Enhancing crop yield by using Rubisco activase to improve photosynthesis under elevated temperatures

Inosha Wijewardene, Guoxin Shen, Hong Zhang

Stress Biology ›› 2021, Vol. 1 ›› Issue (1) : 2. DOI: 10.1007/s44154-021-00002-5
Review

Enhancing crop yield by using Rubisco activase to improve photosynthesis under elevated temperatures

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Abstract

With the rapid growth of world population, it is essential to increase agricultural productivity to feed the growing population. Over the past decades, many methods have been used to increase crop yields. Despite the success in boosting the crop yield through these methods, global food production still needs to be increased to be on par with the increasing population and its dynamic consumption patterns. Additionally, given the prevailing environmental conditions pertaining to the global temperature increase, heat stress will likely be a critical factor that negatively affects plant biomass and crop yield. One of the key elements hindering photosynthesis and plant productivity under heat stress is the thermo-sensitivity of the Rubisco activase (RCA), a molecular chaperone that converts Rubisco back to active form after it becomes inactive. It would be an attractive and practical strategy to maintain photosynthetic activity under elevated temperatures by enhancing the thermo-stability of RCA. In this context, this review discusses the need to improve the thermo-tolerance of RCA under current climatic conditions and to further study RCA structure and regulation, and its limitations at elevated temperatures. This review summarizes successful results and provides a perspective on RCA research and its implication in improving crop yield under elevated temperature conditions in the future.

Keywords

Climate change / Drought / Heat stress / Temperature increase / Rubisco activase

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Inosha Wijewardene, Guoxin Shen, Hong Zhang. Enhancing crop yield by using Rubisco activase to improve photosynthesis under elevated temperatures. Stress Biology, 2021, 1(1): 2 https://doi.org/10.1007/s44154-021-00002-5

References

[1]
Acuña-GalindoMA, MasonRE, SubramanianNK, HaysDB. Meta-analysis of wheat QTL regions associated with adaptation to drought and heat stress. Crop Sci, 2015, 55(2):477-492
CrossRef Google scholar
[2]
AkterN, IslamMR. Heat stress effects and management in wheat. A review. Agron Sustain Dev, 2017, 37(5):37
CrossRef Google scholar
[3]
AliM, MuhammadI, Ul HaqS, AlamM, KhattakAM, AkhtarK, UllahH, KhanA, LuG, GongZH. The CaChiVI2 gene of Capsicum annuum L. confers resistance against heat stress and infection of Phytophthora capsici. Front Plant Sci, 2020, 11: 219
CrossRef Google scholar
[4]
AllakhverdievSI, KreslavskiVD, KlimovVV, LosDA, CarpentierR, MohantyP. Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res, 2008, 98(1-3):541-550
CrossRef Google scholar
[5]
AnjumNA. Plant acclimation to environmental stress: a critical appraisal. Front Plant Sci, 2015, 6: 445
CrossRef Google scholar
[6]
AntonovskyN, GleizerS, MiloR. Engineering carbon fixation in E. coli: from heterologous RuBisCO expression to the Calvin–Benson–Bassham cycle. Curr Opin Biotechnol, 2017, 47: 83-91
CrossRef Google scholar
[7]
Ayala-OchoaA, Vargas-SuárezM, Loza-TaveraH, LeonP, Jimenez-GarciaL, Sanchez-De-JimenezE. In maize, two distinct ribulose 1, 5-bisphosphate carboxylase/oxygenase activase transcripts have different day/night patterns of expression. Biochimie., 2004, 86(7):439-449
CrossRef Google scholar
[8]
BartaC, DunkleAM, WachterRM, SalvucciME. Structural changes associated with the acute thermal instability of Rubisco activase. Arch Biochem Biophys, 2010, 499: 17-25
CrossRef Google scholar
[9]
BayramovS. Changes in protein quantities of phosphoenolpyruvate carboxylase and Rubisco activase in various wheat genotypes. Saudi J Biol Sci, 2017, 24(7):1529-1533
CrossRef Google scholar
[10]
