4 photosynthesis, an additional photosynthetic pathway, the C4 dicarboxylate cycle, collects CO2 from" the outer tissues of the leaf and releases it inside the cells o f the inner photosynthetic tissue in which R u b i s C O is localized. This may increase the effective CO2 concentration 100-fold and so eliminate photorespiration, a The end product o f photosynthesis, the triose sugar which leaves the RPP-cycle, forms the basic assimilate or carbon skeleton for biomass production. After biochemical interconversion, it will be incorporated into structural material of different plant tissues or alternatively used as a respiratory source for the growth of new and the maintenance of old tissues. At the whole plant level much research of photosynthesis has been concerned with the assimilation of CO2 by whole leaves (A) and its relation to environmental variables. Of more pertinence is the net photosynthetic rate of the canopy (the net influx of CO2 to a canopy = A c ) , which is given by

Ac = A X L

(1)

where /[ = mean A of individual leaves in the canopy L = leaf area index (m 2 leaf m -2 ground) Canopy photosynthesis is therefore determined by A and the distribution and size of the photosynthetic surface in the canopy. This normally means that the efficiency with which light is intercepted is lower for individual leaves than for the canopy.

Biomass production To assess the efficiency o f light energy conversion, a knowledge of total plant biomass production must be acquired. This section reviews information on biomass production on a global scale and examines the serious limitations o f current information.

P h o t o s y n t h e s i s - is it l i m i t i n g to b i o m a s s p r o d u c t i o n ?

125

Two measures o f production must be distinguished. Gross primary production (Pg) is the photosynthetic assimilation of organic m a t t e r by a plant c o m m u n i t y during a specified period, including the amount used by respiration. Net primary production (Pn) is Pg less respiratory losses (Rt). In an ecological context Pg is the sum o f the photosynthetic inputs, Rt is the sum o f the respiratory losses and Pn is the total photosynthetic input available to other trophic levels. Biomass production will here refer to Pn. Thus Pn = Pg -- Rt

(2)

Total NAPP therefore sums the Pn o f different ecosystems during an annual cycle (Table 1). The areas occupied by the different ecosystems of the world and their mean, m a x i m u m and total productivities show that the two groups of ecosystems of immediate potential and actual importance to man through their primary production are the natural forests which occupy 4-5 X 107 km 2 with an NAPP amounting to 72 Gt year -x and the natural grasslands which occupy 3.0 X 107 km 2 with an NAPP 6f 2 Gt year-l.l.s In spite of differences in estimated Pn, forests have similar efficiencies at all latitudes which appear to be approximately double those found in productive grassland communities (Table 1). Although small discrepancies are apparent between the values purporting to be total and ecosystem Pn (Table 1), these fade into insignificance when compared to their accuracy. This is particularly the case in natural ecosystems, an unfortunate aspect of the techniques used to assemble this data which rarely if ever measure actual Pn- Secondly, they are essentially measurements o f a minute and non-random sample of the whole biosphere. Continuous measurements of the gaseous fluxes of COz into and out of the plants of a c o m m u n i t y ( = A t ) would be needed to directly determinePn. At present this is technically a very difficult measurement and has only been used in a handful of instances. 6' 7 Most commonly Pn has been estimated from measurements of the sum o f change in plant c o m m u n i t y biomass and losses of this biomass through death and grazing. Thus Pn = AB + L D + L G + L E

(3)

LD (loss through death) = AD + r/}

(4)

and

C. L. Beadle, S. P. Long

126

where = biomass change over a specified time interval t L c = direct plant losses to consumer organisms (herbivores and parasites) during t LE = losses through r o o t exudation AD = dead biomass change over a specified time interval t r = relative rate o f disappearance or decomposition o f plant material over a specified time interval t = mean quantity of dead vegetation present during the interval t AB

Whilst this approach appears relatively simple, in practice many problems arise, some merely from definition. F o r example biomass (B) refers strictly to organic (ash-free dry) weight and to living material. Thus many studies have not taken account of the inorganic or ash content which range typically from 10-30% of the dry weight, amounting to a very significant source o f error in Pn.8 Defining living material is a sampling problem in the treatment of senescing leaves which are often indistinguishable from dead leaves, and in separating live from dead roots. It is still more difficult to deal with organs which show sequential senescence such as grass leaves which may have dead tips and healthy bases. Further, biomass (B) is usually measured by harvesting sub-samples o f vegetation in natural ecosystems where heterogeneity results in large variation between samples and decreased precision. Even when a large n u m b e r (n > 50) o f replicates are used in a simple grassland community, confidence limits on estimates o f mean B in the region of + or - - 4 0 % are not u n c o m m o n ? '9 In forests, where stem biomass is often estimated from regression equations (based on the harvest of a few plants) o f biomass against the stem diameter at breast height (DBH) the variation about the regression for trees of 2 m DBH ranged from about 600 to 3 0 0 0 g y e a r -l , an error on the regression estimate of + or - - 60%.10 Many estimates o f Pn are also largely based on peak biomass o f the c o m m u n i t y (Bmax) or individual species (~Bmax), i.e. LG and to some extent LE are ignored. This is valid if LD and L~ are zero before the peak biomass is attained and if production is zero afterwards. Any deviation would cause underestimation o f Pn, though one can only hypothesize by h o w much. In one comparative study of techniques for measuring Pn, a factor o f as much as 4× was suggested. H All of these

P h o t o s y n t h e s i s - is it limiting to biomass p r o d u c t i o n ?

127

techniques suffer from certain sources of error and even the various techniques devised for estimating LD usually underestimate its true value.12 It is quite obvious that plants which show sequential senescence will lose large amounts o f leaf and root material before Bma x is reached. An estimate o f r and LD is therefore essential if a serious underestimation o f Pn is to be avoided. F r o m the little comparative data available this underestimation could be as much as 75% for above-ground production and even more for below-ground. 13 Indeed in stable communities, B may remain relatively constant throughout the year to the extent that estimates o f P n will be heavily dependent on the estimate o f t . Losses to grazing (Lc) may or may not be difficult to measure. Those to large herbivores may be estimated simply by the use of exclosures or from herbivore production. Insect grazers however, especially sap sucking insects, can only be excluded by the use of very fine mesh materials which unfortunately alter the plant microenvironment and significantly affect growth. Few estimates of production include below-ground biomass, yet this may account for up to 83% o f the total biomass. 14 Many wetland communities have considerable underground biomass 12'1s and in other communities root production may contribute more to Pn than previously suspected, particularly if the turnover of the fine root population is high. F o r example, r o o t : s h o o t production ratios are higher in temperate herbaceous than temperate forest communities. 16 The differences between the efficiencies of grasslands and forests may therefore be less than suggested in Table 1 since these figures are based on above-ground NAPP only. Exudation and leaching (LE) of organic c o m p o u n d s from roots into the soil water may account for up to 50% of Pn. 17. Both roots and root exudates may therefore make substantial contributions to Pn. The problems o f obtaining actual Pn can be illustrated by taking a salt marsh ecosystem as a case study. Of 200 estimates of Pn, 190 were based solely on changes in biomass (AB). 18 Some equated P , to Bma× recorded through one year, others to the difference between minimum and maximum recorded B for one year. Some defined biomass correctly, viz. B, other studies as B plus D. Only ten studies attempted to measure LD and only three took account of below-ground biomass. When the different techniques o f estimating Pn are applied to the same

