Log in

Regulation of Calvin–Benson cycle enzymes under high temperature stress

  • Review
  • Published:
aBIOTECH Aims and scope Submit manuscript

Abstract

The Calvin–Benson cycle (CBC) consists of three critical processes, including fixation of CO2 by Rubisco, reduction of 3-phosphoglycerate (3PGA) to triose phosphate (triose-P) with NADPH and ATP generated by the light reactions, and regeneration of ribulose 1,5-bisphosphate (RuBP) from triose-P. The activities of photosynthesis-related proteins, mainly from the CBC, were found more significantly affected and regulated in plants challenged with high temperature stress, including Rubisco, Rubisco activase (RCA) and the enzymes involved in RuBP regeneration, such as sedoheptulose-1,7-bisphosphatase (SBPase). Over the past years, the regulatory mechanism of CBC, especially for redox-regulation, has attracted major interest, because balancing flux at the various enzymatic reactions and maintaining metabolite levels in a range are of critical importance for the optimal operation of CBC under high temperature stress, providing insights into the genetic manipulation of photosynthesis. Here, we summarize recent progress regarding the identification of various layers of regulation point to the key enzymes of CBC for acclimation to environmental temperature changes along with open questions are also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Spain)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmad N, Zaidi SS-E-A, Mansoor S (2020) Alternative routes to improving photosynthesis in field crops. Trends Plant Sci 25(10):958–960

    Article  CAS  Google Scholar 

  • Ainsworth EA, Ort DR (2010) How do we improve crop production in a warming world? Plant Physiol 154(2):526–530

    Article  CAS  Google Scholar 

  • Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp PCC 6803. BBA-Bioenerg 1657(1):23–32

    Article  CAS  Google Scholar 

  • Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R et al (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98(1–3):541–550

    Article  CAS  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141(2):391–396

    Article  CAS  Google Scholar 

  • Bhat JY, Thieulin-Pardo G, Hartl FU, Hayer-Hartl M (2017) Rubisco activases: AAA plus chaperones adapted to enzyme repair. Front Mol Biosci 4:20. https://doi.org/10.3389/fmolb.2017.00020

    Article  CAS  Google Scholar 

  • Bracher A, Whitney SM, Hartl FU, Hayer-Hartl M (2017) Biogenesis and metabolic maintenance of Rubisco. Annu Rev Plant Biol 68:29–60

    Article  CAS  Google Scholar 

  • Buchanan BB (2016) The path to thioredoxin and redox regulation in chloroplasts. Annu Rev Plant Biol 67:1–24

    Article  CAS  Google Scholar 

  • Busch FA, Tominaga J, Muroya M, Shirakami N, Takahashi S et al (2020) Overexpression of bundle sheath defective 2 improves the efficiency of photosynthesis and growth in Arabidopsis. Plant J 102(1):129–137

    Article  CAS  Google Scholar 

  • Carmo-Silva AE, Salvucci ME (2011) The activity of Rubisco’s molecular chaperone, Rubisco activase, in leaf extracts. Photosynth Res 108(2–3):143–155

    Article  CAS  Google Scholar 

  • Carmo-Silva AE, Gore MA, Andrade-Sanchez P, French AN, Hunsaker DJ et al (2012) Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environ Exp Bot 83:1–11

    Article  CAS  Google Scholar 

  • Castro-Nava S, Lopez-Rubio E (2019) Thermotolerance and physiological traits as fast tools to heat tolerance selection in experimental sugarcane genotypes. Agriculture-Basel 9(12):251

    Article  CAS  Google Scholar 

  • Chaurasia SP, Deswal R (2017) Identification and in silico analysis of major redox modulated proteins from Brassica juncea seedlings using 2D redox SDS page (2-dimensional diagonal redox sodium dodecyl sulfate polyacrylamide gel electrophoresis). Protein J 36(1):64–76

    Article  CAS  Google Scholar 

  • Chen J-H, Chen S-T, He N-Y, Wang Q-L, Zhao Y et al (2020) Nuclear-encoded synthesis of the D1 subunit of photosystem II increases photosynthetic efficiency and crop yield. Nat Plants 6(5):570

    Article  CAS  Google Scholar 

  • Crafts-Brandner SJ, Law RD (2000) Effect of heat stress on the inhibition and recovery of the ribulose-1,5-bisphosphate carboxylase/oxygenase activation state. Planta 212(1):67–74