BhatJY, MiličićG, Thieulin-PardoG, BracherA, MaxwellA, CiniawskyS, Mueller-CajarO, EngenJR, HartlFU, WendlerP. Mechanism of enzyme repair by the AAA+ chaperone Rubisco activase. Mol Cell, 2017, 67: 744-756. e746
CrossRef Google scholar
[11]
Bhat JY, Thieulin-Pardo G, Hartl FU, Hayer-Hartl M (2017b) Rubisco activases: AAA+ chaperones adapted to enzyme repair. Front Mol Biosci 4. https://doi.org/10.3389/fmolb.2017.00020
[12]
BiH, DongX, LiuP, LiQ, AiX. Influence of over expression of CsRCA on photosynthesis of cucumber seedlings under high temperature stress. J Appl Ecol, 2016, 27: 2308-2314
CrossRef Google scholar
[13]
BiH, LiuP, JiangZ, AiX. Overexpression of the rubisco activase gene improves growth and low temperature and weak light tolerance in Cucumis sativus. Physiol Plant, 2017, 161: 224-234
CrossRef Google scholar
[14]
Bi HH, Zhao Y, Li HH, Liu WX (2020) Wheat heat shock factor TaHsfA6f increases aba levels and enhances tolerance to multiple abiotic stresses in transgenic plants. Int J Mol Sci 21:9. https://doi.org/10.3390/ijms21093121
[15]
BuschFA, SageRF. The sensitivity of photosynthesis to O2 and CO2 concentration identifies strong Rubisco control above the thermal optimum. New Phytol, 2017, 213: 1036-1051
CrossRef Google scholar
[16]
Carmo-SilvaAE, SalvucciME. The activity of Rubisco's molecular chaperone, Rubisco activase, in leaf extracts. Photosynth Res, 2011, 108(2-3):143-155
CrossRef Google scholar
[17]
Carmo-SilvaAE, SalvucciME. The regulatory properties of Rubisco activase differ among species and affect photosynthetic induction during light transitions. Plant Physiol, 2013, 161: 1645-1655
CrossRef Google scholar
[18]
Carmo-SilvaE, ScalesJC, MadgwickPJ, ParryMA. Optimizing Rubisco and its regulation for greater resource use efficiency. Plant Cell Environ, 2015, 38(9):1817-1832
CrossRef Google scholar
[19]
ChaoM, YinZ, HaoD, ZhangJ, SongH, NingA, XuX, YuD. Variation in Rubisco activase (RCAβ) gene promoters and expression in soybean [Glycine max (L.) Merr.]. J Exp Bot, 2014, 65: 47-59
CrossRef Google scholar
[20]
ChenY, JinJH, JiangQS, YuCL, ChenJ, XuLG, JiangDA. Sodium bisulfite enhances photosynthesis in rice by inducing Rubisco activase gene expression. Photosynthetica., 2014, 52(3):475-478
CrossRef Google scholar
[21]
Crafts-BrandnerSJ, SalvucciME. Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci U S A, 2000, 97(24):13430-13435
CrossRef Google scholar
[22]
Crafts-BrandnerSJ, SalvucciME, EgliDB. Fruit removal in soybean induces the formation of an insoluble form of ribulose-1, 5-bisphosphate carboxylase/oxygenase in leaf extracts. Planta., 1991, 183(2):300-306
CrossRef Google scholar
[23]
Crafts-BrandnerSJ, Van De LooFJ, SalvucciME. The two forms of ribulose-1, 5-bisphosphate carboxylase/oxygenase activase differ in sensitivity to elevated temperature. Plant Physiol, 1997, 114: 439-444
CrossRef Google scholar
[24]
CvikrováM, GemperlováL, DobráJ, MartincováO, PrásilIT, GubisJ, VankováR. Effect of heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Sci, 2012, 182: 49-58
CrossRef Google scholar
[25]
DegenGE, WorrallD, Carmo-SilvaE. An isoleucine residue acts as a thermal and regulatory switch in wheat Rubisco activase. Plant J, 2020, 103(2):742-751
CrossRef Google scholar
[26]
Demirevska-KepovaK, HolzerR, Simova-StoilovaL, FellerU. Heat stress effects on ribulose-1, 5-bisphosphate carboxylase/oxygenase, Rubisco binding protein and Rubisco activase in wheat leaves. Biol Plant, 2005, 49(4):521-525
CrossRef Google scholar
[27]
DeridderBP, SalvucciME. Modulation of Rubisco activase gene expression during heat stress in cotton (Gossypium hirsutum L.) involves post-transcriptional mechanisms. Plant Sci, 2007, 172(2):246-254
CrossRef Google scholar
[28]
DeridderBP, ShybutME, DyleMC, KremlingKA, ShapiroMB. Changes at the 3′-untranslated region stabilize Rubisco activase transcript levels during heat stress in Arabidopsis. Planta., 2012, 236: 463-476
CrossRef Google scholar
[29]
