JXB Advance Access published online on September 17, 2007
Journal of Experimental Botany, doi:10.1093/jxb/erm192
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© 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER |
Trends in leaf photosynthesis in historical rice varieties developed in the Philippines since 1966
1Division of Agricultural and Environmental Science, School of Biosciences, University of Nottingham, Sutton Bonington, Loughborough, Leicestershire LE12 5RD, UK
2Crop and Environmental Sciences Division, International Rice Research Institute (IRRI), Los Baños, Philippines
3Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Court, Western Bank, Sheffield S10 2TN, UK
4South China Institute of Botany, Academia Sinica, Leyiju, Guangzhou 510650, PR China
* To whom correspondence should be addressed. E-mail: Erik.murchie{at}nottingham.ac.uk
Received 20 February 2007; Revised 11 July 2007 Accepted 24 July 2007
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Abstract |
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Crop improvement in terms of yield is rarely linked to leaf photosynthesis. However, in certain crop plants such as rice, it is predicted that an increase in photosynthetic rate will be required to support future grain yield potential. In order to understand the relationships between yield improvement and leaf photosynthesis, controlled environment conditions were used to grow 10 varieties which were released from the International Rice Research Institute (IRRI) between 1966 and 1995 and one newly developed line. Two growth light intensities were used: high light (1500 µmol m–2 s–1) and low light (300 µmol m–2 s–1). Gas exchange, leaf protein, chlorophyll, and leaf morphology were measured in the ninth leaf on the main stem. A high level of variation was observed among high light-grown plants for light-saturated photosynthetic rate per unit leaf area (Pmax), stomatal conductance (g), content of ribulose bisphosphate carboxylase-oxygenase (Rubisco), and total leaf protein content. Notably, between 1966 and 1980 there was a decline in Pmax, g, leaf protein, chlorophyll, and Rubisco content. Values recovered in those varieties released after 1980. This striking trend coincides with a previous published observation that grain yield in IRRI varieties released prior to 1980 correlated with harvest index whereas that for those released after 1980 correlated with biomass. Pmax showed significant correlations with both g and Rubisco content. Large differences were observed between high light- and low light-grown plants (photoacclimation). The photoacclimation ‘range’ for Pmax correlated with Pmax in high light-grown plants. It is concluded that (i) leaf photosynthesis may be systematically affected by breeding strategy; (ii) Pmax is a useful target for yield improvements where yield is limited by biomass production rather than partitioning; and (iii) the capacity for photoacclimation is related to high Pmax values.
Key words: Acclimation, biomass, historical, improvement, irradiance, morphology, photosynthesis, rice, Rubisco, variation
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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The yields of major crops including rice have risen by around 2-fold in the last century through genetic improvement, management practice, control of pests and diseases, and a greatly increased fertilizer application rate (Evans, 1993). However, it is predicted that further improvements will be required on existing land area to meet the demand of future populations (Sheehy, 2000). As with many other crop species, the major improvements in rice yield potential in the past have included empirical breeding to alter morphological and physiological traits which ultimately improve the efficiency of resource capture. The breakthrough arose with the release of the variety IR8 at the International Rice Research Institute (IRRI) in 1966. This was the first high-yielding modern rice variety, and it heralded the start of the ‘green revolution’ in Asian rice production. IR8 was semi-dwarf with a high tillering rate, erect leaves, high harvest index (HI), and high nitrogen responsiveness. From 1966 to 1997, >44 semi-dwarf indica varieties developed by IRRI have been released for irrigated lowland rice, with the emphasis on breeding to improve disease and pest resistance, and grain quality, and to shorten growth duration (Peng et al., 1999; Khush and Virk, 2005).
Evidence suggests that many of the mechanisms used to improve rice yield potential in the past, such as canopy architecture and HI, are now close to optimization and that future improvements will arise from an improvement in total biomass production (Horton, 2000; Sheehy, 2000; Long et al., 2006b). A useful parameter is radiation use efficiency (RUE) which is the amount of biomass produced per unit of radiation intercepted. Among a comparison of different crop species it was concluded that rice has one of the lowest RUEs of C3 crops (Mitchell et al., 1998). It is strongly predicted that raising the leaf photosynthetic rate in rice will also raise the RUE, biomass production, and yield. There is therefore renewed interest in ways of improving photosynthetic rate on the individual leaf level. Direct evidence already exists that an increased photosynthetic rate forms the basis for an increase in canopy CO2 fixation rate and productivity; for example, growth of crops in elevated CO2 levels often results in a higher biomass and yield (Ainsworth et al., 2004; Long et al., 2006b), including rice (Baker et al., 1990; Ziska et al., 1997).