    Article  CAS  Google Scholar 

  • Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97(24):13430–13435

    Article  CAS  Google Scholar 

  • Degen GE, Orr DJ, Carmo-Silva E (2021) Heat-induced changes in the abundance of wheat Rubisco activase isoforms. New Phytol 229(3):1298–1311

    Article  CAS  Google Scholar 

  • Driever SM, Simkin AJ, Alotaibi S, Fisk SJ, Madgwick PJ et al (2017) Increased SBPase activity improves photosynthesis and grain yield in wheat grown in greenhouse conditions. Philos Transact R Soc B-Biol Sci 372(1730):20160384

    Article  Google Scholar 

  • Dunford RP, Durrant MC, Catley MA, Dyer TA (1998) Location of the redox-active cysteines in chloroplast sedoheptulose-1,7-bisphosphatase indicates that its allosteric regulation is similar but not identical to that of fructose-1,6-bisphosphatase. Photosynth Res 58(3):221–230

    Article  CAS  Google Scholar 

  • Feng L, Wang K, Li Y, Tan Y, Kong J et al (2007) Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Rep 26(9):1635–1646

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2013) Redox signaling in plants. Antioxid Redox Signal 18(16):2087–2090

    Article  CAS  Google Scholar 

  • Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717

    Article  CAS  Google Scholar 

  • Fukayama H, Ueguchi C, Nishikawa K, Katoh N, Ishikawa C et al (2012) Overexpression of rubisco activase decreases the photosynthetic CO2 assimilation rate by reducing rubisco content in rice leaves. Plant Cell Physiol 53(6):976–986

    Article  CAS  Google Scholar 

  • Fukayama H, Mizumoto A, Ueguchi C, Katsunuma J, Morita R et al (2018) Expression level of Rubisco activase negatively correlates with Rubisco content in transgenic rice. Photosynth Res 137(3):465–474

    Article  CAS  Google Scholar 

  • Garciaferris C, Moreno J (1994) Oxidative modification and breakdown of Ribulose-1,5-Bisphosphate carboxylase oxygenase induced in Euglena-Gracilis by nitrogen starvation. Planta 193(2):208–215

    CAS  Google Scholar 

  • Gurrieri L, Fermani S, Zaffagnini M, Sparla F, Trost P (2021) Calvin–Benson cycle regulation is getting complex. Trends Plant Sci 26(9):898–912

    Article  CAS  Google Scholar 

  • Gururani MA, Venkatesh J, Lam-Son Phan T (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8(9):1304–1320

    Article  CAS  Google Scholar 

  • Gutle DD, Roret T, Muller SJ, Couturier J, Lemaire SD et al (2016) Chloroplast FBPase and SBPase are thioredoxin-linked enzymes with similar architecture but different evolutionary histories. Proc Natl Acad Sci USA 113(24):6779–6784

    Article  Google Scholar 

  • Hagemann M, Bauwe H (2016) Photorespiration and the potential to improve photosynthesis. Curr Opin Chem Biol 35:109–116

    Article  CAS  Google Scholar 

  • Harrison EP, Willingham NM, Lloyd JC, Raines CA (1998) Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204(1):27–36

    Article  CAS  Google Scholar 

  • Hatfield JL, Dold C (2018) Agroclimatology and wheat production: co** with climate change. Front Plant Sci 9:224

    Article  Google Scholar 

  • Hayer-Hartl M, Hartl FU (2020) Chaperone machineries of Rubisco—the most abundant enzyme. Trends Biochem Sci 45(9):748–763

    Article  CAS  Google Scholar 

  • Hildebrandt T, Knuesting J, Berndt C, Morgan B, Scheibe R (2015) Cytosolic thiol switches regulating basic cellular functions: GAPDH as an information hub? Biol Chem 396(5):523–537

    Article  CAS  Google Scholar 

  • Hussain S, Ulhassan Z, Brestic M, Zivcak M, Zhou W et al (2021) Photosynthesis research under climate change. Photosynthesis Res 150:5–19

    Article  CAS  Google Scholar 

  • Jesus Garcia-Murria M, Sudhani HPK, Marin-Navarro J, Sanchez del Pino MM, Moreno J (2018) Dissecting the individual contribution of conserved cysteines to the redox regulation of RubisCO. Photosynth Res 137(2):251–262