DrukaA, PotokinaE, LuoZ, JiangN, ChenX, KearseyM, WaughR. Expression quantitative trait loci analysis in plants. Plant Biotechnol J, 2010, 8: 10-27
CrossRef Google scholar
[30]
Dubey PK, Singh GS, Abhilash PC (2020) Agriculture in a changing climate. Adaptive Agricultural Practices: Building resilience in a changing climate. Springer, Cham. pp 1–10. https://doi.org/10.1007/978-3-030-15519-3_1
[31]
EckardtNA, SnyderGW, PortisAR Jr, OgrenWL. Growth and photosynthesis under high and low irradiance of Arabidopsis thaliana antisense mutants with reduced ribulose-1, 5-bisphosphate carboxylase/oxygenase activase content. Plant Physiol, 1997, 113: 575-586
CrossRef Google scholar
[32]
El-EsawiMA, Al-GhamdiAA, AliHM, AhmadM. Overexpression of AtWRKY30 transcription factor enhances heat and drought stress tolerance in wheat (Triticum aestivum L.). Genes, 2019, 10(2):163
CrossRef Google scholar
[33]
FahadS, BajwaAA, NazirU, AnjumSA, FarooqA, ZohaibA, SadiaS, NasimW, AdkinsS, SaudS. Crop production under drought and heat stress: plant responses and management options. Front Plant Sci, 2017, 8: 1147
CrossRef Google scholar
[34]
FanY, MaC, HuangZ, AbidM, JiangS, DaiT, ZhangW, MaS, JiangD, HanX. Heat priming during early reproductive stages enhances thermo-tolerance to post-anthesis heat stress via improving photosynthesis and plant productivity in winter wheat (Triticum aestivum L.). Front Plant Sci, 2018, 9: 805
CrossRef Google scholar
[35]
Flecken M, Wang H, Popilka L, Hartl FU, Bracher A, Hayer-Hartl M (2020) Dual role of a rubisco activase in metabolic repair and carboxysome organization. BioRxiv, Cell 91. https://doi.org/10.1101/2020.05.16.099382
[36]
FukayamaH, AbeR, UchidaN. SDS-dependent proteases induced by ABA and its relation to Rubisco and Rubisco activase contents in rice leaves. Plant Physiol Biochem, 2010, 48: 808-812
CrossRef Google scholar
[37]
FukayamaH, MizumotoA, UeguchiC, KatsunumaJ, MoritaR, SasayamaD, HatanakaT, AzumaT. Expression level of rubisco activase negatively correlates with rubisco content in transgenic rice. Photosynth Res, 2018, 137(3):465-474
CrossRef Google scholar
[38]
FukayamaH, UchidaN, AzumaT, YasudaT. Relationships between photosynthetic activity and the amounts of Rubisco activase and Rubisco in rice leaves from emergence through senescence. Japanese J Crop Sci, 1996, 65(2):296-302
CrossRef Google scholar
[39]
FukayamaH, UeguchiC, NishikawaK, KatohN, IshikawaC, MasumotoC, HatanakaT, MisooS. Overexpression of Rubisco activase decreases the photosynthetic co2 assimilation rate by reducing rubisco content in rice leaves. Plant Cell Physiol, 2012, 53: 976-986
CrossRef Google scholar
[40]
GaxiolaRA, LiJS, UndurragaS, DangLM, AllenGJ, AlperSL, FinkGR. Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci U S A, 2001, 98(20):11444-11449
CrossRef Google scholar
[41]
GhoshS, KambleNU, VermaP, SalviP, PetlaBP, RoyS, RaoV, HazraA, VarshneyV, KaurH, MajeeM. Arabidopsis protein l-ISOASPARTYL METHYLTRANSFERASE repairs isoaspartyl damage to antioxidant enzymes and increases heat and oxidative stress tolerance. J Biol Chem, 2020, 295(3):783-799
CrossRef Google scholar
[42]
HammondET, AndrewsTJ, MottKA, WoodrowIE. Regulation of Rubisco activation in antisense plants of tobacco containing reduced levels of Rubisco activase. Plant J, 1998, 14: 101-110
CrossRef Google scholar
[43]
HartlM, FüßlM, BoersemaPJ, JostJO, KramerK, BakirbasA, SindlingerJ, PlöchingerM, LeisterD, UhrigG. Lysine acetylome profiling uncovers novel histone deacetylase substrate proteins in Arabidopsis. Mol Syst Biol, 2017, 13: 949
CrossRef Google scholar
[44]
HasseD, LarssonAM, AnderssonI. Structure of Arabidopsis thaliana Rubisco activase. Acta Crystallogr D Biol, 2015, 71: 800-808
CrossRef Google scholar
[45]
HeZ, Von CaemmererS, HudsonGS, PriceGD, BadgerMR, AndrewsTJ. Ribulose-1, 5-bisphosphate carboxylase/oxygenase activase deficiency delays senescence of ribulose-1, 5-bisphosphate carboxylase/oxygenase but progressively impairs its catalysis during tobacco leaf development. Plant Physiol, 1997, 115(4):1569-1580