However, attempts to improve yield by selecting for crop plants with high light-saturated photosynthetic rate (Pmax) have resulted in mixed success (Austin et al., 1989; Gutierrez-Rodriguez et al., 2000). There have been a number of mechanisms proposed to explain this. First, grain yield improvement has so far targeted beneficial traits and practices which did not depend on increasing or even maintaining the level of leaf photosynthesis. For example, leaf area index (LAI), application and uptake of nitrogen fertilizer, and increased leaf duration are all traits which have the potential to increase photosynthesis per unit canopy but which can occur with no change (or paradoxically even a decline) in photosynthesis per unit leaf area. It seems likely that leaf photosynthetic rate will exert a higher degree of control on grain yield only when the effect of other factors such as partitioning, nutrient responsiveness, and LAI have been minimized (Long et al., 2006b). In fact, experiments which have attempted to reduce the background genetic variation have had greater success (Watanabe et al., 1994; Gutierrez-Rodriguez et al., 2000). For this reason, the relationship between leaf photosynthesis and grain yield should become particularly close when only biomass production is limiting for yield, rather than partitioning or nitrogen application.
Secondly, the question of which photosynthetic parameter will be most relevant in crop improvement has been debated. On a leaf level, most attention has been focused on the Pmax, possibly because photosynthesis at light-limiting conditions is much more variable. However, a large number of leaves within mature canopies exist in a light-limited state (Murchie et al., 2002a). Therefore, the value of Pmax in yield improvement needs to be established.
Studying well-characterized series of historical varieties allows the comparison of leaf photosynthesis with the known changes that were introduced through breeding. In fact, there have been many studies of historical series in different crop species which attempt to identify the genetic improvement in yield potential. In those examples which examined leaf photosynthesis, substantial variation in photosynthetic capacity has been observed. Attempts have been made to rationalize this variation according to physiological trends in breeding and associated strategies of adaptation, but with varying degrees of success (Evans, 1993). In the case of rice, photosynthesis tended to be lower in the wild Oryza species compared with O. sativa (Cook and Evans, 1983). However, in another study (Yeo et al., 1994), a higher rate of photosynthesis was observed in O. australiensis compared with O. sativa, and a similar observation has been made for wheat (Evans and Dunstone, 1970; Austin et al., 1982). Among varieties of O. sativa, there has been evidence that varieties released after 1950 in Japan have an elevated rate of photosynthesis per unit leaf area (Zhang and Kokubun, 2004). A rice variety series bred in Japan over a hundred year period showed improvements in photosynthetic capacity in the 2 week period following heading (Sasaki and Ishii, 1992). A rice variety series released over the same time period showed yield improvement and concluded that photosynthetic improvements could be seen 3 weeks after heading under high nitrogen application (Zhang and Kokubun, 2004).
Whilst these studies have been useful, it is argued that it is now essential to perform comparisons under controlled environment (CE) conditions which simulate field conditions in a realistic manner. In this way the physiological and biochemical limitations to photosynthesis can be tightly regulated and measured. In the field, environmental conditions have the potential to cause a much higher level of variation in leaf photosynthetic capacity (Black et al., 1995; Murchie et al., 1999). Peng et al., (2000) grew rice varieties developed at IRRI between 1966 and 1995 to reveal the underlying traits associated with yield improvement over this period. A biphasic response was shown where grain yield in varieties before 1980 correlated with HI and those after 1980 correlated with total biomass.
