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The Physiological Ecology of C3-C4 Intermediate Eudicots in Warm Environments

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The Physiological Ecology of C3-C4 Intermediate Eudicots in Warm Environments THE PHYSIOLOGICAL ECOLOGY OF C3-C4 INTERMEDIATE EUDICOTS IN WARM ENVIRONMENTS by Patrick John Vogan A thesis submitted in conformity with the requirements for the degree of Doctorate of Philosophy Department of Ecology and Evolutionary Biology University of Toronto © Copyright Patrick John Vogan 2010 ii The Physiological Ecology of C3-C4 Intermediate Eudicots in Warm Environments Patrick John Vogan, Doctor of Philosophy, 2010 Department of Ecology and Evolutionary Biology, University of Toronto Abstract The C3 photosynthetic pathway uses light energy to reduce CO2 to carbohydrates and other organic compounds and is a central component of biological metabolism. In C3 photosynthesis, CO2 assimilation is catalyzed by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), which reacts with both CO2 and O2. While competitive inhibition of CO2 assimilation by oxygen is suppressed at high CO2 concentrations, O2 inhibition is substantial when CO2 concentration is low and O2 concentration is high; this inhibition is amplified by high temperature and aridity (Sage 2004). Atmospheric CO2 concentration dropped below saturating levels 25-30 million years ago (Tipple & Pagani 2007), and the C4 photosynthetic pathway is hypothesized to have first evolved in warm, low latitude environments around this time (Christin et al. 2008a). The primary feature of C4 photosynthesis is suppression of O2 inhibition through concentration of CO2 around Rubisco. This pathway is estimated to have evolved almost 50 times across 19 angiosperm families (Muhaidat et al. 2007), a remarkable example of evolutionary convergence. In several C4 lineages, there are species with photosynthetic traits that are intermediate between the C3 and C4 states, known as C3-C4 intermediates. In two eudicot genera, Flaveria (Asteraceae) and Alternanthera (Amaranthaceae), there is evidence that these species represented an intermediate state in the evolution of the C4 pathway (McKown et al. 2005; Sanchez-del Pino 2009). The purpose of this thesis is to ascertain the specific benefits to plant carbon balance ii iii and resource-use efficiencies of the C3-C4 pathway relative to C3 species, particularly at low CO2 concentrations and high temperatures, factors which are thought to have been important in selecting for C3-C4 traits (Ehleringer et al. 1991). This will provide information on the particular advantages of the C3-C4 pathway in warm, often arid environments and how these advantages may have been important in advancing the initial stages of C4 evolution in eudicots. This thesis addresses the physiological intermediacy of previously uncharacterized C3-C4 species of Heliotropium (Boraginaceae); the water- and nitrogen-use efficiencies of C3-C4 species of Flaveria; and the photosynthetic performance and acclimation of C3, C4 and C3-C4 species of Heliotropium, Flaveria and Alternanthera grown at low and current ambient CO2 levels and high temperature. iii iv Acknowledgements I would like to recognize those who contributed to the completion of this thesis. Firstly, my graduate advisor, Dr. Rowan Sage for educating me in plant physiological ecology and spending countless hours reviewing and overseeing my research. Also, I would like to thank my parents, John and Donna Vogan, for their selfless support of my education and personal development for all these years, as well as the rest of my family. Finally, I must recognize the contributions of the innumerable friends and colleagues that I have met in the past five and a half years in Canada, the United States and the United Kingdom. There are far too many to list individually, but I want to express my sincerest gratitude to the graduate students, faculty members, technicians, horticulturists, post-doctoral fellows, administrative staff, research collaborators and friends from all walks of life who supported me in countless ways during the completion of my degree. iv v Table of Contents Abstract……………………………………………………………………………………….ii Acknowledgements………………………………………………………………...….…......iv Table of Contents......................................................................................................................v List of Tables..........................................................................................................................viii List of Figures..........................................................................................................................ix Chapter One – Introduction.......................................................................................................1 I.) C3 photosynthesis and the problem of photorespiration...........................................1 i.) C3 photosynthesis: mechanism and origins...........................................................1 ii.) The photorespiratory cycle....................................................................................2 iii.) The effects of photorespiration on CO2 assimilation............................................4 iv.) Carbon balance and fitness of C3 plants under low CO2 conditions.....................6 II.) Atmospheric CO2 and the rise of C4 photosynthesis...............................................9 i.) The mechanism of C4 photosynthesis....................................................................9 ii.) The physiological ecology of C4 photosynthesis.................................................16 iii.) The evolutionary origins of C4 photosynthesis....................................................19 III.) C3-C4 intermediate photosynthesis.......................................................................23 i.) The anatomy and physiology of C3-C4 photosynthetic plants..............................23 ii.) The taxonomic and ecological distributions of C3-C4 photosynthesis.................26 IV.) Models of C4 evolution........................................................................................28 V.) Thesis objectives..................................................................................................33 Chapter Two – The functional significance of C3-C4 intermediate traits in Heliotropium (Boraginaceae): gas exchange perspectives.............................................................................36 v vi Abstract........................................................................................................................36 Introduction.................................................................................................................36 Materials and Methods................................................................................................39 Results.........................................................................................................................43 Discussion....................................................................................................................55 Conclusion...................................................................................................................59 Chapter Three – Water-use and nitrogen-use efficiency of C3-C4 intermediate species of Flaveria Juss. (Asteraceae).....................................................................................................61 Abstract.......................................................................................................................61 Introduction.................................................................................................................61 Materials and Methods................................................................................................66 Results.........................................................................................................................69 Discussion....................................................................................................................90 Conclusion...................................................................................................................96 Chapter Four - Photosynthetic performance and acclimation of C3, C4 and C3-C4 species from three eudicot genera grown at low CO2 concentrations..........................................................97 Abstract.......................................................................................................................97 Introduction.................................................................................................................98 Materials and Methods..............................................................................................103 Results.......................................................................................................................105 Discussion..................................................................................................................133 Conclusion.................................................................................................................139 Chapter Five – Discussion.....................................................................................................141 vi vii I.) C3-C4 intermediacy in Heliotropium and the development of new model systems to study C4 evolution.....................................................................................................142 II.) Water- and nitrogen-use efficiencies of C3-C4 Flaveria species.........................145 III.) The effects of low CO2 on carbon balance and photosynthetic acclimation in C3, C4 and C3-C4 species from multiple evolutionary lineages.......................................150
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