128

C. L. Beadle, S. P. Long

area of salt marsh, estimates of Pn vary by a factor of 4.1~' 12 Thus, what appears at first sight to be a well defined ecosystem with respect to Pn is in fact poorly understood. Since it is only the above-ground biomass of standing vegetation which can usually be harvested and is therefore of potential value to man, it is arguable that Pn is of little interest. This is true for harvestable biomass, but not true where we wish to understand photosynthetic efficiency of light energy conversion into biomass. Most, if not all, estimates of Pn for natural ecosystems are gross underestimates of the true Pn, and the quoted conversion efficiencies of light energy into biomass not a true measure without taking account of the biomass formed below-ground or that lost by any cause before harvesting. In the most productive forest ecosystems therefore, the conversion efficiency of solar radiation may considerably exceed rather than be 1% (Table 1). In contrast to natural communities, many detailed and precise estimates of the productivity and efficiency of crops exist. However, interest has naturally focused on the harvested material and as with natural ecosystems, few studies have been concerned with the production of roots or measuring parts of the plants which die and are shed before harvesting. Estimates of Pn from arable land total 9 Gt and vary from 1 to 88 t ha -1 (mean 6 to 6.5 t ha-l), a direct result of the confounding of environment, cultivation practice and economic constraints on the expression of genotypic or environmental potential of crop plants. 1 For many species, only a proportion of the plant is of economic importance and in several instances they have been deliberately bred to optimize economic yield at the expense of biomass yield. Secondly, economic yields are often achieved at planting densities which are less than those necessary to maximize Pn .19 Maximum biomass yields (tha -1year-l) and photosynthetic efficiencies are only realized with maximum input of nutrients, a good water supply, optimum climatic conditions and pest control. Where these conditions prevail, apparent conversion efficiencies of solar radiation of C3 plants are normally less than those of C4 plants which can exceed 1-5% in productive C4 forage grasses (Table 2). This is clearly a consequence of higher short-term growth rates and conversion efficiencies which exceed 3%. As a result, the maximum biomass yields of terrestrial C4 plants (approximated by harvest index [HI], the proportion of the crop of potential value to man: this is equivalent to above ground

TABLE 2 Good Annual and Short-Term Biomass Production and the Respective Conversion Efficiencies of Total Short-Wave Radiation of C4 and C3 Agricultural Crops from Contrasting Environments 2' ag,20, 21,32 Type

Annual yield (t ha -1 year -1)

Efficiencya, b (%)

Shortterm yield (g m -2 day -1)

Efficiencya, c (%)

C4 C4

88 21

1,6 -

39 54

4.2 4.3

C4 27 C4 C3 Ca

66 0-8 23 22 38

37 2.9 51 27 18

3.8 3-0 2.9 2.0

C3 C3 C3

29 30 11

0.3

11 23 37

1.4 1.4 2.3

Tropical/sub-tropical

Pennisetum purpureum Pennisetum typhoides Saccharum officaarum Zea mays C4 Sorghum spp. Oryza sativa Manihot esculenta Elaeis guineensis Medicago sativa Solanium tuberosum Pinus radiata Gossypium hirsutum Glycine max

1-2 52 0.7 1.1

C3

-

-

41

2.7

Ca C3

9

0.2

27 -

2.1 -

C3 C3 C3 C3

32 23 11 21

1.1 1,3 0.5 1.1

31 8 23 21

4.3 2.5 2.5 2.2

Temperate

Beta vulgaris Lolium perenne Solanium tuberosum Brassica oleracea Triticum aestivum Hordeum Festuca arundinacea Dactylis glomerata Trifolium spp. Other Water hyacinth Algae Salvinia

C3

12

0.4

18

1.7

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-

-

23 43 40 23

1.8 3.5 3.3 1-9

C3 C3 C3

250 91 250

-

24 -

1.5 -

M u l t i p l y efficiencies b y x 2 for % c o n v e r s i o n e f f i c i e n c y o f P A R . b T h e e f f i c i e n c y reflects t h e h a r v e s t i n d e x o n l y a n d n o t t o t a l B or Pn. c T h e e f f i c i e n c y reflects seasonal a n d g r o w t h - r e l a t e d f a c t o r s w h i c h result in faster s h o r t - t e r m rates o f h a r v e s t a b l e b i o m a s s p r o d u c t i o n t h a n o b s e r v e d w h e n c a l c u l a t e d o n an a n n u a l basis.

a

130

C. L. Beadle, S. P. Long

production in Pennisetum pur pur eum and Saccharum officinarum) normally exceed those of terrestrial C3 plants, 22'23 except in nutrient rich marine or freshwater systems where biomass production can equal or exceed that of agricultural crops as it is not restricted by water or substrate (CO2) supply (Table 2). N.B. Figures in columns 1 and 2 of Table 2 underestimate Pn and biomass production as HI only is measured and this percentage varies markedly between crops. Annual food production (approaching 2000 Mt or around 22% of estimated Pn for arable land 1'23 (Table 1)) currently exceeds that required by the world population by 10% and countries in food surplus could feed those in food deficit if political and economic restraints were removed.24 Nevertheless, as population growth in food deficit countries often exceeds that of improvements in production and as long as world population continues to grow, it remains necessary to sustain further increases in food production.

Conclusion to part 1 The productive capacity of the world is limited by cultural, socioeconomic and political conditions. To this extent maximum yields, particularly of food crops are unlikely to be attained where economic constraints dominate productivity or where net margins are commensurate with economically optimum rather than maximum yields. Nevertheless, should these constraints be removed, including limitations imposed by mineral deficiencies, plant disease and agronomic practice, dramatic increases in food production are projected.2s Canopy photosynthesis (F¢) sets the ultimate limit on biomass production. Any improvement in photosynthetic efficiency means increasing our potential ability to produce biomass, whether for food, fibres or fuels. We should examine the extent to which we exploit the photosynthetic potential of plants at present. Clearly, we understand much about the fundamental features of photosynthesis and it is arguable that the process cannot be made substantially more efficient at the physical and chemical level, when there would have been strong pressures for such improvement by natural selection over a very long period (> 10 l° years). At the level of production, however, it is difficult to assess the efficiency with which dry matter can be produced even in productive ecosystems, as Pn has been consistently underestimated. It is possible to calculate the potential conversion efficiency of solar radiation into dry matter and then suggest means whereby this may be realized.

Photosynthesis

-

is

it limiting to biomass production?

131

2. LIMITS TO SOLAR ENERGY EFFICIENCY AND THE INFLUENCE OF THE ENVIRONMENT

Limits to efficiency

Photosynthetically active radiation

Sunlight energy for biomass production is obtained from the total short-wave radiation incident at the earth's surface (I0). The major proportion of this radiation (99%) is in the waveband 0.3 to 4/~m and t h e longer wavelengths in particular are not available for photosynthesis in the sense that they cannot be absorbed by the photosynthetic pigments. These pigments harvest photons from the visible spectrum only (0.4-0.7/~m) which is referred to as photosynthetically active radiation (PAR). Losses of available energy to photosynthesis accrue, however, due to the physical properties of leaves and more fundamental energy considerations for successful conversion and storage of sunlight as chemical energy in the photosynthetic process. There is therefore a defined maximum proportion of incident PAR as well as total solar energy which can be utilized for ATP, NADPH and ultimately biomass production even when other factors are not limiting photosynthesis. Table 3 illustrates the proportions of I0 which are lost through inefficiencies at different stages in the photosynthetic process. PAR is approximately 0.5 as a proportion of 10.27 This figure is independent of solar elevation and includes a diffuse component which if overlooked results in an underestimate of PAR of approximately 5%. Some incident PAR is lost due to the physical properties of leaves which reflect and transmit light by multiple reflection at cell walls. Reflectivity and transmissivity is a complex function of canopy structure and even if full vegetation cover is assumed, no single estimate of either is possible. As forward and backward scattering of light is similar however, the quality and quantity of reflected light is nearly equal.27'28 Published estimates of reflection and transmission coefficients suggest that losses of sunlight are 0-05-0-1 as a proportion of I0 for each. Relative sunlight remaining is therefore 0-4-0-45 and if further losses from inactive absorption by cell walls, cytoplasm and non-photosynthetic pigments are estimated as 0 . 0 2 5 , 29 the proportion available for light harvesting is then 0.38-0.43 (Table 3).

132

C. L. Beadle, S. P. Long TABLE 3

Inefficiencies in the Conversion of Sunlight Energy Incident on Vegetation into Biomass

Energy losses due to."

1. Energy lying outside photosynthetically active region (PAR) 2. Reflection and transmission 3. Absorption by inactive components 4. Photochemistry (degradation of energy of absorbed photons) 5. Carbohydrate synthesis, i.e. C-metabolism (based on d-glucose) 6. Photorespiration (Ca plants only) 7. Dark respiration in C3 plants ~ in C4 plants

Relative solar energy % loss

% remaining

50 5-10 2.5

50 40-45 37.5-42-5

8.7

28.8-33.8

18.9-22.2 2.5-2.9 3.7-4.3 4.9-5 -8

9.9-11.6 7-4-8.7 3.7-4.4 5.0-5.8

The figures are given in relative terms (total incident sunlight being 100%). This table is developed from Table 1 in Bolton (1978). 26 Underlined values indicate final conversion efficiencies of PAR into biomass. Ligh t harvesting

The reaction which incorporates the energy of sunlight into ATP and NADP through the splitting of water molecules can be summarized as 2H20 + sunlight ~ 02 + 4H ÷ + 4e

(5)

and is initiated by p h o t o n capture which transfers pigment molecules to the excited state. At this point energy losses occur as part of photochemistry. Their source requires an appreciation of the excitation reaction during light harvesting. Light absorbed at the blue end of the spectrum has a shorter wavelength but higher energy than that absorbed in the red region which can be used directly to drive photosystems I & II. The excess energy derived from blue p h o t o n s is therefore degraded and lost as heat. Bolton 26 has calculated this loss as ca. 0.09 o f radiant energy. The proportion available for driving electron transport and for storage as chemical energy is therefore 0.28-0-34 of radiant energy.