The search for ways to improve the photosynthetic performance of crops is timely, and here it is argued that it is vital to understand how leaf photosynthesis has been altered by plant breeding. In this report, photosynthetic variation in a series of historical IRRI varieties is analysed. By growing plants in a purpose-built tropical CE facility under hydroponic conditions where pot confinement is not an issue, the hypothesis is tested that leaf level photosynthesis was affected by genetic alterations in whole plant morphology and partitioning. Grain partitioning or grain sink effects are deliberately avoided by conducting measurements in the pre-heading stage. Pmax also responds to long-term changes in irradiance, a process termed acclimation or photoacclimation. There is a need to analyse the significance of photoacclimation in the context of crop photosynthesis and assess whether there is scope for improvement. The hypothesis is tested that photoacclimation will affect the measurement of Pmax and its use in yield improvement.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Ten varieties were selected as being widely planted in different historical periods from 1966 to 1997. The varieties and year of release were IR8 (1966), IR20 (1969), IR22 (1969), IR40 (1977), IR42 (1977), IR45 (1978), IR54 (1980), IR68 (1988), IR72 (1988), and PSBRc2 (1991). Breeders’ seeds of the entries were used. The seed was stored at 18 °C and multiplied every 4 years. Additionally, one new plant type (NPT) line (IR655680-42-5-2) was used for comparison (unreleased, 1997). Plants were grown at the University of Sheffield in a Conviron BDW 160-R walk-in CE chamber (Conviron, Winnipeg, Canada). Irradiance was provided by a combination of metal halide and tungsten–halogen incandescent bulbs. Air temperature was maintained at 30/20 °C (day/night). Photoperiod was 12 h and both temperature and light intensity were raised from night level to day level over a 3 h period in the morning and then lowered to night level over a 3 h period in the same way in the evening. A full photosynthetic photon flux density (PPFD) of 1500 µmol m–2 s–1 was therefore achieved for a 7 h period. Relative humidity was maintained at 60% throughout the photoperiod. Low light (LL) treatment of 300 µmol m–2 s–1 was provided by neutral density shading (‘Scrim’, Lee filters, Andover, UK). These rooms provided good mixing of air and an even distribution of light.
Germinated seedlings were planted out on to a hydroponic growing system which consisted of containers 10.0 l in volume and 22 cm in diameter. Each of these containers held three plants using a plastic support. The containers were largely impermeable to light, and very little algal growth was observed. Nutrients were supplied in a hydroponics medium which was replaced weekly. De-ionized water was used to make up a solution containing 1.4 mM NH4NO3, 0.6 mM NaH2PO4·.2H2O, 0.5 mM K2SO4, 0.8 mM MgSO4, 0.2 mM CaCl2·.6H2O, 0.07 mM Fe-EDTA, 0.009 mM MnCl2·.4H2O, 0.0001 mM (NH4)6Mo7O24·.4H2O, 0.037 mM H3BO3, 0.0003 mM CuSO4·.5H2O, 0.000138 mM NH4VO3, 0.00075 mM ZnSO4·.7H2O, and 0.2 g l–1 potassium silicate solution (VWR Chemicals, No. 296546S). The pH of this solution was monitored and was always between 5 and 6. Plants were grown to the leaf 9 stage before measurements and samples were taken. Only the main stem was used for measurements. The point of full leaf expansion (FLE) was determined on leaf 9 for each plant. The distance from the leaf tip to ligule was measured daily, and FLE taken as the cessation of elongation of the leaf blade. To avoid any reduction in photosynthesis caused by leaf ageing, measurements were made and samples taken on the fourth day after FLE (Murchie et al., 2005).
Photosynthesis was measured using a Li-cor 6400 portable photosynthesis system (Li-Cor Inc., Lincoln, NE, USA) with the 6400-40 attachment which used red/blue light-emitting diodes (LEDs) for provision of actinic light (maximum 10% blue). Measurements were made in situ within the growth chamber for practical purposes. Leaf chamber temperature was maintained at 30 °C and ambient humidity was used. Photosynthesis was measured using automatically generated light response curves with the following protocol. Measurements were made on a region of leaf one-third the distance from tip to ligule. Once the leaf was within the chamber, the program commenced with a 3 min dark period. The program remained at each light intensity for a minimum of 3 min until stability of 
CO2 was achieved in the sample chamber, as determined by the system software. At the end of each light period, gas exchange parameters were recorded. The sequence of PPFD (in µmol m–2 s–1) was 0, 20, 100, 300, 500, 700, 1000, 1500, 1800, 2000, and 2500. The light-saturated rate of photosynthesis was taken as the rate at 2500 µmol m–2 s–1.