CrossRef Google scholar
[46]
HendersonJN, KuriataAM, FrommeR, SalvucciME, WachterRM. Atomic resolution x-ray structure of the substrate recognition domain of higher plant ribulose-bisphosphate carboxylase/oxygenase (Rubisco) activase. J Biol Chem, 2011, 286(41):35683-35688
CrossRef Google scholar
[47]
HongJ, JiangDA, WengXY, WangWB, HuDW. Leaf anatomy, chloroplast ultrastructure, and cellular localisation of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCO) and RuBPCO activase in Amaranthus tricolor L. Photosynthetica., 2005, 43(4):519-528
CrossRef Google scholar
[48]
Ipcc IPOCC BongaartsJ. Special report on global warming of 1.5 °C (SR15). Popul Dev Rev, 2019, 45(1):251-252
CrossRef Google scholar
[49]
JiangY, WangJ, TaoX, ZhangY. Characterization and expression of Rubisco activase genes in Ipomoea batatas. Mol Biol Rep, 2013, 40(11):6309-6321
CrossRef Google scholar
[50]
JiangY, YongB, ChenJ, ZhangY. Two Rubisco activase genes from ipomoea Batatas have different roles in photosynthesis of Arabidopsis. Pak J Bot, 2014, 46: 1381À1388
[51]
JinSH, HongJ, LiXQ, JiangDA. Antisense inhibition of Rubisco activase increases Rubisco content and alters the proportion of Rubisco activase in stroma and thylakoids in chloroplasts of rice leaves. Ann Bot, 2006, 97(5):739-744
CrossRef Google scholar
[52]
JurczykB, HuraK, TrzemeckaA, RapaczM. Evidence for alternative splicing mechanisms in meadow fescue (Festuca pratensis) and perennial ryegrass (Lolium perenne) Rubisco activase gene. J Plant Physiol, 2015, 176: 61-64
CrossRef Google scholar
[53]
JurczykB, PociechaE, GrzesiakM, RapaczM. Enhanced expression of Rubisco activase confers to increase in Rubisco activity during cold acclimation in Lolium perenne. Procedia Environ Sci, 2015, 29: 213-214
CrossRef Google scholar
[54]
KhushGS. What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol, 2005, 59(1):1-6
CrossRef Google scholar
[55]
KimK, PortisAR Jr. Temperature dependence of photosynthesis in Arabidopsis plants with modifications in Rubisco activase and membrane fluidity. Plant Cell Physiol, 2005, 46: 522-530
CrossRef Google scholar
[56]
KimSY, HarveyCM, GieseJ, LassowskatI, SinghV, CavanaghAP, SpaldingMH, FinkemeierI, OrtDR, HuberSC. In vivo evidence for a regulatory role of phosphorylation of Arabidopsis Rubisco activase at the Thr78 site. Proc Natl Acad Sci U S A, 2019, 116(37):18723-18731
CrossRef Google scholar
[57]
KumarA, LiCS, PortisAR. Arabidopsis thaliana expressing a thermostable chimeric Rubisco activase exhibits enhanced growth and higher rates of photosynthesis at moderately high temperatures. Photosynth Res, 2009, 100(3):143-153
CrossRef Google scholar
[58]
KumarRR, GoswamiS, DubeyK, SinghK, SinghJP, KumarA, RaiGK, SinghSD, BakshiS, SinghB. RuBisCo activase—a catalytic chaperone involved in modulating the RuBisCo activity and heat stress-tolerance in wheat. J Plant Biochem Biotechnol, 2019, 28(1):63-75
CrossRef Google scholar
[59]
KumarRR, GoswamiS, ShamimM, DubeyK, SinghK, SinghS, KalaYK, NirajRR, SakhreyA, SinghGP. Exploring the heat-responsive chaperones and microsatellite markers associated with terminal heat stress tolerance in developing wheat. Funct Integr Genomics, 2017, 17: 621-640
CrossRef Google scholar
[60]
KumarRR, GoswamiS, SinghK, DubeyK, SinghS, SharmaR, VermaN, KalaYK, RaiGK, GroverM. Identification of putative RuBisCo Activase (TaRca1)- the catalytic chaperone regulating carbon assimilatory pathway in wheat (Triticum aestivum) under the heat stress. Front Plant Sci, 2016, 7: 986
CrossRef Google scholar
[61]
KurekI, ChangTK, BertainSM, MadrigalA, LiuL, LassnerMW, ZhuGH. Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell, 2007, 19(10):3230-3241
CrossRef Google scholar
[62]
KuriataAM, ChakrabortyM, HendersonJN, HazraS, SerbanAJ, PhamTV, LevitusM, WachterRM. ATP and magnesium promote cotton short-form ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) activase hexamer formation at low micromolar concentrations. Biochemistry., 2014, 53: 7232-7246
