High temperature enhances inhibitor production but reduces fallover in tobacco Rubisco
Stephen M. Schrader A D , Heather J. Kane B , Thomas D. Sharkey C and Susanne von Caemmerer BA Photosynthesis Research Unit, Agricultural Research Service, United States Department of Agriculture, 1201 W. Gregory Dr., Urbana, IL 61801, USA.
B Molecular Plant Physiology, Research School of Biological Sciences, Australian National University, GPO Box 475, Canberra, ACT 2601, Australia.
C Department of Botany, University of Wisconsin — Madison, 430 Lincoln Drive, Madison, WI 53706, USA.
D Corresponding author. Email: Schrader@uiuc.edu
Functional Plant Biology 33(10) 921-929 https://doi.org/10.1071/FP06059
Submitted: 20 March 2006 Accepted: 24 May 2006 Published: 2 October 2006
Abstract
High temperature inhibits photosynthesis by several mechanisms including reduction in Rubisco activity. While the initial reaction velocity of purified, fully carbamylated, inhibitor-free Rubisco increases with temperature in vitro, over time, the reaction velocity slowly declines (fallover) because of the enzymatic and non-enzymatic production of inhibitors from the substrate ribulose-1,5-bisphosphate. We tested whether fallover could contribute to the decline in Rubisco activity observed in leaf extracts at high temperature. Production of d-xylulose-1,5-bisphosphate (XuBP), an inhibitor of Rubisco, was greater at 35 and 45°C than at 25°C but fallover was less severe at 35 and 45°C than at 25°C, both in rate and extent under saturating CO2 and ambient O2. This apparent dichotomy is consistent with the catalytic site of Rubisco loosening at higher temperatures and releasing inhibitors more easily. The loosening of the catalytic site was supported by the observation that RuBP and XuBP were released from their complexes with uncarbamylated, Mg2+-free Rubisco faster at 35 and 45°C than at 25°C. We conclude that, although XuBP production increased relative to catalytic throughput at higher temperatures, this was more than compensated for by its faster release, resulting in less fallover inhibition at higher temperatures.
Keywords: fallover, heat stress, high temperature, Rubisco.
Acknowledgments
We thank Dr John Andrews for helpful advice and discussion during the course of this study. This work was supported by the USDA-CSREES, National Research Initiative grant no. 2004-35100-14860.
Andrews TJ, Hatch MD
(1969) Properties and mechanism of action of pyruvate, phosphate dikinase from leaves. The Biochemical Journal 114, 117–125.
| PubMed |
Andrews TJ, Kane HJ
(1991) Pyruvate is a by-product of catalysis by ribulosebisphosphate carboxylase oxygenase. Journal of Biological Chemistry 266, 9447–9452.
| PubMed |
Badger MR, Collatz GJ
(1977) Studies on the kinetic mechanism of ribulose-1,5-bisphosphate carboxylase and oxygenase reactions, with particular reference to the effect of temperature on the kinetic parameters. Carnegie Institute Washington Year Book 76, 355–361.
Berry JA, Björkman O
(1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491–543.
| Crossref | GoogleScholarGoogle Scholar |
Chen YR, Hartman FC
(1995) Signature of the oxygenase intermediate of Rubisco catalysis as provided by a novel product formed with a site-directed mutant. FASEB Journal 9, A1485.
Crafts-Brandner SJ, Salvucci ME
(2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proceedings of the National Academy of Sciences USA 97, 13 430–13 435.
| Crossref | GoogleScholarGoogle Scholar |
Duff AP,
Andrews TJ, Curmi PMG
(2000) The transition between the open and closed states of Rubisco is triggered by the inter-phosphate distance of the bound bisphosphate. Journal of Molecular Biology 298, 903–916.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eckardt NA, Portis AR
(1997) Heat denaturation profiles of ribulose-1,5-bisphosphate carboxylase / oxygenase (Rubisco) and Rubisco activase and the inability of Rubisco activase to restore activity of heat-denatured Rubisco. Plant Physiology 113, 243–248.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eckardt NA,
Snyder GW,
Portis AR, Ogren WL
(1997) Growth and photosynthesis under high and low irradiance of Arabidopsis thaliana antisense mutants with reduced ribulose-1,5-bisphosphate carboxylase / oxygenase activase content. Plant Physiology 113, 575–586.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Edmondson DL,
Badger MR, Andrews TJ
(1990a) A kinetic characterization of slow inactivation of ribulosebisphosphate carboxylase during catalysis. Plant Physiology 93, 1376–1382.