Following photosynthetic measurements, leaf morphology measurements were made and leaf samples were taken for protein and pigment analysis using a circular hole-punch of known area. Leaves were immediately frozen in liquid nitrogen and stored at –80 °C until analysed, which was within 3 months. Chlorophyll a and b were measured by extraction and analysis in 80% (v/v) acetone (Porra et al., 1989). The amount of total protein and ribulose bisphosphate carboxylase-oxygenase (Rubisco) was determined according to Murchie et al. (2002b). Total protein determination used the Bradford total protein assay method, and Rubisco was analysed using SDS-PAGE followed by densitometric analysis of Coomassie-stained gels, quantified using purified wheat Rubisco as a standard. Statistical analyses were made using Graphpad Prism (Graphpad Software, San Diego, CA, USA) and Sigmaplot (Systat Software, San Jose, CA, USA).
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Results and discussion |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Identifying trends in leaf photosynthetic capacity
It has been argued that leaf photosynthesis stands out as a trait which will improve the yield potential of key crops in the absence of an alteration of other crop yield components, such as HI (Horton, 2000; Reynolds et al., 2000; Long et al., 2006a). In the case of C3 crops such as rice and wheat, an increase in the efficiency of Rubisco carboxylation is seen as a key step in the future attainment of plants with a higher potential photosynthetic rate and RUE. Besides Rubisco there are other targets that have been proposed which are based on raising the efficiency of light capture and transduction at morphological and biochemical levels (Murchie et al., 1999; Horton, 2000; Zhu et al., 2004; Long et al., 2006b). If achieved, all of these fundamental improvements to crop biology should form the basis for a revolution in agricultural productivity.
IR8 was the first high-yielding modern variety of rice for the tropics. It is a semi-dwarf with a high N responsiveness, high HI, erect leaves, and a high numbers of tillers. Since its release, breeding has focused on disease and insect resistance, earlier maturity, and grain quality improvement. When historical varieties developed at IRRI were grown in the field in 1996 and 1995, a clear correlation between grain yield and year of release, from 7 t ha–1 (released in 1966) to almost 10 t ha–1 (released in 1995), was seen (Peng et al., 2000). When the underlying mechanisms were analysed, a biphasic pattern emerged. Grain yield in varieties released during the period 1966–1980 correlated significantly with HI. This reflected the need to increase the low grain weight or poor grain filling of varieties during the period 1966–1973. Conversely, grain yield in those varieties released during the period 1980–1995 correlated significantly with biomass production. From a physiological viewpoint, it may be argued that these two periods represent fundamentally different processes driving improvements in grain yield. Raising HI involved a reduction in canopy height, growth duration, and spikelets per panicle, and therefore increased relative sink capacity (Peng et al., 2000). Improvements in biomass production had largely unknown physiological origins.
Varieties developed by IRRI and released over the period 1966–1995, grown under controlled conditions, were used. Figure 1 shows data for gas exchange, and chlorophyll and protein content for high light (HL)-grown plants. Despite a large variation, no clear single trend in photosynthetic parameters (Pmax) or leaf composition could be identified over the 30 year period for either HL- or LL-grown plants. A number of interesting features appear, such as the high Pmax in IR8 (the original high yielding variety), strongly suggesting that yield improvements since 1966 were not related to changes in Pmax.
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However, if the data are separated into the two eras of yield improvement identified by Peng et al. (2000), an intriguing picture emerges, shown in Fig. 1. Between 1966 and 1980 (in HL plants), a significant decline in Pmax, stomatal conductance (g), Rubisco content, total leaf protein, and chlorophyll content was observed. No significant correlations for any parameter were observed for the period 1980–1995. The cause of these striking trends is unclear. An immediate suggestion would be that they are related to morphology: an improvement in LAI, for example, is achieved by increasing total leaf area of the plant. As pointed out by other workers, this may involve a decreased investment per unit leaf area, resulting in a lower amount of photosynthetic components, i.e. more photosynthesis but over a larger leaf area (Evans, 1993). The area of leaf 9 did not correlate significantly with either Pmax or Rubisco content (Fig. 2) and therefore this process occurred on a whole plant scale rather than the scale of the individual leaf. However, data for IRRI varieties during this period show that for varieties released between 1966 and 1980, LAI and plant height declined whilst tillering rate and HI increased (Peng et al., 2000). This would tend toward a ‘concentration’ of photosynthetic components over a smaller leaf area rather than a ‘dilution’ over a large one. It is concluded that the decline in leaf photosynthetic rate in varieties released during this period was not caused by an alteration in plant morphology. The coincidence of changes in Rubisco, protein, and chlorophyll per unit leaf area could have been caused by an alteration of rice leaf thickness (Murchie et al., 2005), or photosynthetic components per unit cell or per unit chloroplast (Murchie and Horton, 1997).