Photosynthesis - is it limiting to biomass production?

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Electron transport and carbon reduction

As NADPH is used to reduce CO2 to simple carbohydrate, it follows from eqn 2 that: 4H + + 4e + CO2 -+ (CH20) + H20

(6)

This equation incorporates a sequence of reactions which in some instances involve an input of energy (ATP) to activate the substrates and drive the chemical reaction forward. The RPP-cycle must be exergonic if the final products are to remain stable however and this loss of energy sufficient to form an activation barrier between the level of net energy storage and a back reaction to the final level of excitation. Further, for m a x i m u m work output, any chemical process must accommodate large irreversibility losses (up to 50%), 3° and some of these will occur during photochemistry, electron transport and carbon metabolism. Bolton 26 calculates a m a x i m u m storage efficiency of any photochemical reaction (using sunlight) to be 0.15-0.16 as a proportion of total radiant energy (i.e. I0). The potential storage efficiency of gross photosynthesis has been found to be somewhat lower than this value, though a precise estimate is not possible as certain assumptions must be made, particularly with respect to q u a n t u m yield (4~, a dimensionless constant = tool CO2 fixed (tool photons absorbed)-l). As can be seen from eqn (6) above, 4 electrons must be transferred to reduce one molecule of CO2 to carbohydrate, but as two photosystems are required, i.e. 2 photons per electron moved, a m i n i m u m of 8 quanta (4~ = 0-125) must be absorbed. Furthermore, as the reaction centres ( P S I and PS II) are excited by light of 700 and 680 nm respectively, a mean quantum energy absorbed during photochemistry equivalent to that of monochromatic light at 690 nm can be assumed. One mole of 690 nm light contains 173.3 kJ. As 1 mote of carbohydrate conserves 477.0 k J, it follows that the maximum efficiency of electron transport and photosynthetic reduction of CO2 is 34.4% excitation energy. As this value is close to the theoretical photochemical efficiency of photosynthesis assuming that half the energy is trapped and half used for external work, 31 photosynthesis is clearly a very efficient process at the chloroplast level. The energy losses through these stages are therefore 1 9-22% and the relative storage efficiency of gross photosynthesis 9.9-11.6% of solar radiation. 26 It should be stressed that these are minimum (energy losses) and maximum (efficiency

134

C. L. Beadle, S. P. Long

of gross photosynthesis) values respectively, which will only be approached in exceptional circumstances when light is the sole factor limiting photosynthesis. Similar estimates of gross photosynthetic efficiency but with less detailed analysis have been published previously.3°'32'3a In an alternative approach using actual data for Phaseolus vulgaris L. and quantum yields corrected for respiratory losses, the overall efficiency was calculated to be 9.5% of solar radiation.26 These conversion efficiencies are theoretical of course and will never be approached in practice, as respiratory losses of carbon always accompany its photosynthetic reduction in the presence of oxygen (Table 3). Respiration Photorespiration means an immediate loss of C to net CO2 fixation, except in C4 plants. The products of photosynthesis are utilized in the development and differentiation of new cells as well as supporting the existing tissues of the plant. This requires energy, which is also derived from photosynthetic products and harnessed through dark respiration. It is therefore possible to distinguish between the gross efficiency of photosynthesis, which is of theoretical importance only,and working maxima corrected for respiratory losses of C. Steady-state measurements of photorespiration are possible with labelled COs and labelled 02, but the rates measured are necessarily underestimates owing to dilution of the label by respiratory COs and photosynthetic 02, respectively)a' as Some early estimates with labelled leaf discs suggested that rates of photorespiration could exceed 50% gross photosynthesis, but estimates from whole plants suggest much lower values, 14-18% of gross photosynthesis.36' 3~ A more appropriate estimate in the context of biomass production is 25% for field-grown wheat. 38'39 As photorespiration as a proportion of photosynthesis increases with temperature, the actual percentage may increase with environmental stress, in particular water stress. If 25% is representative, by simple extrapolation the maximum conversion efficiency net of photorespiration in C3 plants is lowered to 0.074-0.087. Photorespiration does not normally occur in C4 plants, but some internal recycling of CO2 through the photorespiratory pathway can occur,4° thus some loss in efficiency will result. Dark respiration has been considered to consist of two components, related to the photosynthesis and existing dry weight of the plant

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respectively. The first c o m p o n e n t relates respiration to synthetic processes in the plant. By resort to handbooks of biochemistry and by assuming maximum efficiency of substrate and energy utilization by plants, the theoretical conversion efficiency of p h o t o s y n t h a t e to dry matter (Zea m a y s ) expressed in terms of carbohydrate is 75%. 41 This is in close accord with practical results (in Loliurn perenne, H o r d e u m vulgare and Z. m a y s ) and suggests that the respiratory c o m p o n e n t associated with synthesis and growth is approximately 25% of current photosynthesis, and that the above assumptions are correct. The second comp.onent of respiration is related to the maintenance of existing structures and organization. These respiratory losses are more difficult to estimate from a theoretical approach because of difficulties in identifying the processes involved, but over a growth period may equal the requirements for synthesis. 42'43 The respiratory efflux of CO2 can therefore account for 50% net photosynthesis (A). 44 Conversely, total Pn is approximately half that of the p h o t o s y n t h a t e produced by the leaves. The theoretical upper limits of biomass production are therefore 0.037-0.044. Quan turn yield

At low quantum flux densities (Q), i.e. Q < 200/zmol m -2 s-I in many plants, photosynthesis is strictly light limited and proportional to O. The slope of this relationship, dA/dQ when (2-+ 0, is the quantum efficiency, i.e. number of moles of COa assimilated per mole of photons (qS). This was assumed in the preceding discussion to have a theoretical value of 0.125, i.e. the quantum requirement (1/4) is 8.11l practice, the physiological 1/4 of C 3 plants in 2c/4 oxygen, where photorespiration would be fully inhibited, and of C4 plants is 13.6 and 18.6 respectively. 4s the greater energy requirements of C4 plants resulting from the additional pathways of carbon flow in C4 photosynthesis. 46 These values of 1/4 include inactive absorption and degradation of absorbed light energy which cannot be separated experimentally from that used for electron transport and carbon fixation, but which accounts for just over a quarter of the energy absorbed (Table 3). The precise physiological 1/4 for conversion to glucose in C 3 and ('4 plants was therefore 10.0 and 13.7 respectively in this experiment. This difference between the measured and estimated 1/4 is probably due to a higher minimum quantum requirement and to the energy demand of other light activated processes, e.g. nitrate and sulphate

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metabolism. 47'48 In practice, the physiological q~ of several C4 and C s plants under experimental conditions was identical at 30°C (4) = 0.0524 + or -- 0.0014 and 0-0534 + or -- 0.0009 respectively) though 4~ of C3 plants is negatively correlated with temperature due to photorespiration. 4s Below 30°C, 4~ was higher in the C3 species, but above 30°C the converse was true. This is because, above this point, the energy consumed by photorespiration in C3 species is greater than that consumed by C4 species in operating their additional C4 photosynthetic dicarboxylate cycle, which serves to concentrate CO2 and eliminate photorespiration. 4s The temperature at which this cross-over occurs varies, depending on the type of C4 metabolism. 46 Maximum efficiencies of conversion into biomass are observed only during short periods of the growth cycle when other growth factors are not limiting, and light interception is 100% (Table 2). In some instances this efficiency exceeds 6% PAR, but as maintenance respiration will increase linearly with biomass, this respiratory c o m p o n e n t is probably much less than 25% gross photosynthesis during periods of rapid growth. Otherwise, it is interesting to note the close agreement between the predicted and measured m a x i m u m conversion efficiencies observed for some C4 and C3 crops, a clear indication that crop plants are already adapted to exploit their photosynthetic potential when other factors are non-limiting. That they are never realized in practice relates to the environment, assimilate partitioning, genetic limitations and agricultural practice. Environmental influence Levels of solar radiation are well defined for most latitudes throughout the year. Extremes of temperature and lack of water may reduce or prevent photosynthesis in spite of the presence of adequate light. The outcome is well defined growing seasons, outside the humid tropics, which are often associated with photoperiod. Even within the growing seasons, nutrient deficiency or mineral toxicity (sometimes expressed through salinity), extremes of pH and pollution frequently reduce potential photosynthesis and efficiency of conversion of light energy into biomass. Light

