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Doctoral Thesis 2015 DOCTORAL THESIS 2015 ACCLIMATION OF PHOTOSYNTHESIS TO WATER DEFICIT AND HIGH TEMPERATURE: PHYSIOLOGICAL AND BIOCHEMICAL ASPECTS Juan Alejandro Perdomo López DOCTORAL THESIS 2015 Doctoral Programme of Biology of the Plants ACCLIMATION OF PHOTOSYNTHESIS TO WATER DEFICIT AND HIGH TEMPERATURE: PHYSIOLOGICAL AND BIOCHEMICAL ASPECTS Juan Alejandro Perdomo López Thesis Supervisor: Dr. Jeroni Galmés Galmés Doctor by the Universitat de les Illes Balears Yo, Dr. Jeroni Galmés Galmés, Profesor Titular del Departamento de Biología de la Facultat de Ciències de la Universitat de les Illes Balears CERTIFICO: Que el presente trabajo titulado “Acclimation of photosynthesis to water deficit and high temperature: physiological and biochemical aspects” presentado por Juan Alejandro Perdomo López para optar al TÍTULO univesitario oficial de DOCTOR por la Universitat de les Illes Balears dentro del Programa de Doctorado de Biología de las Plantas en Condiciones Mediterráneas, se ha realizado bajo mi dirección. Revisado el presente trabajo, autorizo su presentación para que pueda ser juzgada por el tribunal correspondiente. Palma de Mallorca, 24 de noviembre del 2014 Director Autor Dr. Jeroni Galmés Galmés Juan Alejandro Perdomo López A mi Madre y mi Hermana, SYMBOLS AND ABBREVIATIONS LIST Symbol Meaning ADP adenosine diphosphate AG gross CO2 assimilation rate AN net CO2 assimilation rate ATP adenosine triphosphate BL biochemical limitations Bq becquerel Bt total dry biomass Ca atmospheric CO2 concentration Cc chloroplastic CO2 concentration Ci sub-stomatal CO2 concentration CSIRO Commonwealth Scientific and Industrial Research Organization CT control temperature dAN daily net CO2 assimilation rate dAN/dgs daily intrinsic water use efficiency dgs daily stomatal conductance DL diffusive limitations dR daily leaf dark respiration DTT dithiothreitol EDTA ethylene diamine tetraacetic acid ETR electron transport rate FAO Food and Agriculture Organization of the United Nations Fm’ maximum fluorescence in light-adapted state Fm maximum fluorescence in dark-adapted state Fo basal fluorescence of the dark adapted leaf Fs steady-state fluorescence signal Fv/Fm maximum quantum efficiency of PSII photochemistry gbs bundle sheath gm mesophyll conductance GRC growth response coefficient GRCLAR growth response coefficient for the leaf area ratio GRCLCB growth response coefficient for the leaf carbon balance i gs stomatal conductance HT high temperature iAN instantaneous net CO2 assimilation iAN/igs instantaneous intrinsic water use efficiency igs instantaneous stomatal conductance IPCC Intergovernmental Panel on Climate Change iR instantaneous mitochondrial respiration Jmax maximum photosynthetic electron transport rate Kc Michaelis constant for the carboxylation activity of Rubisco c kcat reaction turnover rate for carboxylation activity of Rubisco Ko Michaelis constant for the oxygenation activity of Rubisco KP Michaelis constant of phosphoenol pyruvate carboxylase KRuBP Michaelis constant for the RuBP LA leaf area LAR leaf area ratio LCB leaf carbon balance LMA leaf mass per area LMR leaf mass ratio NCAR the National Center for Atmospheric Research O O2 mole fraction PAR photosynthetic active radiation PEG polyethylene glycol PEP phosphoenolpyruvate PEPC phosphoenolpyruvate carboxylase PG Phosphoglycolate PGA Phosphoglycerate PPFD photosynthetic photon flux density PSII photosystem II PVPP polyvivilpolypirrolidone R mitochondrial respiration RAI relative affectation index Rca Rubisco activase RL non-photorespiratory CO2 evolution in the light ii RuBP 1,5-ribulosebiphosphate RWC relative water content Sc/o In vitro Rubisco specificity factor TAI temperature acclimation index temperature sensitivity index TSI temperature sensitivity index Vcmax maximum rate for the carboxylation activity of Rubisco VPD vapour pressure deficit WD water deficit WW well-watered α alpha β beta ∆Ha activation energy Γ* Gamma star δ13C carbon isotope discrimination iii iv LIST OF PUBLICATIONS DERIVED FROM THIS THESIS Perdomo JA, Conesa MÀ, Medrano H, Ribas-Carbó M, Galmés J (2014) Effects of long-term individual and combined water and temperature stress on the growth of rice, wheat and maize: relationship with morphological and physiological acclimation. Accepted on Physiologia Plantarum. Perdomo JA, Carmo-Silva E, Hermida C, Flexas J, Galmés J (2014) Biochemical and diffusive limitations to photosynthesis in rice, wheat and maize grown at high temperature and under water deficit. In preparation. Perdomo JA, Carmo-Silva E, Salvucci ME, Galmés J (2014) Rubisco and Rubisco activase play an important role in the biochemical limitations of photosynthesis in rice, wheat and maize under high temperature and water deficit. In preparation. Perdomo JA, Cavanagh AP, Kubien DS, Galmés J (2014) Temperature dependence of in vitro Rubisco kinetics in species of Flaveria with different photosynthetic mechanisms. Submitted to Photosynthesis Research (minor revisions). v vi CONTENTS SYMBOLS AND ABBREVIATIONS………………………………………………..