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It is important to note that Pmax recovered to higher levels in varieties released after 1980 (Fig. 1). It is suggested from these data that an increase in leaf level photosynthesis in rice is more likely to be observed in circumstances where an increase in biomass production dominates. It is interesting that this observation has been made in the pre-heading stage which will not be influenced by grain partitioning or grain sink effects. According to Yoshida (1981) this is a growth stage with a high growth rate. Previous research has often used the grain filling period since this is a period critical to final yield, which has also been observed to result in sink limitation of photosynthesis (Evans, 1993), but not in some studies (Murchie et al., 2002a).
The mechanism of variation in Pmax
The previous section successfully placed the variation in Pmax according to breeding period. Figure 3 plots Pmax against (g) and Rubisco content for HL-grown plants. Pmax at saturating irradiance and ambient CO2 levels frequently correlates well with Rubisco content in rice (Makino et al., 1985; Makino, 2003). Biochemical models of leaf photosynthesis show that under these conditions in unstressed leaves a large component of the total photosynthetic rate is limited by the rate of carboxylation of Rubisco (von Caemmerer and Farquhar, 1981). It is notable that the correlation of Pmax with g was higher than the correlation with Rubisco content. Under the conditions used in this study which were not water limited, stomatal resistance would not be expected to be a large component of Pmax. Additionally, there may be variation among varieties in the extent of activation of Rubisco. It is interesting here to compare how stomatal conductance varies between varieties in relation to Rubisco content. It will be important in future work to determine the proportional contribution of stomatal and mesophyll conductance to trends in Pmax. This also has high relevance for strategies to maximize assimilation in crops where water is an increasingly limited resource.
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Figure 3 also shows how the relationship between Pmax, g, and Rubisco content differs for each variety. Varieties are grouped to show that they occupy the same positions on both plots, with one notable exception: IR72. This variety possessed a particularly high Pmax and g for a given Rubisco content. If this variety is removed, the correlation between Rubisco and Pmax was much improved. It could be concluded that IR72 achieved a higher Pmax/Rubisco content, and this was associated with a higher g. It will be of great interest to ascertain the mechanism by which IR72 can achieve a higher rate of Pmax with a lower Rubisco content. This is in agreement with data collected from the field (Murchie et al., 1999, 2002) which showed IR72 with a higher Pmax but lower Rubisco and protein content in comparison with NPT lines. It was suggested that this was caused by the dominant role of the need to accumulate high levels of leaf nitrogen for subsequent remobilization during grain growth.
Photoacclimation in rice crops
Photosynthesis responds to irradiance in the long term by altering amounts of photosynthetic components per unit leaf area and per unit chloroplast, a process called acclimation or photoacclimation. At lower irradiance levels these alterations have the effect of changing the Pmax. However, when a sufficiently high irradiance is reached, the capacity for photoacclimation is exceeded and the increased imbalance in absorbed versus utilized light energy causes the induction of photoprotective processes. In the case of rice, photoacclimation has been observed in the field (Murchie et al., 2002a) and in the laboratory (Murchie et al., 2005), and can be separated from the effects of leaf ageing.
For the most part, acclimation is a well-characterized process. It acts to optimize the photosynthetic rate according to available resources. Despite suggestions in the literature that its existence is widespread among species and varieties, its role in crop photosynthesis and even crop improvement has remained largely unexplored. It is argued that its analysis in the context of crop improvement is timely: first it remains to be demonstrated whether Pmax is in part determined by the ability to acclimate to high irradiance levels such as those experienced in tropical conditions (Murchie et al., 2002). Secondly, recent work predicts that the dynamic nature of irradiance within crop canopies influences canopy photosynthetic rate via the slow recovery of 
CO2 and PSII (photosystem II) following high light exposure (Zhu et al., 2004). Since photoacclimation alters the proportion of absorbed light which is in excess of photosynthetic requirements, it is likely to influence these processes. Thirdly, work in crop plants and among a number of other species has shown that leaf N content is closely related to the irradiance level within canopies. Since photosynthetic components are a large sink for leaf N (Rubisco makes up 
30% of total leaf protein), this strongly implies that the process of photoacclimation is involved in optimization of the photosynthesis–N relationship within rice canopies (Murchie et al., 2002). This is important since a significant proportion of photosynthesis in crop canopies is within the light-limited state (Ort and Baker, 1988). Acclimation to irradiance therefore affects a number of leaf level processes in addition to the efficiency of canopy light capture. It seems likely that variability in photoacclimation would have a genetic basis.