Monteith 49 has estimated that record levels of biomass production of the major agricultural crops of the UK represent between 37-49% of

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the visible light energy (X = 0.4-0.7 lam) intercepted, assuming 100% for the actual light intercepted through the year. The length of the growing season is therefore the, determinant of the maximum biomass gain. Only the PAR intercepted by the chlorophyll is available for biomass production however, and this does not necessarily equate to that incident above the crop. s° Thus during the early part of the growing season, interception is closely related to the available leaf area: PAR falling on the soil will not be absorbed by the photosynthetic apparatus, sl Losses of potential biomass production will also occur towards the end of the growing season as the photosynthetic activity of senescing leaves declines. Taken together, a large proportion (e.g. 86%) of total biomass production may be produced in a short part (e.g. 44%) of the growing period, s2 Even during periods of full crop cover, when maximum crop growth rates (C = biomass per unit area and time or g m -2 s-1) are sustained, the effects of mutual shading of leaves ensures a continued increase in biomass production with increase in PAR. This response will be more marked the greater the proportion of light limited : light saturated leaves. Temperature

All photosynthetic reactions, with the exception of primary photochemistry, are thermochemical, being dependent on the probability of collision between reactant molecules. As temperature (T) is a direct expression of the kinetic energy of these molecules photosynthesis will, in theory, increase with T. In practice net CO2 assimilation (A) will also be determined by respiratory losses of C which are also a function of temperature, the effects of temperature extremes which are imparted both directly and indirectly on photosynthetic components, and the interactions with other variables. The resultant shape of the response curve between A and T is bell-shaped and characterized by a high and low temperature compensation point and an optimum temperature. Differences in biomass production correlate with this response particularly when the temperature environment is the major limiting factor to growth, s3 The solubility of CO2 relative to 02 decreases with increase in temperature. Since photorespiration increases with the ratio of O2/CO2, one effect of increase in temperature is increase in photorespiration, sa In general, C4 species have higher o p t i m u m and compensation temperatures than C3 species from similar habitats. C4 plants are susceptible to low temperature stress, 54 conversely Ca plants, particularly those from cool environments, are susceptible to high temperature stress. Chilling-

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tolerant species will only remain photosynthetically active, however, as long as the cells are not frozen, ss Similarly, temperature extremes above and below the high and low temperature compensation points respectively may cause irreversible damage to the photosynthetic mechanism. The underlying mechanisms which determine the shape of the temperature response curve o f photosynthesis include the relationship between photosynthesis and photorespiration, the temperature related chemical properties of enzymes and perhaps stomatal limitations, s6 As temperature is not an environmental factor which can be controlled in the field, biomass production will be determined by diurnal and seasonal changes of T acting in concert with other limiting factors. Biomass production will be more seriously affected if temperature extremes cause irreversible damage or injury to the photosynthetic system, as potential productivity cannot then be realized even on return to o p t i m u m growth conditions. Water Water is fundamental to photosynthesis as a reactant, as a milieu for biochemical reactions, and for its passive role in transpiration. The availability and utilization o f water are therefore major factors influencing biomass production even in temperate or humid climates. Periods of drought are well k n o w n for their devastating repercussions on production in arid and semi-arid zones as are extreme cases of water surfeit which limit the ability of roots to take up water through development of anoxic soil conditions. The quantity o f water required for water splitting in photosynthesis is between 2 and 3 orders of magnitude less than that required for transpiration. Nevertheless, photosynthetic CO2 assimilation (A) declines under water stress and may cease completely should severe water deficits develop. Leaf area expansion, and therefore the production of new photosynthetic area, ceases because of low turgor pressures s7 and the diversion of p h o t o s y n t h a t e from loading sites in the phloem to osmoregulation :8 To obtain CO2 for photosynthesis, leaves expose wet surfaces, i.e. the cell walls of the substomatal cavity, to the atmosphere, and evaporative water loss occurs as a result. This is an inevitable prerequisite for obtaining CO 2 for photosynthesis, but also essential for evaporative cooling and the maintenance of equable leaf temperatures. 3° Net photosynthesis and biomass production will slow down or cease if the leaf

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temperature approaches or exceeds the high temperature compensation point, respectively, under water stress conditions. Each major resistance in the diffusion pathway of CO2 from the atmosphere to the sites of carboxylation within the mesophyll may increase with water stress: 9 The curling of leaves increases r a. Loss of turgor in the guard cells leads to stomatal closure whilst increased ABA levels under water stress inhibit stomatal opening and this may persist several days b e y o n d the return of the plant to high water potential. The decline in A under water stress may be caused by rate limitation at the stomatal and mesophyll level 6°'61 though A may be ultimately limited by p h o t o p h o s p h o r y l a t i o n under severe water stress. 6z The loss of biomass production through the reduction in A during periods of water stress is difficult to quantify. Stress periods differ in length and intensity both in different environments and in different seasons, and may coincide with different growth stages which vary in their sensitivity to water stress. Since there is much evidence to suggest that leaf area development and biomass production is correlated with transpiration and water use, even mild water stress would cause a reduction in productivity. 63' 64 The accumulation of biomass can be summarized in terms of three processes: 6S total biomass production

=

light intercepted

X

efficiency of photosynthesis

X

fraction remaining after respiration

Ill a comparison of unirrigated and irrigated H o r d e u m s a t i v u m , the major factor which decreased biomass production in the unirrigated crop was a 40% reduction in photosynthetic leaf area and a shortened growing season. 65 In the same experiment, the estimated effect of decreased stomatal conductance on the unirrigated plants was a 7% lower A than in the irrigated plants. 66 The major effect of water stress is therefore a significant reduction in total light interception, at least in determinate crops. In many crops, the economic yield (or harvest index HI) is only a part of the total biomass production and the effects of stress on HI are usually less than on total biomass production, as translocation of reserves already present may help to maintain the harvestable product. F o r example, McPherson and Boyer 67 subjected Z e a m a y s to a continuous period of water stress between tasselling and harvest. Although A was approximately zero throughout this period, grain yield

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was 47-67% of controls. The reduction in current photosynthate supply during periods of stress is, at least in part, counteracted by the mobilization of storage compounds. This emphasizes the importance of integrated photosynthetic accumulation as a determinant of economic yield as well as for maximizing total biomass. N u tri e n ts

Deficiencies of nearly all the essential nutrients reduce A, since many including metals and trace elements are incorporated into components of the light (P, Mg, Fe, Cu, S, Mn) and dark (P, Mg) reactions.59' 68, 69, 70 It is nitrogen (N) which has the most profound effect on photosynthesis and biomass production, as most forms are soluble and easily leached. Nitrogen is the basic constituent of amino acids, and as the production of protein is directly proportional to the availability of N, this element plays an important role in biomass production. 71 Nitrogen is a component of chlorophyll, the intermediates of the electron transport chain, the enzymes and metabolite transfer components of the Ca/C4/ CAM reactions and of photorespiratory carbon transformations. Deficiencies of N often result in lower levels of photosynthetic enzymes, in particular the primary carboxylase, ribulose-1, 5-bisphosphate carboxylase/oxygenase.72 Nitrogen and other nutrients are also essential for the normal development of the photosynthetic canopy.7a Indeed application of N to plants can lead to dramatic increases in leaf area. Nitrogen is thus of obvious importance to biomass production at two levels: light interception and the efficiency of carbon fixation through the light and dark reactions. Biomass production can also be lost through the effects of nutrient toxicity. An increasingly important area in this respect is the effect of salinity in the environment. Saline soils, typically dominated by NaC1 and Na2SO4 have an electrolyte concentration which is inhibitory to the growth of plants. Natural saline soils excluding the hot deserts occupy 4 X 106 km 2. In addition, secondary salinization is continually adding to this total through irrigation and drainage practices, an example of shortterm attempts to increase biomass production leading to long-term net losses of biomass production. At a conservative estimate 400 km 2 of formerly productive land is lost annually by secondary salinization. 74 The deleterious symptoms observed in plants at critical salt concentrations are the result of a complex series of interactions and there is no p r i m a facie case for expecting a single lesion 7s or that photosynthesis