| PubMed |
Edmondson DL,
Badger MR, Andrews TJ
(1990b) Slow inactivation of ribulosebisphosphate carboxylase during catalysis is caused by accumulation of a slow, tight-binding inhibitor at the catalytic site. Plant Physiology 93, 1390–1397.
| PubMed |
Edmondson DL,
Badger MR, Andrews TJ
(1990c) Slow inactivation of ribulosebisphosphate carboxylase during catalysis is not due to decarbamylation of the catalytic site. Plant Physiology 93, 1383–1389.
| PubMed |
Edmondson DL,
Kane HJ, Andrews TJ
(1990d) Substrate isomerization inhibits ribulosebisphospate carboxylase–oxygenase during catalysis. FEBS Letters 260, 62–66.
| Crossref | GoogleScholarGoogle Scholar |
Galmes J,
Flexas J,
Keys AJ,
Cifre J,
Mitchell RAC,
Madgwick PJ,
Haslam RP,
Medrano H, Parry MAJ
(2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant, Cell & Environment 28, 571–579.
| Crossref | GoogleScholarGoogle Scholar |
Harpel MR,
Serpersu EH,
Lamerdin JA,
Huang ZH,
Gage DA, Hartman FC
(1995) Oxygenation mechanism of ribulose-bisphosphate carboxylase oxygenase. Structure and origin of 2-carboxytetritol 1,4-bisphosphate, a novel O2-dependent side product generated by a site-directed mutant. Biochemistry 34, 11296–11306.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jordan DB, Ogren WL
(1984) The CO2 / O2 specificity of ribulose 1,5-bisphosphate carboxylase / oxygenase. Dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161, 308–313.
| Crossref | GoogleScholarGoogle Scholar |
Kane HJ,
Wilkin JM,
Portis AR, Andrews TJ
(1998) Potent inhibition of ribulose-bisphosphate carboxylase by an oxidized impurity in ribulose-1,5-bisphosphate. Plant Physiology 117, 1059–1069.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kim K, Portis AR
(2004) Oxygen-dependent H2O2 production by Rubisco. FEBS Letters 571, 124–128.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kobza J, Edwards GE
(1987) Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiology 83, 69–74.
| PubMed |
Kung SD,
Chollet R, Marsho TV
(1980) Crystallization and assay procedures of tobacco ribulose-1,5-bisphosphate carboxylase-oxygenase. Methods in Enzymology 69, 326–336.
Law RD, Crafts-Brandner SJ
(1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase / oxygenase. Plant Physiology 120, 173–181.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mate CJ,
Hudson GS,
von Caemmerer S,
Evans JR, Andrews TJ
(1993) Reduction of ribulose-bisphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose-bisphosphate carboxylase carbamylation and impairs photosynthesis. Plant Physiology 102, 1119–1128.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mate CJ,
von Caemmerer S,
Evans JR,
Hudson GS, Andrews TJ
(1996) The relationship between CO2-assimilation rate, Rubisco carbamylation and Rubisco activase content in activase-deficient transgenic tobacco suggests a simple model of activase action. Planta 198, 604–613.
| Crossref | GoogleScholarGoogle Scholar |
Ogren WL
(1984) Photorespiration pathways, regulation, and modification. Annual Review of Plant Physiology 35, 415–442.
| Crossref | GoogleScholarGoogle Scholar |
Pearce FG, Andrews TJ
(2003) The relationship between side reactions and slow inhibition of ribulose-bisphosphate carboxylase revealed by a loop 6 mutant of the tobacco enzyme. Journal of Biological Chemistry 278, 32 526–32 536.