    Article  Google Scholar 

  • Kim K, Portis AR (2005) Temperature dependence of photosynthesis in Arabidopsis plants with modifications in Rubisco activase and membrane fluidity. Plant Cell Physiol 46(3):522–530

    Article  CAS  Google Scholar 

  • Kim S-C, Guo L, Wang X (2020) Nuclear moonlighting of cytosolic glyceraldehyde-3-phosphate dehydrogenase regulates Arabidopsis response to heat stress. Nat Commun 11(1):3439

    Article  CAS  Google Scholar 

  • Kim SY, Slattery RA, Ort DR (2021) A role for differential Rubisco activase isoform expression in C-4 bioenergy grasses at high temperature. Glob Change Biol Bioenerg 13(1):211–223

    Article  CAS  Google Scholar 

  • Kohler IH, Ruiz-Vera UM, VanLoocke A, Thomey ML, Clemente T et al (2017) Expression of cyanobacterial FBP/SBPase in soybean prevents yield depression under future climate conditions. J Exp Bot 68(3):715–726

    Google Scholar 

  • Kudo N, Mano K, Suganami M, Kondo E, Suzuki Y et al (2020) Effects of overexpression of the Rubisco small subunit gene under the control of the Rubisco activase promoter on Rubisco contents of rice leaves at different positions. Soil Sci Plant Nutr 66(4):569–578

    Article  CAS  Google Scholar 

  • Kumar A, Li C, Portis AR Jr (2009) Arabidopsis thaliana expressing a thermostable chimeric Rubisco activase exhibits enhanced growth and higher rates of photosynthesis at moderately high temperatures. Photosynth Res 100(3):143–153

    Article  CAS  Google Scholar 

  • Kumar RR, Goswami S, Shamim M, Mishra U, Jain M et al (2016) Biochemical defense response: characterizing the plasticity of source and sink in spring wheat under terminal heat stress. Front Plant Sci 8:986

    Google Scholar 

  • Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L et al (2007) Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19(10):3230–3241

    Article  CAS  Google Scholar 

  • Law RD, Crafts-Brandner SJ, Salvucci ME (2001) Heat stress induces the synthesis of a new form of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in cotton leaves. Planta 214(1):117–125

    Article  CAS  Google Scholar 

  • Lee D-G, Ahsan N, Lee S-H, Kang KY, Bahk JD et al (2007) A proteomic approach in analyzing heat-responsive proteins in rice leaves. Proteomics 7(18):3369–3383

    Article  CAS  Google Scholar 

  • Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138(1):451–460

    Article  CAS  Google Scholar 

  • Liu X-L, Yu H-D, Guan Y, Li J-K, Guo F-Q (2012) Carbonylation and loss-of-function analyses of SBPase reveal its metabolic interface role in oxidative stress, carbon assimilation, and multiple aspects of growth and development in Arabidopsis. Mol Plant 5(5):1082–1099

    Article  CAS  Google Scholar 

  • Lobell DB, Asner GP (2003) Climate and management contributions to recent trends in US agricultural yields. Science 299(5609):1032–1032

    Article  CAS  Google Scholar 

  • Long SP, Ort DR (2010) More than taking the heat: crops and global change. Curr Opin Plant Biol 13(3):241–248

    Article  Google Scholar 

  • Long SP, Zhu XG, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant, Cell Environ 29(3):315–330

    Article  CAS  Google Scholar 

  • Long SP, Marshall-Colon A, Zhu X-G (2015) Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell 161(1):56–66

    Article  CAS  Google Scholar 

  • Marin-Navarro J, Moreno J (2006) Cysteines 449 and 459 modulate the reduction-oxidation conformational changes of ribulose 1.5-bisphosphate carboxylase/oxygenase and the translocation of the enzyme to membranes during stress. Plant Cell Environ 29(5):898–908

    Article  CAS  Google Scholar 

  • Martre P, Wallach D, Asseng S, Ewert F, Jones JW et al (2015) Multimodel ensembles of wheat growth: many models are better than one. Glob Change Biol 21(2):911–925

    Article  Google Scholar 

  • Michelet L, Zaffagnini M, Morisse S, Sparla F, Perez-Perez ME et al (2013) Redox regulation of the Calvin-Benson cycle: something old, something new. Front Plant Sci 4:470

    Article  Google Scholar 

  • Mohanty P, Kreslavski VD, Klimov VV, Los DA, Mimuro M et al (2012) Heat stress: susceptibility, recovery and regulation. Photosynthesis: plastid biology, energy conversion and carbon assimilation. pp. 251–274.