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is necessarily a primary site of action. Salinity at sublethal levels reduces biomass production both by reducing leaf area, the rate of CO2 assimilation (A) and maintenance respiration) 6 The question of which one of these factors is the more important in determining canopy photosynthesis cannot be answered from existing information. As with water stress, the decline in A is the result of both stomatal closure and disruption of the chloroplasts with increase in salinity. There is also evidence that salinity decreases biomass production through increased respiration) 7 Pollu tio n

The presence o f gaseous pollutants in the atmosphere, in particular SO2, the nitrogen oxides (NOx) and 03 have combined to produce quite significant losses of biomass production, in some instances at sites quite remote from the source of the pollutant gas. Sulphur dioxide (SO2) is the most abundant S-containing pollutant. It is a b y p r o d u c t of fossil fuel consumption, and in the industrial countries of the world moderate concentrations of 2 0 - 5 0 ~g kg -1 occur over large areas o f l a n d ) 8 SO2 pollution is supplemented by particulate SO4, acid rain and H2S. There appears to be a threshold level of SO2 concentration below which no damage occurs. To some extent this threshold is a function of the sulphur status of the soil above which biomass losses will occur. Much of the information concerning the effects of SO2 on photosynthetic CO2 assimilation (A) and biomass production appears contradictory and inconsistent, as earlier studies into the effects of SO2 on photosynthetic CO2 assimilation (A) used unrealistic concentrations of the pollutant which greatly exceeded levels of exposure in the field. There is, however, considerable evidence to suggest that A and ultimately biomass production are inhibited by SO2 fumigation, despite an increase in stomatal conductance. Unlike CO2, the mesophyll may be a near infinite sink for SO2, since gaseous concentrations of SO 2 in the substomatal cavities can be close to zero even during periods of rapid SO 2 u p t a k e ) 9 Once in the chloroplast, the effects on the light reactions are often qualitatively similar to those associated with water and temperature stress. The oxides of N are also combustion products of fossil fuels. Changes in stomatal conductance are observed but the effects of NOx on A are thought to occur principally through absorption of NO~ by the meso-

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phyll. It is possible that saturation of nitrite reductase causes a build-up of toxic levels of nitrite, s° Ozone (03) is important in areas of high temperature and irradiance since both are required for significant photochemical formation of 03 from its precursors. This reactive molecule with two unpaired electrons can form hydroxyl, superoxide and other free radicals.81 As a result, the primary effect of 03 is thought to be damage to cell membranes, in this instance thylakoid membranes and stromal lameUae, as both photosystems and R u b i s C O activity are inhibited. Stomata are probably the major pathway for the entry of 03 into plants, but it is not yet clear whether the flux, and therefore the degree of injury, is proportional to stomatal conductance,s2 The precise effects of atmospheric pollutants on photosynthesis and biomass production have still to be quantified. In general, one would expect this to be related to the duration of exposure and concentration of pollutant stress, or alternatively the rate of uptake of pollutant. The susceptibility of plants to photosynthetic damage, however, appears to be a function of the stage of plant development as well as soil and climatic factors. As polluted air may contain several gaseous pollutants, it may be difficult to isolate the individual effect of any one pollutant. Further information is not only required at realistic atmospheric levels of pollutants but should also account for additive and synergistic reactions in the presence of more than one pollutant. A number of studies have shown that the uptake and accumulation of heavy metals, viz. Cd, Ni, Pb, T1, Zn, Co and A1 inhibit photosynthesis and biomass production. Stomatal closure may also be a secondary influence of heavy metal toxicity, the primary sites of action being at chloroplast level in the light and dark reactions,s3 As heavy metals are often present as mixed contaminants, additive or synergistic effects may be anticipated. UV (k = 0.25-0.44#m) is subdivided into three wavebands. The middle waveband (UV-B, k = 0.28-0.32 tam) is present in solar radiation at the earth's surface and causes biological damage. Of concern at present is the possibility that the stratospheric 03 layer is being depleted because of industrial emissions. As UV-B is the component of UV most sensitive to any change in the thickness of the 03 layer, enhanced levels will increase biological damage,s4 Action spectra suggest that the major receptor sites for UV-B include both nucleic acids and proteins but photosynthesis is also affected at the levels of photochemistry, electron

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transport, photophosphorylation and carboxylation. These observations suggest that the disruption of the thylakoid membrane and stromal lamellae may be ultimately responsible for UV-B induced reduction in CO2 assimilation. Assimilate partitioning

It is to be expected that production of substances in photosynthesis will be closely linked to the requirement for those substances, particularly in organisms as complex as higher plants. By way of illustration, it is well known that artificial manipulation of the size o f 'sources' (e.g. the removal of leaves), or the size o f 'sinks' (e.g. the removal of storage organs), affects A and that in general A increases with increase in the 'sink' to 'source' ratio. Further, the bulk of C assimilated by the chloroplasts is exported from the leaf in the form of sucrose, and in most leaves this export does not keep pace with A during daylight hours. This imbalance, manifested in the formation of starch in the chloroplasts, reduces A and is greater under conditions where translocation is inhibited, e.g. a reduced 'sink size', or under environmental stress. This interaction between photosynthesis and the demand for p h o t o s y n t h a t e means that biomass production may not reflect photosynthetic potential, and therefore represents a loss of conversion efficiency to biomass. As yet the mechanisms which regulate Pn through assimilate levels, and/or the demand for assimilate, remain uncertain, ss Conclusion to part 2 Biomass production is ultimately determined by the flux of PAR incident on the plant canopy. Does the conversion efficiency with which the process converts PAR to biomass ultimately determine production? Data accumulated from a limited number of c r o p plants suggest that the answer is probably no. Photosynthesis has already evolved in such a way that, thermodynamically, the photochemical efficiency of the process is apparently at or near its maximum. Thus when photosynthesis is light limited and the photosynthetic apparatus is functioning normally (i.e. not under stress), and when account is taken of respiratory losses of C, the conversion efficiency of light (PAR) to biomass is about 3% of solar energy or ca. 2.0 g biomass MJ -1 of solar energy (the energy equivalent of carbohydrate is 477 kJ mole-it. A figure c o m m o n l y observed for temperate crops growing under

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optimum conditions over a wide range of latitudes is 1.5 g biomass Mj-l,s0, a6, 87 ignoring production of non-storage roots. Canopy photosynthesis is also limited by determinants which do not involve the process itself but nevertheless reduce its conversion efficiency. Genetic size limitations have arisen from breeding programmes on crop plants where harvest index rather than total biomass yield has been emphasized. Similarly row width and direction are determined for maximizing economic yield, and often result in loss of conversion efficiency of PAR into biomass. These are unavoidable losses in the context of agriculture. Conversely, losses from poor soil fertility, poor husbandry, pests and diseases are potentially avoidable. These usually result in considerable reductions in leaf area. In this context, the use of pesticides and fertilizers has led to considerable increases in biomass production and economic yield. Further discussion of these limitations which indirectly limit photosynthesis is outside the context of this review. Considerable increases in production are possible by alleviating these problems. The question that remains is can A be increased by improving the actual ability of plants to fix CO2 and improving the tolerance of the process to environmental extremes, thereby reducing irreversible losses of biomass production?

