Rubisco activity is associated with photosynthetic thermotolerance in a wild rice (Oryza meridionalis).

Oryza meridionalis is a wild species of rice, endemic to tropical Australia. It shares a significant genome homology with the common domesticated rice Oryza sativa. Exploiting the fact that the two species are highly related but O. meridionalis has superior heat tolerance, experiments were undertaken to identify the impact of temperature on key events in photosynthesis. At an ambient CO(2) partial pressure of 38 Pa and irradiance of 1500 µmol quanta m(-2) s(-1), the temperature optimum of photosynthesis was 33.7 ± 0.8°C for O. meridionalis, significantly higher than the 30.6 ± 0.7°C temperature optimum of O. sativa. To understand the basis for this difference, we measured gas exchange and rubisco activation state between 20 and 42°C and modeled the response to determine the rate-limiting steps of photosynthesis. The temperature response of light respiration (R(light)) and the CO(2) compensation point in the absence of respiration (Γ(*)) were determined and found to be similar for the two species. C3 photosynthesis modeling showed that despite the difference in susceptibility to high temperature, both species had a similar temperature-dependent limitation to photosynthesis. Both rice species were limited by ribulose-1,5-bisphosphate (RuBP) regeneration at temperatures of 25 and 30°C but became RuBP carboxylation limited at 35 and 40°C. The activation state of rubisco in O. meridionalis was more stable at higher temperatures, explaining its greater heat tolerance compared with O. sativa.

[1]  J. R. Evans,et al.  Temperature response of mesophyll conductance in cultivated and wild Oryza species with contrasting mesophyll cell wall thickness. , 2011, Plant, cell & environment.

[2]  Wataru Yamori,et al.  The rate-limiting step for CO(2) assimilation at different temperatures is influenced by the leaf nitrogen content in several C(3) crop species. , 2011, Plant, cell & environment.

[3]  Csengele Barta,et al.  Rubisco activase activity assays. , 2011, Methods in molecular biology.

[4]  M. Badger,et al.  The Roles of ATP Synthase and the Cytochrome b6/f Complexes in Limiting Chloroplast Electron Transport and Determining Photosynthetic Capacity1[W][OA] , 2010, Plant Physiology.

[5]  J. R. Evans,et al.  Effects of growth and measurement light intensities on temperature dependence of CO(2) assimilation rate in tobacco leaves. , 2010, Plant, cell & environment.

[6]  P. Haynes,et al.  Physiological and molecular changes in Oryza meridionalis Ng., a heat-tolerant species of wild rice. , 2010, Journal of experimental botany.

[7]  R. Wing,et al.  Australian Oryza: Utility and Conservation , 2010, Rice.

[8]  K. Hikosaka,et al.  Phenotypic Plasticity in Photosynthetic Temperature Acclimation among Crop Species with Different Cold Tolerances1[W][OA] , 2009, Plant Physiology.

[9]  Jaume Flexas,et al.  Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations. , 2009, Journal of experimental botany.

[10]  Shiwei Guo,et al.  Light-saturated photosynthetic rate in high-nitrogen rice (Oryza sativa L.) leaves is related to chloroplastic CO2 concentration. , 2009, Journal of experimental botany.

[11]  R. Sage,et al.  Rubisco, Rubisco activase, and global climate change. , 2008, Journal of experimental botany.

[12]  M. Salvucci,et al.  Association of Rubisco activase with chaperonin-60beta: a possible mechanism for protecting photosynthesis during heat stress. , 2007, Journal of experimental botany.

[13]  R. Sage,et al.  Temperature response of photosynthesis in transgenic rice transformed with 'sense' or 'antisense' rbcS. , 2007, Plant & cell physiology.

[14]  T. Sharkey,et al.  Fitting photosynthetic carbon dioxide response curves for C(3) leaves. , 2007, Plant, cell & environment.

[15]  S. Mccouch,et al.  The Complex History of the Domestication of Rice , 2007, Annals of botany.

[16]  B. Lu,et al.  Phylogenetic Analysis of AA-genome Oryza Species (Poaceae) Based on Chloroplast, Mitochondrial, and Nuclear DNA Sequences , 2007, Biochemical Genetics.

[17]  J. Flexas,et al.  Acclimation of Rubisco specificity factor to drought in tobacco: discrepancies between in vitro and in vivo estimations. , 2006, Journal of experimental botany.

[18]  K. Noguchi,et al.  Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. , 2006, Plant, cell & environment.

[19]  T. Pons,et al.  High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric , 2006 .

[20]  K. Hikosaka,et al.  Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. , 2006, Journal of experimental botany.