CrossRef Google scholar
[63]
LamaouiM, JemoM, DatlaR, BekkaouiF. Heat and drought stresses in crops and approaches for their mitigation. Front Chem, 2018, 6: 26
CrossRef Google scholar
[64]
LawDR, Crafts-BrandnerSJ, SalvucciME. Heat stress induces the synthesis of a new form of ribulose-1, 5-bisphosphate carboxylase/oxygenase activase in cotton leaves. Planta., 2001, 214: 117-125
CrossRef Google scholar
[65]
LawRD, Crafts-BrandnerSJ. Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1, 5-bisphosphate carboxylase/oxygenase. Plant Physiol, 1999, 120(1):173-182
CrossRef Google scholar
[66]
LawRD, Crafts-BrandnerSJ. High temperature stress increases the expression of wheat leaf ribulose-1, 5-bisphosphate carboxylase/oxygenase activase protein. Arch Biochem Biophys, 2001, 386(2):261-267
CrossRef Google scholar
[67]
LiC, SalvucciME, PortisAR. Two residues of Rubisco activase involved in recognition of the Rubisco substrate. J Biol Chem, 2005, 280(26):24864-24869
CrossRef Google scholar
[68]
LinYH, HuangLF, HaseT, HuangHE, FengTY. Expression of plant ferredoxin-like protein (PFLP) enhances tolerance to heat stress in Arabidopsis thaliana. N Biotechnol, 2015, 32(2):235-242
CrossRef Google scholar
[69]
LiuX, HuangB. Photosynthetic acclimation to high temperatures associated with heat tolerance in creeping bentgrass. J Plant Physiol, 2008, 165: 1947-1953
CrossRef Google scholar
[70]
LiuY, TangL, QiuX, LiuB, ChangX, LiuL, ZhangX, CaoW, ZhuY. Impacts of 1.5 and 2.0°C global warming on rice production across China. Agric For Meteorol, 2020, 284: 107900
CrossRef Google scholar
[71]
LiuZ, TaubCC, McclungCR. Identification of an Arabidopsis thaliana ribulose-1, 5-bisphosphate carboxylase/oxygenase activase (RCA) minimal promoter regulated by light and the circadian clock. Plant Physiol, 1996, 112: 43-51
CrossRef Google scholar
[72]
LoganathanN, TsaiYCC, Mueller-CajarO. Characterization of the heterooligomeric red-type rubisco activase from red algae. Proc Natl Acad Sci U S A, 2016, 113: 14019-14024
CrossRef Google scholar
[73]
Martínez-BarajasE, Molina-GalánJ, De JimenezES. Regulation of Rubisco activity during grain-fill in maize: possible role of Rubisco activase. J Agric Sci, 1997, 128(2):155-161
CrossRef Google scholar
[74]
MateCJ, HudsonGS, Von CaemmererS, EvansJR, AndrewsTJ. Reduction of ribulose bisphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose bisphosphate carboxylase carbamylation and impairs photosynthesis. Plant Physiol, 1993, 102: 1119-1128
CrossRef Google scholar
[75]
MinhasPS, RaneJ, PasalaRK. Abiotic stresses in agriculture: an overview. Abiotic stress Management for Resilient Agriculture, 2017 Singapore Springer 3-8
CrossRef Google scholar
[76]
Mueller-CajarO, WhitneySM. Directing the evolution of Rubisco and Rubisco activase: first impressions of a new tool for photosynthesis research. Photosynth Res, 2008, 98(1-3):667-675
CrossRef Google scholar
[77]
NadeemM, LiJ, WangM, ShahL, LuS, WangX, MaC. Unraveling field crops sensitivity to heat stress: mechanisms, approaches, and future prospects. Agronomy., 2018, 8: 128
CrossRef Google scholar
[78]
NagarajanR, GillKS. Evolution of Rubisco activase gene in plants. Plant Mol Biol, 2018, 96(1-2):69-87
CrossRef Google scholar
[79]
NalluriN, KarriVR. Recent advances in genetic manipulation of crops: a promising approach to address the global food and industrial applications. Plant Sci Today, 2020, 7: 70-92
CrossRef Google scholar
[80]
OgbagaCC, StepienP, AtharHUR, AshrafM. Engineering Rubisco activase from thermophilic cyanobacteria into high-temperature sensitive plants. Crit Rev Biotechnol, 2018, 38(4):559-572
CrossRef Google scholar
[81]
OttCM, SmithBD, PortisAR, SpreitzerRJ. Activase region on chloroplast Ribulose-1, 5-bisphosphate carboxylase/oxygenase nonconservative substitution in the large subunit alters species specificity of protein interaction. J Biol Chem, 2000, 275(34):26241-26244
CrossRef Google scholar
[82]