  • Moore CE, Meacham-Hensold K, Lemonnier P, Slattery RA, Benjamin C et al (2021) The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. J Exp Bot 72(8):2822–2844

    Article  CAS  Google Scholar 

  • Moreno J, Penarrubia L, Garciaferris C (1995) The mechanism of redox regulation of Ribulose-1,5-Bisphosphate carboxylase oxygenase turnover—a hypothesis. Plant Physiol Biochem 33(1):121–127

    CAS  Google Scholar 

  • Moreno J, Jesus Garcia-Murria M, Marin-Navarro J (2008) Redox modulation of Rubisco conformation and activity through its cysteine residues. J Exp Bot 59(7):1605–1614

    Article  CAS  Google Scholar 

  • Mueller-Cajar O (2017) The diverse AAA plus machines that repair inhibited Rubisco active sites. Front Mol Biosci 4:31

    Article  Google Scholar 

  • Mueller-Cajar O, Stotz M, Bracher A (2014) Maintaining photosynthetic CO2 fixation via protein remodelling: the Rubisco activases. Photosynth Res 119(1–2):191–201

    Article  CAS  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. BBA-Bioenerg 1767(6):414–421

    Article  CAS  Google Scholar 

  • Muthuramalingam M, Matros A, Scheibe R, Mock H-P, Dietz K-J (2013) The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Front Plant Sci 4:54

    Article  Google Scholar 

  • Nikkanen L, Rintamaki E (2019) Chloroplast thioredoxin systems dynamically regulate photosynthesis in plants. Biochem J 476:1159–1172

    Article  CAS  Google Scholar 

  • Nikkanen L, Toivola J, Diaz MG, Rintamaki E (2017) Chloroplast thioredoxin systems: prospects for improving photosynthesis. Philos Transact R Soc B 372(1730):20160474

    Article  Google Scholar 

  • Nishiyama Y (2020) Resilience under climate change. Nat Plants 6(5):442–443

    Article  Google Scholar 

  • Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A et al (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20(20):5587–5594

    Article  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp PCC 6803. Biochemistry 43(35):11321–11330

    Article  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142(1):35–46

    Article  CAS  Google Scholar 

  • Ogbaga CC, Stepien P, Athar H-U-R, Ashraf M (2018) Engineering Rubisco activase from thermophilic cyanobacteria into high-temperature sensitive plants. Crit Rev Biotechnol 38(4):559–572

    Article  CAS  Google Scholar 

  • Osei-Bonsu I, McClain AM, Walker BJ, Sharkey TD, Kramer DM (2021) The roles of photorespiration and alternative electron acceptors in the responses of photosynthesis to elevated temperatures in cowpea. Plant Cell Environ 44(7):2290–2307

    Article  CAS  Google Scholar 

  • Parry MAJ, Andralojc PJ, Scales JC, Salvucci ME, Carmo-Silva AE et al (2013) Rubisco activity and regulation as targets for crop improvement. J Exp Bot 64(3):717–730

    Article  CAS  Google Scholar 

  • Portis AR (2003) Rubisco activase—Rubisco’s catalytic chaperone. Photosynth Res 75(1):11–27

    Article  CAS  Google Scholar 

  • Portis AR Jr, Li C, Wang D, Salvucci ME (2008) Regulation of Rubisco activase and its interaction with Rubisco. J Exp Bot 59(7):1597–1604

    Article  CAS  Google Scholar 

  • Raines CA (2003) The Calvin cycle revisited. Photosynth Res 75(1):1–10

    Article  CAS  Google Scholar 

  • Raines CA, Lloyd JC, Dyer TA (1999) New insights into the structure and function of sedoheptulose-1,7-bisphosphatase; an important but neglected Calvin cycle enzyme. J Exp Bot 50(330):1–8

    CAS  Google Scholar 

  • Raines CA, Harrison EP, Olcer H, Lloyd JC (2000) Investigating the role of the thiol-regulated enzyme sedoheptulose-1,7-bisphosphatase in the control of photosynthesis. Physiol Plant 110(3):303–308