In addition to its apparent ubiquity, photoacclimation can be considered to have a dynamic range (Bailey et al., 2001) which varies according to species and variety (Murchie and Horton, 1997; Murchie et al., 2002). This range was measured in the historical IRRI varieties. The plants showed a strong response to growth irradiance in terms of morphology, Pmax, chlorophyll, and protein content (Murchie and Horton, 1997; Murchie et al., 2002a; Walters, 2005). Consistent with previous work, plants grown at 300 µmol m–2 s–1 had a higher area per leaf with a lower value per unit area of Pmax, Rubisco, and total protein, and a higher value of chlorophyll per unit leaf area when compared with those grown at 1500 µmol m–2 s–1. It is important to note that no trend for photoacclimation of leaf area (proportional change) could be seen, nor were there correlations with photoacclimation of other measurements. Therefore, changes were not due to a ‘dilution’ effect.
A lower chlorophyll a:b ratio was also observed, which is caused by an increase in amounts of light-harvesting complexes relative to other chlorophyll-containing pigment proteins. These data are shown in Fig. 4 where the proportional change in each parameter is shown. In seven of the varieties, g was higher in LL-grown plants. The phenomenon of shade-grown plants possessing a high transpiration rate on exposure to high irradiance has been documented (Sims and Pearcy, 1992). Ci was generally higher in the shade-grown plants, most probably due to the higher stomatal conductance and lowered photosynthetic and respiratory capacity (not shown).
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However, identifying any pattern in photoacclimation pattern according to year of release or breeding strategy is not straightforward. In fact, there were no significant correlations between year of release and photoacclimation (calculated as the proportional difference between HL and LL for any parameter). However, if the same analysis as seen in Fig. 1 is applied, then a number of features emerge (Fig. 4). Significant trends were seen for chlorophyll content (pre-1980), chlorophyll a:b ratio (post-1980), and total protein (pre-1980). These are difficult to reconcile. However, it is suggested that (i) there are signs of a decline in the ability of leaves to undergo photoacclimation between 1966 and 1980; and (ii) the chlorophyll a:b ratio showed less photoacclimation between 1980 and 1995. Interestingly the trends in chlorophyll content were not clearly related to photoacclimation of Rubisco, total protein, or Pmax, which all showed broadly similar patterns. The chlorophyll a:b ratio of varieties released between 1980 and 1995 showed a decline in photoacclimation, because of a lower ratio in HL-grown plants. During this breeding period there was an effort to produce plants with higher chlorophyll content where it was used as a proxy for higher nitrogen and photosynthetic rate. Higher chlorophyll seems to have been achieved by enrichment in chlorophyll b, i.e. through the synthesis of more light-harvesting complexes.
It has been argued that the ability to increase Pmax in response to high growth irradiance (photoacclimation) is one of the factors involved in determining the upper limit to Pmax (Horton, 2000; Murchie et al., 2002a). If this is the case, then one consequence may be a positive relationship between the proportional increase in values between HL and LL and the final HL value of Pmax. This relationship is investigated in Fig. 5. A statistically significant correlation was seen between Pmax under HL and the proportional change in Pmax. The same effect was noted with Rubisco content. This supports the hypothesis that the dynamic range for photoacclimation is related to the Pmax value for a given genotype. It has important consequences for the future improvement of Pmax, and it is concluded that the genetic basis of photoacclimation range in crop plants should be analysed with urgency. The significance of the value of Pmax for LL is uncertain, although it may be of importance when considering variation in irradiance level caused by light flecks in the canopy.