PanzadeKP, VishwakarmaH, PadariaJC. Heat stress inducible cytoplasmic isoform of ClpB1 from Z. nummularia exhibits enhanced thermotolerance in transgenic tobacco. Mol Biol Rep, 2020, 47(5):3821-3831
CrossRef Google scholar
[83]
Parry MAJ, Andralojc PJ, Mitchell RA, Madgwick PJ, Keys AJ (2003) Manipulation of Rubisco: the amount, activity, function and regulation. J Exp Bot 54(386):1321–1333. https://doi.org/10.1093/jxb/erg141
[84]
ParryMAJ, AndralojcPJ, ScalesJC, SalvucciME, Carmo-SilvaAE, AlonsoH, WhitneySM. Rubisco activity and regulation as targets for crop improvement. J Exp Bot, 2013, 64: 717-730
CrossRef Google scholar
[85]
Parry M AJ, Madgwick PJ, Carvalho JFC, Andralojc PJ (2007) Prospects for increasing photosynthesis by overcoming the limitations of Rubisco. J Agric Sci 145(1):31–43. https://doi.org/10.1017/S0021859606006666
[86]
PasapulaV, ShenG, KuppuS, Paez-ValenciaJ, MendozaM, HouP, ChenJ, QiuX, ZhuL, ZhangX, AuldD, BlumwaldE, ZhangH, GaxiolaR, PaytonP. Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fibre yield in the field conditions. Plant Biotechnol J, 2011, 9(1):88-99
CrossRef Google scholar
[87]
PerdomoJA, Capó-BauçàS, Carmo-SilvaE, GalmésJ. 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. Front Plant Sci, 2017, 8: 490
CrossRef Google scholar
[88]
PerdomoJA, DegenGE, WorrallD, Carmo-SilvaE. Rubisco activation by wheat Rubisco activase isoform 2β is insensitive to inhibition by ADP. Biochem J, 2019, 476: 2595-2606
CrossRef Google scholar
[89]
PortisAR. Rubisco activase - Rubisco's catalytic chaperone. Photosynth Res, 2003, 75: 11-27
CrossRef Google scholar
[90]
PortisAR Jr. Rubisco activase. Biochim Biophys Acta, 1990, 1015: 15-28
CrossRef Google scholar
[91]
PortisAR Jr, LiC, WangD, SalvucciME. Regulation of Rubisco activase and its interaction with Rubisco. J Exp Bot, 2008, 59(7):1597-1604
CrossRef Google scholar
[92]
PortisAR Jr, SalvucciME. The discovery of Rubisco activase–yet another story of serendipity. Photosynth Res, 2002, 73(1/3):257-264
CrossRef Google scholar
[93]
QiY, LiuY, ZhangZ, GaoJ, GuanZ, FangW, ChenS, ChenF, JiangJ. The over-expression of a chrysanthemum gene encoding an RNA polymerase II CTD phosphatase-like 1 enzyme enhances tolerance to heat stress. Hortic Res, 2018, 5(1):1-10
CrossRef Google scholar
[94]
QianJ, RodermelSR. Ribulose-1, 5-bisphosphate carboxylase/oxygenase activase cDNAs from Nicotiana tabacum. Plant Physiol, 1993, 102(2):683-684
CrossRef Google scholar
[95]
QuD, SongY, LiW, PeiX, WangZ, JiaS, ZhangY. Isolation and characterization of the organ-specific and light-inducible promoter of the gene encoding rubisco activase in potato (Solanum tuberosum). Genet Mol Res, 2011, 10(2):621-631
CrossRef Google scholar
[96]
Qu Y, Sakoda K, Fukayama H, Kondo E, Suzuki Y, Makino A, Yamori W (2021) Overexpression of both Rubisco and Rubisco activase rescues rice photosynthesis and biomass under heat stress. Plant Cell Environ. https://doi.org/10.1111/pce.14051
[97]
RisticZ, MomčilovićI, BukovnikU, PrasadPVV, FuJ, DeridderBP, ElthonTE, MladenovN. Rubisco activase and wheat productivity under heat-stress conditions. J Exp Bot, 2009, 60: 4003-4014
CrossRef Google scholar
[98]
RokkaA, ZhangL, AroEM. Rubisco activase: an enzyme with a temperature-dependent dual function?. Plant J, 2001, 25: 463-471
CrossRef Google scholar
[99]
RollinsJ, HabteE, TemplerS, ColbyT, SchmidtJ, Von KorffM. Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). J Exp Bot, 2013, 64(11):3201-3212
CrossRef Google scholar
[100]
RundleSJ, ZielinskiRE. Organization and expression of two tandemly oriented genes encoding ribulosebisphosphate carboxylase/oxygenase activase in barley. J Biol Chem, 1991, 266: 4677-4685
CrossRef Google scholar
[101]
RuuskaSA, AndrewsTJ, BadgerMR, PriceGD, Von CaemmererS. The role of chloroplast electron transport and metabolites in modulating Rubisco activity in tobacco. Insights from transgenic plants with reduced amounts of cytochrome b/fcomplex or glyceraldehyde 3-phosphate dehydrogenase. Plant Physiol, 2000, 122: 491-504