    Article  CAS  Google Scholar 

  • Rodermel S, Haley J, Jiang CZ, Tsai CH, Bogorad L (1996) A mechanism for intergenomic integration: Abundance of Ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA. Proc Natl Acad Sci USA 93(9):3881–3885

    Article  CAS  Google Scholar 

  • Rosenthal DM, Locke AM, Khozaei M, Raines CA, Long SP et al (2011) Over-expressing the C-3 photosynthesis cycle enzyme sedoheptulose-1–7 bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO2 fumigation (FACE). BMC Plant Biol 11:123

    Article  CAS  Google Scholar 

  • Sage RF, Way DA, Kubien DS (2008) Rubisco, Rubisco activase, and global climate change. J Exp Bot 59(7):1581–1595

    Article  CAS  Google Scholar 

  • Salvucci ME, Crafts-Brandner SJ (2004a) Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiol 134(4):1460–1470

    Article  CAS  Google Scholar 

  • Salvucci ME, Crafts-Brandner SJ (2004b) Mechanism for deactivation of Rubisco under moderate heat stress. Physiol Plant 122(4):513–519

    Article  CAS  Google Scholar 

  • Salvucci ME, Crafts-Brandner SJ (2004c) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120(2):179–186

    Article  CAS  Google Scholar 

  • Scafaro AP, Yamori W, Carmo-Silva AE, Salvucci ME, von Caemmerer S et al (2012) Rubisco activity is associated with photosynthetic thermotolerance in a wild rice (Oryza meridionalis). Physiol Plant 146(1):99–109

    Article  CAS  Google Scholar 

  • Scafaro AP, Atwell BJ, Muylaert S, Van Reusel B, Ruiz GA et al (2018) A thermotolerant variant of Rubisco activase from a wild relative improves growth and seed yield in rice under heat stress. Front Plant Sci 9:1663

    Article  Google Scholar 

  • Scafaro AP, Bautsoens N, den Boer B, Van Rie J, Galle A (2019) A conserved sequence from heat-adapted species improves Rubisco activase thermostability in wheat. Plant Physiol 181(1):43–54

    Article  CAS  Google Scholar 

  • Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ 28(3):269–277

    Article  CAS  Google Scholar 

  • Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. J Integr Plant Biol 52(8):712–722

    Article  CAS  Google Scholar 

  • Sharkey TD, Badger MR, von Caemmerer S, Andrews TJ (2001) Increased heat sensitivity of photosynthesis in tobacco plants with reduced Rubisco activase. Photosynth Res 67(1–2):147–156

    Article  CAS  Google Scholar 

  • Sharmin SA, Alam I, Rahman MA, Kim K-H, Kim Y-G et al (2013) Map** the leaf proteome of Miscanthus sinensis and its application to the identification of heat-responsive proteins. Planta 238(3):459–474

    Article  CAS  Google Scholar 

  • Simkin AJ, Lopez-Calcagno PE, Davey PA, Headland LR, Lawson T et al (2017) Simultaneous stimulation of sedoheptulose 1,7-bisphosphatase, fructose 1,6-bisphophate aldolase and the photorespiratory glycine decarboxylase-H protein increases CO2 assimilation, vegetative biomass and seed yield in Arabidopsis. Plant Biotechnol J 15(7):805–816

    Article  CAS  Google Scholar 

  • Slattery RA, Ort DR (2019) Carbon assimilation in crops at high temperatures. Plant Cell Environ 42(10):2750–2758

    Article  CAS  Google Scholar 

  • Stirbet A, Lazar D, Guo Y, Govindjee G (2020) Photosynthesis: basics, history and modelling. Ann Bot 126(4):511–537

    Article  CAS  Google Scholar 

  • Stotz M, Mueller-Cajar O, Ciniawsky S, Wendler P, Hartl FU et al (2011) Structure of green-type Rubisco activase from tobacco. Nat Struct Mol Biol 18(12):1366-U1378

    Article  CAS  Google Scholar 

  • Suganami M, Suzuki Y, Sato T, Makino A (2018) Relationship between Rubisco activase and Rubisco contents in transgenic rice plants with overproduced or decreased Rubisco content. Soil Sci Plant Nutr 64(3):352–359