3. IMPROVING CANOPY PHOTOSYNTHESIS Canopy photosynthesis can be increased at the level of both CO2 assimilation per unit of leaf area (A) and/or total leaf area (L). Maximizing conversion efficiency of solar energy into biomass is therefore a question of realizing the potential of both light harvesting and CO2 reduction in photosynthesis, and exploiting this potential to the full. Ligh t reactions

The similarity of 4~within Ca plants when photorespiration is suppressed and within C4 species is consistent with a theoretical explanation that 4) should be similar among plants that use identical photosynthetic mechanisms in a physico-chemical process which is independent of T. as It would also seem that the mechanism of light energy conversion into chemical energy is already close to the practical maximum upper limit. 26 There is some evidence that ~ may be significantly higher in

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some C4 sub-types than in others 46 and in C4 species which have adapted to low light or low temperature environments. 54'89 Otherwise there is remarkable constancy of q~'throughout species of higher plants. The efficiency of the light reactions may be a relatively conservative property of green plants and n o t subject to easy manipulation. Little is known o f any direct relationship between the productivity and light reactions, and it is not obvious, in spite of detailed knowledge of these reactions, how they might be manipulated to increase biomass production. Obviously there can be no biomass without photochemistry, but in the field h o w frequently do the light reactions limit the rate of biomass production? Although individual leaves of most C3 plants are unable to utilize additional radiation above } full sunlight (N.B. C4 plants normally fail to saturate in full sunlight), this is not true of a photosynthetic canopy where shading ensures a continued increase in biomass accumulation with increase in amount of light. Thus light is usually limiting to biomass production in an established crop. However it is not clear whether this is in any way due to the photochemical production of NADPH + ATP. There is considerable between-species variation in the photosynthetic capacities of C3 and C4 plants. For example, the maximum rate of CO2 assimilation (Amax) of C4 grasses varies from 1.4-2.9 mg m -2 s-l. 90'91 Although their functional basis is not clear, these differences almost certainly originate in the chloroplast and may be linked to photochemical processes. As some plants are seemingly able to utilize their supply of PAR to better advantage than others, this may in some way be linked to constraints in the design of their photochemical apparatus. 92 In this respect Leverenz and Jarvis 93 have suggested that the convexity of the light response curve of a species may be related to its productivity. This convexity should increase when the chloroplasts are more evenly illuminated and this was observed under bilateral, compared to unilateral, illumination. If within species variation in the convexity of the response curve can be detected, this may form a basis for selection at the level of light absorption. Dark reactions

In theory, the process of electron capture is fundamental to productivity. In practice, it is the subsequent utilization of the energy of the captured photons, after conversion to energy rich compounds, i.e.

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NADPH and ATP, which probably determines productivity. To some extent therefore, the amount of energy plants invest in the synthesis of the photochemical c o m p o n e n t s o f photosynthesis should be determined by the maximum demand for energy and reducing p o w e r in the dark reactions and for p h o t o s y n t h a t e for growth. In this sense a distinction is made between improving the efficiency of the light reactions per se, and more efficient use of its products (NADPH/ATP) in the dark reactions. The light and dark reactions should not be considered in isolation, however. In recent years, several connections have become apparent. F o r example, cyclic electron flow is reputed to be particularly active and important during the induction o f photosynthesis from a darkened state by contributing additional ATP to phosphorylate carbon cycle intermediates and light-harvesting chlorophyll-protein (LHCP). This may set in motion the autocatalysis responsible for the attainment o f high rates o f photosynthetic CO2 assimilation. 94 The light driven exchange o f Mg 2+ and H + between the thylakoid inner space and stroma, and the reduction of thioredoxin via ferredoxin have been shown to have a strong influence on the activity of certain key enzymes, notably fructose bisphosphatase (FbPase) and sedoheptulose bisphosphatase (SbPase). 94-97 Thus when a leaf is illuminated after a period in the dark, the increase in A shows a lag of 30 s-3 min followed by a rise over 3 - 3 0 rain before the maximum A and maximum efficiency of light energy conversion is reached. 98 It is the early phase of this lag which probably represents the time taken for the activation of some enzymes o f carbon metabolism through the events of the light reactions, and the subsequent rise the time taken for autocatalysis within the RPP-cycle to raise the level of intermediates, in particular RubP, the primary acceptor of CO2, to a maximum. The maintenance of steady-state assimilation of C must necessarily balance the regeneration of RubP from assimilated C against the loss o f C to other metabolic pathways, a balance point which is reached when A reaches a maximum and remains constant. Dark-light transitions may seem of little direct relevance to the field situation where changes in solar radiation on clear or overcast days are gradual. The speed with which a leaf can optimize its photosynthetic apparatus to sudden changes in light levels, e.g. as a cloud crosses the sun, will, however, have a direct influence on production, but its significance awaits further study.

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The a m o u n t of active e n z y m e as well as the amount of substrate must influence COa assimilation (A). FbPase and SbPase, which are considered to have an important regulatory role, have activities more than adequate to account for measured rates of A.99 Similarly R u b i s C O is often suggested to be in abundant supply, representing ca. 50% of the soluble protein in the chloroplast, at least in C3 plants) °° A number of studies have shown a good correlation between R u b i s C O activity and m a x i m u m A, e.g. Randall et al., ~°~ but this has not been linked to biomass production. Nevertheless, the RPP reactions partially limit photosynthesis, independent of its enzyme complement and of the supply of NADPH and ATP from the light reactions. This is supported by observations that substrate levels, particularly RubP, may be only just sufficient under optimized conditions to determine the m a x i m u m rates of CO2 assimilation which are observed. 1°2 Secondly, the rate of CO 2 assimilation in single leaves of C3 plants and biomass production can be increased by increasing ambient CO2 concentration (Ca). Thirdly, the dark reactions can limit the rate of CO2 assimilation through photorespiration except in C4 and perhaps CAM plants. The absence of photorespiration in C4 plants has two important consequences for production. First, since C4 plants do not photorespire, they can decrease internal CO2 concentrations (Ci) to almost zero, and thus maintain a greater internal air space to atmosphere concentration gradient than can C3 plants. Second, the presence of a photosynthetic bundle sheath surrounded by a photosynthetic mesophyll ef%ctively concentrates ('02 around the sites of fixation. In spite of similar 4~ therefore, A of Ca plants does not light-saturate over the natural range of light levels, and shows higher conversion efficiencies of PAR at high light levels, viz. 1000-2000/amol m -2 s-1. In C3 plants the lowered Ci favours photorespiration, and this explains why C3 plants respond well to increases in Ca. In theory therefore, the productivity of C3 crops would be increased by inhibiting photorespiration. One technique which has proved successful is increase in Ca to a level where RubP oxygenation is inhibited; this is now used on a large scale in the greenhouse culture of L y c o p e r s i c o n e s c u l e n t u m (tomatoes) where it can result in a 50% increase in yield) °3 Similar increases have been reported for Triticum aestivum grown in high Ca. 39 Application of elevated CO2 concentration effects are not practical on a field scale. Chemical inhibition of glycollate metabolism at ambient Ca has also

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been shown to inhibit photorespiration and increase A in short-term experiments.1~ This approach can only be successful, however, if glycollate metabolism is not essential to the functioning of the green cell. Some evidence suggests that it is: photorespiration may be a regulatory mechanism for the removal of excess photoreductant from the chloroplast under conditions where C02 is not available as the terminal electron acceptor, l°s Alternatively, it may have arisen as an accident because RubisCO catalyses an oxygenation reaction which results in formation of glycollate. Photorespiration could then be seen as a metabolic cycle which retrieves part of the C lost from the RPPcycle through oxygenation of RubP. If accidental, it may be possible to reduce photorespiration without adversely affecting the photosynthetic apparatus, thereby increasing biomass production. It has been suggested from a theoretical viewpoint that the relative affinities of RubisCO for CO2 and 02 could be altered. 1°6 However, since years of selection in natural environments where photorespiration is prominent have failed to do this in C3 plants, the practical prospects of this seem poor at present. Nor was hybridization of Atriplex species possessing the C3 and C4 pathways of photosynthesis successful: A of both F1 and F2 hybrids was less than that of both parentsJ °7 The genetic constraints associated with the C4 leaf anatomy make it apparently impossible to impart the properties of compartmentation of photosynthesis, essential to C4 photosynthesis and suppression of photorespiration, into C3 plants, l°s The significance of the continuing increase of atmospheric CO2 concentration (Ca) from the combustion of fossil fuels on photosynthesis, biomass production and the weather has become an intriguing problem. It is possible that Ca remained at 270 vpm for a considerable period as a result of a balance between photosynthesis and respiration which prevented depletion below this level.1°9 Since the start of significant levels of fossil fuel-related emissions of CO2 in the 19th century, Ca has increased approximately 70 vpm to its present level of 340 vpm and continues to increase at approximately 1-2 vpm per year. 1~° Little attempt has been made however to put A and biomass production in the context of a high CO2 environment. One estimate suggests that A has increased 3.1% since the beginning of this century H~ and that increases in biomass production will also occur as a result of increased water-use efficiency. Except under optimum growth conditions,