CrossRef Google scholar
[102]
SageRF, WayDA, KubienDS. Rubisco, rubisco activase, and global climate change. J Exp Bot, 2008, 59: 1581-1595
CrossRef Google scholar
[103]
Salesse-SmithCE, SharwoodRE, BuschFA, KromdijkJ, BardalV, SternDB. Overexpression of Rubisco subunits with RAF1 increases Rubisco content in maize. Nat Plants, 2018, 4(10):802-810
CrossRef Google scholar
[104]
SalvucciME. Association of Rubisco activase with chaperonin-60β: a possible mechanism for protecting photosynthesis during heat stress. J Exp Bot, 2008, 59(7):1923-1933
CrossRef Google scholar
[105]
SalvucciME, Crafts-BrandnerSJ. Mechanism for deactivation of Rubisco under moderate heat stress. Physiol Plant, 2004, 122(4):513-519
CrossRef Google scholar
[106]
SalvucciME, Crafts-BrandnerSJ. Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant, 2004, 120: 179-186
CrossRef Google scholar
[107]
SalvucciME, Crafts-BrandnerSJ. Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiol, 2004, 134: 1460-1470
CrossRef Google scholar
[108]
SalvucciME, DeridderBP, PortisAR Jr. Effect of activase level and isoform on the thermotolerance of photosynthesis in Arabidopsis. J Exp Bot, 2006, 57: 3793-3799
CrossRef Google scholar
[109]
SalvucciME, OgrenWL. The mechanism of Rubisco activase: insights from studies of the properties and structure of the enzyme. Photosynth Res, 1996, 47(1):1-11
CrossRef Google scholar
[110]
SalvucciME, OsteryoungKW, Crafts-BrandnerSJ, VierlingE. Exceptional sensitivity of Rubisco activase to thermal denaturation in vitro and in vivo. Plant Physiol, 2001, 127: 1053-1064
CrossRef Google scholar
[111]
SalvucciME, PortisAR, OgrenWL. A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase/oxygenase activation in vivo. Photosynth Res, 1985, 7: 193-201
CrossRef Google scholar
[112]
SalvucciME, Van De LooFJ, StecherD. Two isoforms of Rubisco activase in cotton, the products of separate genes not alternative splicing. Planta, 2003, 216: 736-744
CrossRef Google scholar
[113]
SalvucciME, WernekeJM, OgrenWL, PortisAR. Purification and species distribution of Rubisco activase. Plant Physiol, 1987, 84(3):930-936
CrossRef Google scholar
[114]
Sanchez De JimenezE, MedranoL, Martinez-BarajasE. Rubisco activase, a possible new member of the molecular chaperone family. Biochemistry, 1995, 34(9):2826-2831
CrossRef Google scholar
[115]
SándorR, Picon-CochardC, MartinR, LouaultF, KlumppK, BorrasD, BellocchiG. Plant acclimation to temperature: developments in the pasture simulation model. Field Crop Res, 2018, 222: 238-255
CrossRef Google scholar
[116]
ScafaroAP, AtwellBJ, MuylaertS, ReuselBV, RuizGA, RieJV, GalléA. A thermotolerant variant of Rubisco activase from a wild relative improves growth and seed yield in rice under heat stress. Front Plant Sci, 2018, 9: 1663
CrossRef Google scholar
[117]
ScafaroAP, BautsoensN, Den BoerB, Van RieJ, GalleA. A conserved sequence from heat-adapted species improves Rubisco activase thermostability in wheat. Plant Physiol, 2019, 181(1):43-54
CrossRef Google scholar
[118]
ScafaroAP, GalleA, Van RieJ, Carmo-SilvaE, SalvucciME, AtwellBJ. Heat tolerance in a wild Oryza species is attributed to maintenance of Rubisco activation by a thermally stable Rubisco activase ortholog. New Phytol, 2016, 211(3):899-911
CrossRef Google scholar
[119]
ShanX, WangJ, ChuaL, JiangD, PengW, XieD. The role of Arabidopsis Rubisco activase in jasmonate-induced leaf senescence. Plant Physiol, 2011, 155(2):751-764
CrossRef Google scholar
[120]
SharkeyTD. Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ, 2005, 28: 269-277
CrossRef Google scholar
[121]
SharkeyTD, BadgerMR, Von CaemmererS, AndrewsTJ. Increased heat sensitivity of photosynthesis in tobacco plants with reduced Rubisco activase. Photosynth Res, 2001, 67: 147-156
CrossRef Google scholar
[122]
ShenJ, OrozcoE, OgrenW. Expression of the two isoforms of spinach ribulose 1, 5-bisphosphate carboxylase activase and essentiality of the conserved lysine in the consensus nucleotide-binding domain. J Biol Chem, 1991, 266: 8963-8968