    Article  CAS  Google Scholar 

  • Suganami M, Suzuki Y, Tazoe Y, Yamori W, Makino A (2021) Co-overproducing Rubisco and Rubisco activase enhances photosynthesis in the optimal temperature range in rice. Plant Physiol 185(1):108–119

    CAS  Google Scholar 

  • Sun A-Z, Guo F-Q (2016) Chloroplast retrograde regulation of heat stress responses in plants. Front Plant Sci 7:398

    Article  Google Scholar 

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13(4):178–182

    Article  CAS  Google Scholar 

  • Tian Z, Wang J-W, Li J, Han B (2021) Designing future crops: challenges and strategies for sustainable agriculture. Plant J 105(5):1165–1178

    Article  CAS  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Wang Q-L, Chen J-H, He N-Y, Guo F-Q (2018) Metabolic reprogramming in chloroplasts under heat stress in plants. Int J Mol Sci 19(3):849

    Article  Google Scholar 

  • Way DA, Yamori W (2014) Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration. Photosynth Res 119(1–2):89–100

    Article  CAS  Google Scholar 

  • Wilson RH, Hayer-Hartl M (2018) Complex chaperone dependence of Rubisco biogenesis. Biochemistry 57(23):3210–3216

    Article  CAS  Google Scholar 

  • Wu L, Han L, Li Q, Wang G, Zhang H et al (2021) Using interactome big data to crack genetic mysteries and enhance future crop breeding. Mol Plant 14(1):77–94

    Article  CAS  Google Scholar 

  • Xu C, Huang B (2010) Differential proteomic response to heat stress in thermal Agrostis scabra and heat-sensitive Agrostis stolonifera. Physiol Plant 139(2):192–204

    Article  CAS  Google Scholar 

  • Xu C, Huang B (2012) Comparative analysis of proteomic responses to single and simultaneous drought and heat stress for two kentucky bluegrass cultivars. Crop Sci 52(3):1246–1260

    Article  CAS  Google Scholar 

  • Yamori W, Masumoto C, Fukayama H, Makino A (2012) Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and to a lesser extent, of steady-state photosynthesis at high temperature. Plant J 71(6):871–880

    Article  CAS  Google Scholar 

  • Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C-3, C-4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119(1–2):101–117

    Article  CAS  Google Scholar 

  • Yang SS, Zhai QH (2017) Cytosolic GAPDH: a key mediator in redox signal transduction in plants. Biol Plant 61(3):417–426

    Article  CAS  Google Scholar 

  • Yoshida K, Hara S, Hisabori T (2015) Thioredoxin selectivity for thiol-based redox regulation of target proteins in chloroplasts. J Biol Chem 290(23):14278–14288

    Article  CAS  Google Scholar 

  • Zaffagnini M, Fermani S, Costa A, Lemaire SD, Trost P (2013) Plant cytoplasmic GAPDH: redox post-translational modifications and moonlighting properties. Front Plant Sci 4:450

    Article  Google Scholar 

  • Zhang N, Portis AR (1999) Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci USA 96(16):9438–9443

    Article  CAS  Google Scholar 

  • Zhang R, Sharkey TD (2009) Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth Res 100(1):29–43

    Article  CAS  Google Scholar 

  • Zhang N, Kallis RP, Ewy RG, Portis AR (2002) Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proc Natl Acad Sci USA 99(5):3330–3334

    Article  CAS  Google Scholar 

  • Zhu X-G, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotechnol 19(2):153–159

    Article  CAS  Google Scholar 

  • Zhu X-G, Long SP, Ort DR (2010) Improving Photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by grants from the Ministry of Science and Technology of China (National Key R&D Program of China, 2020YFA0907604), the National Natural Science Foundation of China (U1812401, 31770314, 32000211 and 31600225), Science and Technology Commission of Shanghai Municipality (19ZR1466100) and the Chinese Academy of Sciences (The Strategic Priority Research Program, XDB27040105).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yin Yi or Fang-Qing Guo.

Ethics declarations

Conflict of interest

No potential conflict of interest was disclosed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, JH., Tang, M., **, XQ. et al. Regulation of Calvin–Benson cycle enzymes under high temperature stress. aBIOTECH 3, 65–77 (2022). https://doi.org/10.1007/s42994-022-00068-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42994-022-00068-3

Keywords

Navigation