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Title:Strategies to improve C4 photosynthesis, water and resource-use efficiency under different atmospheres, temperatures, and light environments
Author(s):Pignon, Charles Pierre Jacques Alberic Leon
Director of Research:Long, Stephen P.
Doctoral Committee Chair(s):Long, Stephen P.
Doctoral Committee Member(s):Leakey, Andrew D B; Ort, Donald R.; Brown, Patrick J.
Department / Program:Crop Sciences
Discipline:Crop Sciences
Degree Granting Institution:University of Illinois at Urbana-Champaign
Climate change
Global warming
Food security
Water-use efficiency
Nitrogen-use efficiency
Food security
Plant physiology
Abstract:Climate change and a growing world population are predicted to place significant strain on global food security in the 21st century. In order for agriculture to provide food, feed and fuel, it is essential that high-performance crops be developed that are productive, resilient, and require minimal use of inputs. Plants using C4 photosynthesis display many of these traits: in C4 leaves, a biochemical carbon-concentrating mechanism significantly boosts photosynthetic efficiency and overall productivity, while improving the efficiency with which key inputs such as water or nitrogen are used. Several of the world's most important and productive crops, such as maize, sugarcane, and sorghum, all use the C4 pathway. However, even this high-performance system is imperfect, and could be significantly improved. In this thesis we explore strategies for the improvement of C4 photosynthesis in crops. In Chapters 1-3, prospects for optimizing leaf biochemical activity to improve C4 photosynthetic CO2 assimilation are examined. In Chapters 4-7, the relationship of C4 photosynthetic CO2 assimilation with water loss through transpiration is examined, along with how this tradeoff could be improved. Photosynthesis depends on a suite of biochemical reactions, and the rate limitation of a single enzymatic reaction can affect the entire process of photosynthetic CO2 assimilation. For a given amount of leaf nutrients, partitioning is optimal when photosynthesis is co-limited by all of these enzymes, rather than limited by a single process. In Chapter 1, a meta-analysis of published measurements suggests that C4 plants are photosynthetically adapted to the level of atmospheric [CO2] in which their ancestors evolved over the past 400, 000 years, rather than to today's current [CO2]. In a modern, high-CO2 atmosphere, this configuration is sub-optimal and leads to over-investment into the carbon-concentrating mechanism at the expense of other processes. In C4 plants, rate limitation of photosynthesis may be narrowed down to a single enzyme under certain conditions. At low temperature (<15 °C), C4 photosynthesis is generally impaired; this is largely due to limitation by the carboxylation enzyme Rubisco. In fact, it has been suggested that structural limitations within C4 leaves could physically limit the volume available for chloroplastic Rubisco investment. In Chapter 2, the hypothesis that total chloroplast volume limits the capacity of C4 plants to photosynthesize effectively at chilling temperatures is examined. In leaves of several C4 species, it was found that chloroplast volume, determined via confocal microscopy, is more than sufficient to support Rubisco contents that would not be limiting to photosynthetic CO2 assimilation at chilling (<14 °C) temperatures. In Chapter 3, chilling tolerance of the cold-tolerant C4 grass Miscanthus x giganteus is explored, a hybrid between Miscanthus sacchariflorus and Miscanthus sinensis, which maintains photosynthesis even at <14 °C by upregulating expression of key rate-limiting enzymes such as Rubisco and PPDK. Accessions of the parent species M. sacchariflorus, originating from the northern limit of occurrence of the species in Russian Siberia, are identified that surpass the exceptional cold tolerance of M. x giganteus. These show potential for breeding of even more cold tolerant M. x giganteus clones. However, it is clear in all Miscanthus accessions that the shift of photosynthesis away from optimal co-limitation, as described in Chapter 1, is even more pronounced at low temperature. Even these highly competent species are unable to optimally adjust nutrient allocation at low temperature. All higher plants experience a tradeoff between photosynthetic carbon assimilation and water loss through transpiration, as the pathway for CO2 entry into the leaf, via specialized pores called stomata, allows an escape route for water vapor. In Chapter 4, published measurements for maize are combined with a leaf and canopy biophysical model, showing that a substantial reduction in stomatal conductance at today's atmospheric [CO2] could cut plant water loss with minimal consequence to total CO2 assimilation. This emerges as a result of the apparent lack of photosynthetic acclimation to increasing atmospheric [CO2], as implied from the analysis in Chapter 1. In Chapter 5, an attempt to reduce stomatal conductance to test this theoretical prediction is undertaken by downregulation of expression of the SPCH gene in S. bicolor. While the construct was shown to be present, no physiological or anatomical effect of this insertion could be demonstrated. In Chapters 1-5, photosynthesis and stomatal conductance are primarily considered under steady-state conditions, which are not representative of the fluctuating environmental conditions typically experienced by plants in the field. In particular, for photosynthesis and photosynthetic water-use efficiency to be maintained requires that photosynthesis and stomatal conductance are co-ordinated to avoid unnecessary transpiration. In many species, this coordination is not achieved due to slow stomatal movement speed, especially when a leaf suddenly goes into shade. In chapter 6, a large and diverse population of Sorghum bicolor lines is phenotyped, and significant variability in stomatal responses to fluctuating light is identified. The complex trait of stomatal closure is shown to be moderately heritable, and is significantly mapped to genetic markers. The coordination of photosynthetic carbon assimilation with stomatal conductance, and its effect on photosynthetic water-use efficiency, is examined in Chapter 7 with a focus on water use efficiency during sun to shade transitions. Greater variability in ability to maintain water-use efficiency under fluctuating light conditions than at steady state is found across a wide range of sorghum lines. This reflects variable kinetics in both photosynthesis and stomatal conductance, and is linked to leaf stomatal patterning. In conclusion, while C4 photosynthesis is regarded as the most efficient pathway available, this study shows there are nevertheless significant opportunities for improvement. Variability in cold tolerance of photosynthesis in Miscanthus, and in stomatal conductance and water-use efficiency under fluctuating light in Sorghum, could be used in breeding and bioengineering programs.
Issue Date:2017-12-08
Rights Information:Copyright 2017 Charles Pignon
Date Available in IDEALS:2018-03-13
Date Deposited:2017-12

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