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Therefore, within any study which examines the role of Pmax it is essential to (i) confirm that measurements are made in plants acclimated to high not low irradiance; and (ii) establish the variation in the ability of a plant to alter Pmax in response to irradiance. It is essential to give consideration to how breeding has affected the acclimation process itself, an area of research in need of attention. The present data show significant levels of acclimation to irradiance of every parameter measured, which confirms the importance of attention to growth irradiance.
Concluding remarks and recommendations
The decline in Pmax for varieties released between 1966 and 1980 and the subsequent recovery suggest that Pmax will be useful in future selection of varieties where biomass production is the major limiting factor for yield. Evidence for variation in the limitation of photosynthesis by both Rubisco and g was found, despite the use of hydroponics and lowland irrigated varieties. It is recommended that both of these limitations should be analysed for future improvements in both lowland and upland systems.
Substantial variation among varieties was observed in the range of photoacclimation, establishing its potential for the improvement of canopy light use efficiency. The correlation between photoacclimation range and Pmax in HL-grown plants is of great interest for the improvement of leaf photosynthesis because it implies that the propensity for photoacclimation is involved in determining the maximum possible value of Pmax. Future work should view photosynthesis in crop plants as a dynamic process in relation to the light environment: in particular it should identify the genetic basis of photoacclimation in crop plants. The functional consequences of the variation in Pmax at lower, light-limiting growth irradiance levels is worthy of further investigation.
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Acknowledgements |
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This work was funded by the UK Department for International Development and the Biotechnology and Biological Sciences Research Council.
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References |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Ainsworth EA, Rogers A, Nelson R, Long SP. Testing the ‘source–sink’ hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agricultural and Forest Meteorology (2004) 122:85–94.[CrossRef][ISI]
Austin RB, Ford MA, Morgan CL. Genetic-improvement in the yield of winter-wheat—a further evaluation. Journal of Agricultural Science (1989) 112:295–301.
Austin RB, Morgan CL, Ford MA. Flag leaf photosynthesis of Triticum aestivum and related diploid and tetraploid species. Annals of Botany (1982) 49:177–189.
Bailey S, Walters RG, Jansson S, Horton P. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta (2001) 213:794–801.[CrossRef][ISI][Medline]
Baker JT, Allen LH, Boote KJ. Growth and yield responses of rice to carbon-dioxide concentration. Journal of Agricultural Science (1990) 115:313–320.
Black CC, Tu ZP, Counce PA, Yao PF, Angelov MN. An integration of photosynthetic traits and mechanisms that can increase crop photosynthesis and grain production. Photosynthesis Research (1995) 46:169–175.[CrossRef][ISI]
Cook MG, Evans LT. Some physiological aspects of the domestication and improvement of rice (Oryza spp). Field Crops Research (1983) 6:219–238.[CrossRef][ISI]
Evans LT. Crop evolution, adaptation and yield. (1993) Cambridge: Cambridge University Press.
Evans LT, Dunstone RL. Some physiological aspects of evolution in wheat. Australian Journal of Biological Sciences (1970) 23:725.
Gutierrez-Rodriguez M, Reynolds MP, Larque-Saavedra A. Photosynthesis of wheat in a warm, irrigated environment. II. Traits associated with genetic gains in yield. Field Crops Research (2000) 66:51–62.[CrossRef][ISI]
Horton P. Prospects for crop improvement through the genetic manipulation of photosynthesis: morphological and biochemical aspects of light capture. Journal of Experimental Botany (2000) 51:475–485.
Khush GS, Virk PS. IR varieties and their impact (2005) Manila, Philippines: International Rice Research Institute.
Long SP, Ainsworth EA, Leakey ADB, Nosberger J, Ort DR. Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations. Science (2006a) 312:1918–1921.
Long SP, Zhu XG, Naidu SL, Ort DR. Can improvement in photosynthesis increase crop yields? Plant, Cell and Environment (2006b) 29:315–330.[CrossRef][Medline]
Makino A. Rubisco and nitrogen relationships in rice: leaf photosynthesis and plant growth. Soil Science and Plant Nutrition (2003) 49:319–327.
Makino A, Mae T, Ohira K. Photosynthesis and ribulose-1,5-bisphosphate carboxylase oxygenase in rice leaves from emergence through senescence—quantitative-analysis by carboxylation oxygenation and regeneration of ribulose 1,5-bisphosphate. Planta (1985) 166:414–420.[CrossRef][ISI]
Mitchell PL, Sheehy JE, Woodward FI. Potential yields and the efficiency of radiation use in rice. IRRI discussion paper series No. 32 (1998) Manila (Philippines): International Rice Research Institute.