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however, e.g. high input agriculture, biomass production may remain primarily limited by water and nutrients. Increased Ca may change species balance in favour of C3 plants where C3 and Ca plants are present in the same environment, as high levels of Ca will have a negligible effect on A and biomass production of C4 plants. (It should be remembered that increased C~ may have profound consequences on the earth's climate. If temperature and rainfall patterns change as a result, these will in themselves influence the production and distribution of C3 and C4 plants. Some of the above conclusions therefore, can only be speculative.) Adaptation of environment

The ability of plants to adapt to prevailing light conditions is a basic growth response, though shade plants by definition grow only at low light fluxes and are incapable of sustaining photosynthesis in a high light flux. To meet this response, plants integrate and adjust several partial processes to maximize CO 2 gain (A) to the available light, but with the constraint that a high photosynthetic efficiency of light utilization at one extreme precludes a high efficiency at the other, x12 For example, if leaves become shaded subsequent to their development or develop in other than high light conditions, the concentration of the components of the electron transport chain and the activity of enzymes will be correlated with the lowered photosynthetic activity. Conversely, plants invest in more LHCP and antennae chlorophyll per unit area at low light flux to maximize their ability to harvest the available light, but have more reaction centre chlorophylls and a higher concentration of carboxylating enzymes under high light conditions. As plants are able to adjust to abrupt changes in ambient light within days in controlled environments, they already have considerable potential to adjust to the less abrupt changes in light which occur naturally. Similarly, plants have the same capacity to acclimate to change in ambient temperature as to their optimum temperature, for photosynthesis will adapt within a few days following the transfer of plants from one temperature to another by 1-3°C for every 5°C change in growth temperature.~3'114 Close correlations between the optimum temperature for photosynthesis and the mean maximum temperature of the ten days prior to measurement have been observed. 1is Such adaptations of the temperature response curve to prevailing temperature will

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also have a role in plant survival, as any accompanying raising or lowering o f the high and low temperature compensation points, respectively, will delay the onset o f irreversible effects o f temperature stress and loss of biomass production. It is therefore at the temperature extremes that most benefit to biomass production will be gained from studying the basis of temperature adaptation. Analysis of temperature lesions has been more frequently studied in vitro and it is possible that partial photosynthetic processes are less temperature sensitive in vivo in the intact system. There is, however, good reason to suppose that the irreversible decline in light-saturated photosynthesis under heat stress may be photosynthetic in origin, and related to the lipid properties of the membranes which support photosynthetic electron transport, s3'116 Thus as the strength of hydrophobic bonds increase and the strength of hydrophilic bonds decrease at high temperature, the distance between the LHCP, antennae and the reaction centre chlorophylls increases and disrupts chloroplast function, s6'117 Within species, differences in membrane stability may therefore be a basis for selection for high temperature tolerance. The deleterious effects o f low temperature differ in detail from those at high temperature and include phase separation of gelled from the remaining liquid components o f the thylakoid membrane and stromal lamellae, and disruption of photosynthetic electron transport. 118 This loss of fluidity o f the membrane is to some extent correlated with its fatty acid composition, and the temperature at which phase separation occurs is positively correlated with the ratio of saturated :unsaturated fatty acids. 119 As acclimation to chilling temperature is associated with an increase in this rati@ 2° increasing the capacity for this change will increase the low temperature tolerance of the photosynthetic process. As well as disruption of electron transport, 121'122 the activities of enzymes o f carbon metabolism and particularly of C4 carbon metabolism decline at low temperature and limit A.54 This change in activity is often expressed as a marked increase in activation energy (AE) at a particular temperature, suggesting a change in tertiary structure. 123 As the rate of low temperature inactivation can differ according to the species from which the e n z y m e is extracted and since differences in the cold lability o f an enzyme can be related to the temperature limits of cultivars within a species, 124'12s the activation energy o f enzymes may therefore form a basis for selection of low temperature tolerance of photosynthesis.

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Caldwell e t al. 126 have proposed that C4 plants which decarboxylate through NADP-linked malic enzyme are less cold tolerant than those plants which utilize NAD-malic enzyme. This has not been further substantiated but it has been suggested that the spread of some PEPcarboxykinase species into high latitudes may relate to their ability to generate PEP directly during decarboxylation and thereby bypass the cold-labile enzyme steps of C4 photosynthesis. 54 Plants may make considerable adjustments of both stomatal and mesophyll conductances to avoid low internal CO2 concentrations. 61' 127 Otherwise, photoinhibition of photosynthesis may be caused either by the presence of excess light energy which cannot be used for electron transport or the presence of excess reductant which is not required for CO2 reduction, which may result when C i is low. In particular, 0 2 may act as an electron acceptor producing superoxide. Superoxide may then be converted to hydrogen peroxide by a dismutation reaction. Hydrogen peroxide is toxic to CO2 assimilation but in the presence of superoxide may give rise to the extremely reactive hydroxyl free radical (-OH). This radical is extremely destructive to photosynthetic membranes and may cause photoinhibition, probably through an effect in or near to the PS II reaction centre. 128' lZ9 Chloroplasts have protective mechanisms for avoiding photoinhibition. For example, secondary pigment molecules including the carotenoids and o~-tocopherol (vitamin E) may assume the role of a sink for the degradation of excess energy which cannot be used for electron transport) 3° Secondly, high levels o f superoxide dismutases (SODs) and peroxidases will detoxify damaging derivatives of oxygen reduction, and large quantities o f ascorbate and glutathione will remove .OH. 131-133 As synthesis of these detoxification agents is crucial to the protection of chlorophyll-protein complexes during periods of stress, any variation in the capacity of species or varieties to produce these colnpounds could be exploited to improve stress tolerance. It is interesting to note that photorespiration may have a role in this respect by recycling ( ' 0 2 to dissipate the excess photochemical energy present when the supply of terminal electron acceptors is reduced under stress conditions. Indeed, photoinhibition in P h a s e o l u s v u t g a r i s (C3) was increased when photorespiration was suppressed by a decrease in O2 content of the air to 1%. A similar role has been proposed for metabolite transfer and CO2 recycling in C4 plants, and the recycling of CO 2 fixed in the dark in CAM plants. 134

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As biomass production is proportional to water use, it would appear that WUE is a constant for a species in a given environment.6s Maximum biomass production will only be realized, therefore, by supplying sufficient water to realize potential leaf area and meet evaporative demand during growth. This can only be achieved where water is available for irrigation. Alternatively real increases in WUE through higher CO2 uptake per unit of water transpired may be a characteristic of some varieties, which can relieve the deleterious effects of water stress on production. CAM is an extreme example of photosynthetic adaptation to high WUE. In these species however, the characteristic is for survival rather than efficient photosynthesis. These species may have a role to play in improving biomass production in hot and arid regions. Similarly, nutrient stress can only be relieved by the application of fertilizers or by the use of varieties which provide an economic yield in soils of low nutrient status. As fertilizers are expensive in real terms, much effort is now expended researching the microbial genetics of nif (N-fixation) genes} 3s Biological N-fixation worldwide remains the major source of inorganic N for plants and of particular interest are the Leguminosae which include several important crops. N-fixation requires energy for the uptake, reduction, interconversion and incorporation of N into carbon skeletons which exceed that required for the incorporation of NOa- and NH~ into organic compounds. Carbohydrate is however required for the growth and respiration of the microorganism. In the Leguminosae as much as 32% of the total photosynthate may be translocated to the nodules, la6 In spite of the lower efficiency of conversion of C into fixed N, the growth of legumes is not limited by high energy requirements as long as sufficient photosynthate is available. 137 Under field conditions however, the reduction of N may be limited by photosynthate supply, particularly during the reproductive phase of growth. The diversion of this large portion of energy into N-fixation in leguminous crops results in a very low conversion efficiency as a result (e.g. G l y c i n e m a x , Table 2). As photosynthesis is ultimately a source of energy, reducing power and carbon skeletons, it may not make sense to divert C away from biomass production by incorporating symbiotic N-fixation into nonleguminous plants. Conversely, there may be a better case for exploiting free-living organisms which can fix N and obtain C from other sources (e.g. organic wastes or root exudates), for mycorrhiza to improve nutrient uptake and the replacement of fertilizers by manures. Alter-