[21]  Y. Cen,et al.  The Regulation of Rubisco Activity in Response to Variation in Temperature and Atmospheric CO2 Partial Pressure in Sweet Potato1[w] , 2005, Plant Physiology.

[22]  J. Flexas,et al.  Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves , 2005 .

[23]  Mark G Tjoelker,et al.  The hot and the cold: unravelling the variable response of plant respiration to temperature. , 2005, Functional plant biology : FPB.

[24]  Thomas D. Sharkey,et al.  Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene , 2005 .

[25]  K. Hikosaka,et al.  Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum. , 2005, Journal of experimental botany.

[26]  R. Bligny,et al.  In Vivo Respiratory Metabolism of Illuminated Leaves , 2005 .

[27]  T. Nishikawa,et al.  Phylogenetic analysis of Oryza species, based on simple sequence repeats and their flanking nucleotide sequences from the mitochondrial and chloroplast genomes , 2005, Theoretical and Applied Genetics.

[28]  Stephen M. Schrader,et al.  Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature , 2004 .

[29]  Michael E. Salvucci,et al.  Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. , 2004, Physiologia plantarum.

[30]  John R. Evans,et al.  The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco , 1994, Planta.

[31]  G. Farquhar,et al.  Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light , 1985, Planta.

[32]  G. Farquhar,et al.  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves , 1981, Planta.

[33]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[34]  Y. Cen,et al.  The activation state of Rubisco directly limits photosynthesis at low CO2 and low O2 partial pressures , 2004, Photosynthesis Research.

[35]  M. Peisker,et al.  Inhibition by light of CO2 evolution from dark respiration: Comparison of two gas exchange methods , 2004, Photosynthesis Research.

[36]  S. Long,et al.  Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. , 2003, Journal of experimental botany.

[37]  F. Loreto,et al.  12CO2 emission from different metabolic pathways measured in illuminated and darkened C3 and C4 leaves at low, atmospheric and elevated CO2 concentration. , 2003, Journal of experimental botany.

[38]  Susanne von Caemmerer,et al.  Temperature Response of Mesophyll Conductance. Implications for the Determination of Rubisco Enzyme Kinetics and for Limitations to Photosynthesis in Vivo , 2002, Plant Physiology.

[39]  M. Salvucci,et al.  Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. , 2002, Annual review of plant biology.

[40]  Carl J. Bernacchi,et al.  Improved temperature response functions for models of Rubisco‐limited photosynthesis , 2001 .

[41]  S. Crafts-Brandner,et al.  Effect of heat stress on the inhibition and recovery of the ribulose-1,5-bisphosphate carboxylase/oxygenase activation state , 2000, Planta.

[42]  M. Salvucci,et al.  Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[43]  S. V. Caemmerer,et al.  Biochemical models of leaf photosynthesis. , 2000 .

[44]  T. Sang,et al.  Phylogeny of rice genomes with emphasis on origins of allotetraploid species. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[45]  K. Hikosaka,et al.  Balancing carboxylation and regeneration of ribulose‐1,5‐ bisphosphate in leaf photosynthesis: temperature acclimation of an evergreen tree, Quercus myrsinaefolia , 1999 .

[46]  S. Crafts-Brandner,et al.  Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate Carboxylase/Oxygenase , 1999, Plant physiology.

[47]  A. Chowdhury,et al.  Ischaemum rugosum - a potential alternate host of rice tungro viruses in West Bengal. , 1999 .

[48]  Murray R. Badger,et al.  The interplay between limiting processes in C3 photosynthesis studied by rapid-response gas exchange using transgenic tobacco impaired in photosynthesis , 1998 .

[49]  M. Havaux,et al.  Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of the xanthophyll content , 1996 .

[50]  A. Makino,et al.  Effects of Growth Temperature on the Responses of Ribulose-1,5-Biphosphate Carboxylase, Electron Transport Components, and Sucrose Synthesis Enzymes to Leaf Nitrogen in Rice, and Their Relationships to Photosynthesis , 1994, Plant physiology.

[51]  R. J. Porra,et al.  Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy , 1989 .

[52]  P. Quinn,et al.  Structural reorganisation of chloroplast thylakoid membranes in response to heat-stress , 1984 .

[53]  D. Jordan,et al.  The CO2/O 2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase : Dependence on ribulosebisphosphate concentration, pH and temperature. , 1984, Planta.

[54]  J. T. Williams,et al.  The recognition of a new species of rice (Oryza) from Australia , 1981 .

[55]  J. Berry,et al.  Photosynthetic Response and Adaptation to Temperature in Higher Plants , 1980 .

[56]  L. Staehelin,et al.  Dissociation of supramolecular complexes in chloroplast membranes. A manifestation of heat damage to the photosynthetic apparatus. , 1980, Biochimica et biophysica acta.