| Crossref | GoogleScholarGoogle Scholar |
Pierce J,
Tolbert NE, Barker R
(1980) Interaction of ribulosebisphosphate carboxylase–oxygenase with transition-state analogs. Biochemistry 19, 934–942.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Portis AR
(1992) Regulation of ribulose 1,5-bisphosphate carboxylase oxygenase activity. Annual Review of Plant Physiology and Plant Molecular Biology 43, 415–437.
| Crossref | GoogleScholarGoogle Scholar |
Portis AR
(2003) Rubisco activase — Rubisco’s catalytic chaperone. Photosynthesis Research 75, 11–27.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Robinson SP, Portis AR
(1988) Release of the nocturnal inhibitor, carboxyarabinitol-1-phosphate, from ribulose bisphosphate carboxylase oxygenase by Rubisco activase. FEBS Letters 233, 413–416.
| Crossref | GoogleScholarGoogle Scholar |
Robinson SP, Portis AR
(1989) Ribulose-1,5-bisphosphate carboxylase oxygenase activase protein prevents the in vitro decline in activity of ribulose-1,5-bisphosphate carboxylase oxygenase. Plant Physiology 90, 968–971.
| PubMed |
Sage RF
(2002) Variation in the k
(cat) of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. Journal of Experimental Botany 53, 609–620.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Salvucci ME, Crafts-Brandner SJ
(2004) Mechanism for deactivation of Rubisco under moderate heat stress. Physiologia Plantarum 122, 513–519.
| Crossref | GoogleScholarGoogle Scholar |
Salvucci ME,
Osteryoung KW,
Crafts-Brandner SJ, Vierling E
(2001) Exceptional sensitivity of rubisco activase to thermal denaturation in vitro and in vivo. Plant Physiology 127, 1053–1064.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Salvucci ME,
Portis AR, Ogren WL
(1985) A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase / oxygenase activation in vivo. Photosynthesis Research 7, 193–201.
| Crossref | GoogleScholarGoogle Scholar |
Schrader SM,
Wise RR,
Wacholtz WF,
Ort DR, Sharkey TD
(2004) Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant, Cell & Environment 27, 725–735.
| Crossref | GoogleScholarGoogle Scholar |
Servaites JC
(1985) Crystalline ribulose bisphosphate carboxylase / oxygenase of high integrity and catalytic activity from Nicotiana tabacum. Archives of Biochemistry and Biophysics 238, 154–160.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sharkey TD,
Badger MR,
von Caemmerer S, Andrews TJ
(2001) Increased heat sensitivity of photosynthesis in tobacco plants with reduced Rubisco activase. Photosynthesis Research 67, 147–156.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wang ZY, Portis AR
(1992) Dissociation of ribulose-1,5-bisphosphate bound to ribulose-1,5-bisphosphate carboxylase oxygenase and its enhancement by ribulose-1,5-bisphosphate carboxylase oxygenase activase-mediated hydrolysis of ATP. Plant Physiology 99, 1348–1353.
| PubMed |
Wang ZY,
Snyder GW,
Esau BD,
Portis AR, Ogren WL
(1992) Species-dependent variation in the interaction of substrate-bound ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco) and Rubisco activase. Plant Physiology 100, 1858–1862.
| PubMed |
Whitney SM,
von Caemmerer S,
Hudson GS, Andrews TJ
(1999) Directed mutation of the Rubisco large subunit of tobacco influences photorespiration and growth. Plant Physiology 121, 579–588.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhu GH,
Bohnert HJ,
Jensen RG, Wildner GF
(1998) Formation of the tight-binding inhibitor, 3-ketoarabinitol-1,5-bisphosphate by ribulose-1,5-bisphosphate carboxylase / oxygenase is O2-dependent. Photosynthesis Research 55, 67–74.
| Crossref | GoogleScholarGoogle Scholar |
Zhu GH, Jensen RG
(1991a) Fallover of ribulose 1,5-bisphosphate carboxylase oxygenase activity — decarbamylation of catalytic sites depends on pH. Plant Physiology 97, 1354–1358.
| PubMed |
Zhu GH, Jensen RG
(1991b) Xylulose 1,5-bisphosphate synthesized by ribulose 1,5-bisphosphate carboxylase oxygenase during catalysis binds to decarbamylated enzyme. Plant Physiology 97, 1348–1353.
| PubMed |