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natively, improving N-use efficiency p e r se may be possible; typically, C4 species may show an N-use efficiency about double that of C3 species) 38 The potential for saline soils could be enhanced by exploring the potential of the available halophytic flora as potential crops. 139 Many halophytic shrub and tree species may be suitable for fuelwood crops and selected cultivars of H o r d e u m sativurn have been shown to survive salinities up to 300 mM .140, a41 The problem arising from photosynthetic damage by pollutants differs from those of other environmental variables, since we have the means to control the cause of photosynthetic inefficiency. Strict emission controls would be the most obvious procedure, but if their presence in the environment is to be long-term, varieties which are resistant to their presence will have to be selected. Plants already differ in their response to UV-B. Some acclimate to prevailing levels of UV-B by synthesizing flavenoids in their epidermal cells to absorb UV-B, thereby screening the underlying photosynthetic tissues: in others alkaloids fulfil this function. 142-144 L e a r area

The size of the photosynthetic canopy is determined by the leaf area index (LAD, if no particular arrangement of the leaves is assumed. The persistence of LAI with time (t) is termed the leaf area duration (LAD). Thus if LAI and LAD are maximized, in theory so will be the interception of incident light. As there is a strong correlation between biomass production and interception, the distribution of p h o t o s y n t h a t e between storage or the production of new leaves will determine seasonal changes in photosynthesis and biomass production. This is particularly the case during the early part of the growing season, after defoliation or in y o u n g vegetation, when L is zero or very small. In order to maximize yield, p h o t o s y n t h a t e should be used at this stage for the production of new photosynthetic surface. This investment in LAI not only results in a rapid increase in photosynthesis p e r se, but as new sinks are created for the products of photosynthesis, A may increase CO2 assimilation by a feedback mechanism. 3° The result will be that 100% light interception will be achieved at an earlier stage in the growth of the crop, and higher production will result. After 100% light interception, the preferred partitioning of photosynthate may be determined by the harvest index. A switch from

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vegetative to reproductive growth will also cause changes in assimilate partitioning. These are often accompanied by changes in photosynthesis and LAI. 21 Most plants remain in the vegetative state for a period after canopy closure however, and since the total accumulation of biomass is often a determinant o f economic yield as well as biomass yield even in determinate crops, efficient interception remains essential. This is determined by the vertical distribution of leaf area, a function of plant height and the distribution of leaf inclination. The distribution of leaf azimuth angle may also be important. Ideally leaves should be horizontal until 100% light interception has been reached. After canopy closure, self shading between leaves reduces both A and the capacity of individual leaves since several may develop and photosynthesize in a restricted light environment. Considerable attention has therefore been given to manipulating the structure o f the photosynthetic canopy to share more effectively the light available among the leaves and to improve the conversion efficiency. This is predicted to have a positive effect on biomass production where LAI is high, i.e. > 4.14s F o r many types of vegetation, the phenology may seem qualitatively obvious, viz. erectophile (erect-leaved) or planophile (horizontal-leaved) but closer inspection reveals that leaf inclination is not a constant property o f plants but may change irreversibly with age as well as being correlated with leaf size) 46 In model canopies, the ideotype 14v dictates that the upper leaves should be erectophile grading to a planophile distribution at the base for efficient light interception and improved biomass production. Graminaceous species have an erectophile growth habit and are grown at high densities for efficient light interception. Selection within this important family for erect leaves has two proposed advantages: a high planting density can be used to increase light interception early in the season and a higher LAI can be maintained during the period of full crop cover. With few exceptions the theory has not been borne out by the results. As C3 cereals are grown at higher densities, have higher LAIs and show saturation of CO 2 assimilation by individual leaves at lower p h o t o n fluxes than C4 cereals like Zea mays and Penniseturn typhoides, the advantage of erect leaved cultivars should be more noticeable in C3 species. 49' 14s, 149 In percentage terms, the more erect-leaved cultivars within a species have a higher crop growth rate but not necessarily a higher economic yield. One exception is grain yield of Oryza

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sativa where the advantages of erect leaves have contributed to the

successful development of the c r o p ) s°'lsl With the other major C a cereals, T r i t i c u m a e s t i v u m , H o r d e u m s a t i v u m and A v e n a s a t i v a , it may be that in spite o f consistently higher levels of crop growth throughout the season in the erectophile cultivars, 152'153 greater translocation of stored materials from the stems of the lax-leaved cultivars results in similar grain yields, ls4 Alternatively, the higher densities permitted by erect leaves may in some way affect the pattern of plant development. The advantage of erect-leaved cultivars should be greater where the harvest index is high and thus the economic yield represents most of the total biomass production, e.g. forage grasses under frequent cutting regimes. However, crop growth rate and canopy photosynthesis varied little in three forage grasses of contrasting structure. 155' ls6 As exploitation of leaf angle has little effect on biomass production, it has been suggested that leaf rigidity, number of tillers per plant, leaf size and tiller angle may be more important determinants of canopy structure and biomass production, sl' ~s7 Predicting the effects on biomass production is clearly complex, as in quantitative terms each varies with species and the o p t i m u m arrangement varies with stage of growthJ s8 In practice therefore, differences in leaf angle and related chracteristics are of lesser significance to biomass production than the rate at which the canopy expands to form and then maintain a complete ground cover for the expression of photosynthetic potential and maximum biomass p r o d u c t i o n ) s9, 16o

Conclusions to part 3 The increase in harvest index has contributed to the improvement of economic yield, particularly in cereal crops, though total biomass production has remained constant in these crops. 161 The point may be being approached, however, where more and more effort will be required to increase harvest index for decreasing gains. As the ultimate potential is set by photosynthetic CO2 assimilation, it is remarkable that as yet little attention has been given to the possibility of increasing total biomass production through increased and more efficient photosynthesis. Improvement of canopy photosynthesis through both improved individual leaf rates of CO 2 assimilation (A) and a larger and more

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persistent canopy (L) will therefore be the necessary step in the longer term to meet the rising and presently unmet demand for plant products. As yet the detailed knowledge and understanding of the photosynthetic process, from the primary photochemical act up to assimilation of COs by individual leaves, has not to date resulted in any improvement in biomass production. If, as seems likely, the efficiency of photosynthesis at the molecular and cellular level apparently approaches the thermodynamic optimum, this is not surprising. Nevertheless, these partial processes ultimately determine photosynthetic efficiency and improved knowledge of their role may be essential, particularly if developments in recombinant DNA and other biotechnology are to be fully exploited in the field of photosynthesis. More immediate benefits to biomass production will be obtained from studies which elucidate how and why some plants are able to photosynthesize better than others in sub- and supra-optimal conditions. This, too, requires better understanding of the effects of these stresses on limitations within the photosynthetic apparatus, which are often manifested as an imbalance between the light harvested and the supply of final electron acceptors. Should this prove to be a common factor or primary result of stress on the photosynthetic apparatus, it would greatly simplify selection for stress tolerance regardless of cause of stress or combination of stress factors in the environment. Perhaps the most significant contribution that current knowledge of crop photosynthesis has made to biomass production has been the selection of rice varieties with a canopy architecture for improved light interception. Although this approach has been less rewarding for other crops, improved canopy architecture may lead to further improvements where biomass rather than the economic yield of one plant component is the selection criterion. For many cereals, the development of the grain is determined by the supply of photosynthate from only a portion of the assimilatory area, by ear photosynthesis itself, and by the supply of carbohydrates stored during growth pre-anthesis, particularly under stress conditions. These more complex growth patterns suggest that studies of canopy photosynthesis should be linked to the partitioning of photosynthate. Preferred patterns of translocation will be very much determined by the growth characteristics of the plant and the proportion harvested, and should resolve which constraints are preventing the expression of maximum conversion efficiency into biomass production or economic

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yield at any particular time during the growing season. A major factor in this respect is the rate of partitioning into new leaf area at the start of the growing season. CONCLUSIONS Renewed interest in biomass production stems from the dependence of the majority of the world's population for their well-being on the productivity of plants. The maximum biomass production of any ecosystem is constrained by complex interactions between various limiting factors which determine photosynthetic CO2 assimilation. 162 Much of the increased food production in the past and present has been achieved by the increased use o f non-renewable and energy intensive resources, deforestation (currently proceeding at the rate of 1 1 X 10 6 ha year-X) 163 to supply new agricultural land and the irrigation of marginal land. There is much evidence that the environment cannot sustain this approach for much longer, as the seeming potential for increased production is negated by competition for resources, subtle changes in climate, and pollution. Other means must therefore be sought to increase f o o d and other forms o f biomass production for foods, fibres and fuels. ACKNOWLEDGEMENTS The authors thank Ms Charmaine Coulston and Ms Rita Bartlett for their help in preparation of the manuscript.

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