Murchie EH, Chen YZ, Hubbart S, Peng SB, Horton P. Interactions between senescence and leaf orientation determine in situ patterns of photosynthesis and photoinhibition in field-grown rice. Plant Physiology (1999) 119:553–563.
Murchie EH, Horton P. Acclimation of photosynthesis to irradiance and spectral quality in British plant species: chlorophyll content, photosynthetic capacity and habitat preference. Plant, Cell and Environment (1997) 20:438–448.[CrossRef]
Murchie EH, Hubbart S, Chen YZ, Peng SB, Horton P. Acclimation of rice photosynthesis to irradiance under field conditions. Plant Physiology (2002a) 130:1999–2010.
Murchie EH, Hubbart S, Peng S, Horton P. Acclimation of photosynthesis to high irradiance in rice: gene expression and interactions with leaf development. Journal of Experimental Botany (2005) 56:449–460.
Murchie EH, Yang JC, Hubbart S, Horton P, Peng SB. Are there associations between grain-filling rate and photosynthesis in the flag leaves of field-grown rice? Journal of Experimental Botany (2002b) 53:2217–2224.
Ort DR, Baker NR. Consideration of photosynthetic efficiency at low light as a major determinant of crop photosynthetic performance. Plant Physiology and Biochemistry (1988) 26:555–565.[ISI]
Peng S, Cassman KG, Virmani SS, Sheehy J, Khush GS. Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential. Crop Science (1999) 39:1552–1559.
Peng S, Laza RC, Visperas RM, Sanico AL, Cassman KG, Khush GS. Grain yield of rice cultivars and lines developed in the Philippines since 1966. Crop Science (2000) 40:307–314.
Porra RJ, Thompson WA, Kriedemann PE. Determination of accurate extinction coefficients and simultaneous-equations for assaying chlorophyll-a and chlorophyll-b extracted with 4 different solvents—verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochimica et Biophysica Acta (1989) 975:384–394.
Reynolds MP, van Ginkel M, Ribaut JM. Avenues for genetic modification of radiation use efficiency in wheat. Journal of Experimental Botany (2000) 51:459–473.
Sasaki H, Ishii R. Cultivar differences in leaf photosynthesis of rice bred in Japan. Photosynthesis Research (1992) 32:139–146.[CrossRef][ISI]
Sheehy JE. Limits to yield for C3 and C4 rice: an agronomist's view. In: Redesigning rice photosynthesis to increase yield—Sheehy JE, Mitchell PL, Hardy B, eds. (2000) Makati City/Amsterdam: International Rice Research Institute/Elsevier.
Sims DA, Pearcy RW. Response of leaf anatomy and photosynthetic capacity in alocasia-macrorrhiza (Araceae) to a transfer from low to high light. American Journal of Botany (1992) 79:449–455.[CrossRef][ISI]
von Caemmerer S, Farquhar G. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta (1981) 153:376–387.[CrossRef][ISI]
Walters RG. Towards an understanding of photosynthetic acclimation. Journal of Experimental Botany (2005) 56:435–447.
Watanabe N, Evans JR, Chow WS. Changes in the photosynthetic properties of Australian wheat cultivars over the last century. Australian Journal of Plant Physiology (1994) 21:169–183.[ISI]
Yeo ME, Yeo AR, Flowers TJ. Photosynthesis and photorespiration in the genus Oryza. Journal of Experimental Botany (1994) 45:553–560.
Yoshida S. Fundamentals of rice crop science (1981) Manila, Philippines: International Rice Research Institute.
Zhang WH, Kokubun M. Historical changes in grain yield and photosynthetic rate of rice cultivars released in the 20th century in Tohoku region. Plant Production Science (2004) 7:36–44.[CrossRef][ISI]
Zhu XG, Ort DR, Whitmarsh J, Long SP. The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. Journal of Experimental Botany (2004) 55:1167–1175.
Ziska LH, Namuco O, Moya T, Quilang J. Growth and yield response of field-grown tropical rice to increasing carbon dioxide and air temperature. Agronomy Journal (1997) 89:45–53.
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