…i LIST OF PUBLICATIONS DERIVED FROM THIS THESIS………………………...v CONTENTS……………………………………………………………………………vii ABSTRACT…………………………………………………………………………….xi RESUMEN…………………………………………………………………………….xiii Chapter 1. INTRODUCTION .................................................................... 1 1.1. Global climate change ............................................................................................... 2 1.2. Climate change repercussions in crop productivity ................................................... 6 1.3. High temperature and water deficit effects on photosynthesis ................................ 10 1.3.1. Effects of high temperature on photosynthesis..................................................... 11 1.3.2. Effects of water deficit on photosynthesis ............................................................ 14 1.3.3. Effects of varying temperature on Rubisco kinetics ............................................. 15 1.4. Effect of water deficit and high temperature on respiration, carbon balance and biomass allocation .......................................................................................................... 16 1.5. Plant acclimation or adaptation?.............................................................................. 18 1.6. Drought and heat stress combination....................................................................... 19 Chapter 2. OBJECTIVES AND OUTLINE ........................................... 23 2.1. GENERAL OBJETIVES ......................................................................................... 24 2.2. SPECIFIC OBJECTIVES ....................................................................................... 24 2.3. OUTLINE OF THE THESIS .................................................................................. 25 Chapter 3. PLANT GROWTH AND PHYSIOLOGICAL ACCLIMATION UNDER HIGH TEMPERATURE AND WATER DEFICIT ................................................................................................... 27 3.1. EFFECTS OF LONG-TERM INDIVIDUAL AND COMBINED WATER AND TEMPERATURE STRESS ON THE GROWTH OF RICE, WHEAT AND MAIZE: RELATIONSHIP WITH MORPHOLOGICAL AND PHYSIOLOGICAL ACCLIMATION ............................................................................................................ 28 vii Chapter 4. PHOTOSYNTHETIC LIMITATIONS UNDER THE INDIVIDUAL AND COMBINED EFFECTS OF HIGH TEMPERATURE AND WATER DEFICIT…………………………..67 4.1. BIOCHEMICAL AND DIFFUSIVE LIMITATIONS TO PHOTOSYNTHESIS IN RICE, WHEAT AND MAIZE GROWN AT HIGH TEMPERATURE AND UNDER WATER DEFICIT. ......................................................................................................... 69 Chapter 5. RUBISCO AND RUBISCO ACTIVASE PLAY AN IMPORTANT ROLE IN THE BIOCHEMICAL LIMITATIONS OF PHOTOSYNTHESIS IN RICE, WHEAT AND MAIZE UNDER HIGH TEMPERATURE AND WATER DEFICIT………………….109 5.1. RUBISCO AND RUBISCO ACTIVASE PLAY AN IMPORTANT ROLE IN THE BIOCHEMICAL LIMITATIONS OF PHOTOSYNTHESIS IN RICE, WHEAT AND MAIZE UNDER HIGH TEMPERATURE AND WATER DEFICIT ........................ 111 Chapter 6. TEMPERATURE DEPENDENCE OF RUBISCO KINETICS IN RELATED SPECIES OF FLAVERIA……………....143 6.1. TEMPERATURE DEPENDENCE OF IN VITRO RUBISCO KINETICS IN SPECIES OF FLAVERIA WITH DIFFERENT PHOTOSYNTHETIC MECHANISMS ...................................................................................................................................... 145 Chapter 7. GENERAL DISCUSSION………………………………...165 7.1. Effects of water deficit and high temperature: individual vs. combined stress on growth, physiological and biochemical processes ........................................................ 167 7.2. Effects of high temperature on photosynthetic parameters: short– vs. long–term exposition……………………………………………………………………………...171 7.2.1. Rubisco acclimation to high temperature and water deficit…………………....173 7.3. The role of Rubisco kinetics in photosynthesis modelling……………………….175 7.3.1. The importance to use the species–specific Rubisco kinetics in the biochemical models of photosynthesis………………………………………………………...……175 7.3.2. The importance to knowing the thermal dependence of Rubisco kinetic parameters for use on the photosynthesis models……………...……………………..178 viii Chapter 8. Conclusions…………….………………………………..…185 Chapter 9. Reference list………………..……………..……………….189 ix x ABSTRACT Global demand of agricultural crops for food, animal feeding and biofuel experienced a notorious increase through the last decades as a consequence of the human population rising. On the
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