CrossRef Google scholar
[123]
ShivhareD, Mueller-CajarO. In vitro characterization of thermostable CAM Rubisco activase reveals a Rubisco interacting surface loop. Plant Physiol, 2017, 174(3):1505-1516
CrossRef Google scholar
[124]
Shivhare D, Mueller-Cajar O (2017b) Rubisco Activase: the molecular chiropractor of the world’s most abundant protein. Photosynth Bioener 159. https://doi.org/10.1142/9789813230309_0008
[125]
ShivhareD, NgJ, TsaiYCC, Mueller-CajarO. Probing the rice Rubisco–Rubisco activase interaction via subunit heterooligomerization. Proc Natl Acad Sci U S A, 2019, 116(48):24041-24048
CrossRef Google scholar
[126]
SinghB, SalariaN, ThakurK, KukrejaS, GautamS, GoutamU. Functional genomic approaches to improve crop plant heat stress tolerance. F1000Res, 2019, 8: 1721
CrossRef Google scholar
[127]
SomervilleCR, PortisAR, OgrenWL. A mutant of Arabidopsis thaliana which lacks activation of RuBP carboxylase in vivo. Plant Physiol, 1982, 70: 381-387
CrossRef Google scholar
[128]
StotzM, Mueller-CajarO, CiniawskyS, WendlerP, HartlFU, BracherA, Hayer-HartlM. Structure of green-type Rubisco activase from tobacco. Nat Struct Mol Biol, 2011, 18(12):1366-1370
CrossRef Google scholar
[129]
SuganamiM, SuzukiY, KondoE, NishidaS, KonnoS, MakinoA. Effects of overproduction of Rubisco Activase on Rubisco content in transgenic rice grown at different N levels. Int J Mol Sci, 2020, 21: 1626
CrossRef Google scholar
[130]
SuganamiM, SuzukiY, SatoT, MakinoA. Relationship between Rubisco activase and Rubisco contents in transgenic rice plants with overproduced or decreased Rubisco content. Soil Sci Plant Nutr, 2018, 64: 352-359
CrossRef Google scholar
[131]
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. https://doi.org/10.1093/plphys/kiaa026
[132]
SunQ, ZhangY, ChenB, JiaB, ZhangZ, CuiM, KanX, ShiH, DengD, YinZ. Expression quantitative trait loci analysis of the rubisco activase gene in maize. Photosynthetica., 2017, 55(2):329-337
CrossRef Google scholar
[133]
SuzukiY, MiyamotoT, YoshizawaR, MaeT, MakinoA. Rubisco content and photosynthesis of leaves at different positions in transgenic rice with an overexpression of RBCS. Plant Cell Environ, 2009, 32(4):417-427
CrossRef Google scholar
[134]
ToKY, SuenDF, ChenSCG. Molecular characterization of ribulose-1, 5-bisphosphate carboxylase/oxygenase activase in rice leaves. Planta., 1999, 209: 66-76
CrossRef Google scholar
[135]
TsaiYCC, LapinaMC, BhushanS, Mueller-CajarO. Identification and characterization of multiple rubisco activases in chemoautotrophic bacteria. Nat Commun, 2015, 6(1):8883
CrossRef Google scholar
[136]
UlukanH. The evolution of cultivated plant species: classical plant breeding versus genetic engineering. Plant Syst Evol, 2009, 280(3-4):133-142
CrossRef Google scholar
[137]
Vargas-SuárezM, Ayala-OchoaA, Lozano-FrancoJ, García-TorresI, Díaz-QuiñonezA, Ortíz-NavarreteVF, Sánchez-De-JiménezE. Rubisco activase chaperone activity is regulated by a post-translational mechanism in maize leaves. J Exp Bot, 2004, 55(408):2533-2539
CrossRef Google scholar
[138]
WahidA, GelaniS, AshrafM, FooladMR. Heat tolerance in plants: an overview. Environ Exp Bot, 2007, 61: 199-223
CrossRef Google scholar
[139]
WalterA, FingerR, HuberR, BuchmannN. Opinion: smart farming is key to developing sustainable agriculture. Proc Natl Acad Sci U S A, 2017, 114: 6148-6150
CrossRef Google scholar
[140]
WangD, LiXF, ZhouZJ, FengXP, YangWJ, JiangDA. Two Rubisco activase isoforms may play different roles in photosynthetic heat acclimation in the rice plant. Physiol Plant, 2010, 139: 55-67
CrossRef Google scholar
[141]
WangD, LuQ, LiX, JiangQ, WuJ, JiangD. Relationship between Rubisco activase isoform levels and photosynthetic rate in different leaf positions of rice plant. Photosynthetica., 2009, 47(4):621-629
CrossRef Google scholar
[142]
Wang J, Gao X, Dong J, Tian X, Wang J, Palta JA, Xu S, Fang Y, Wang Z (2020) Over-expression of the heat-responsive wheat gene TaHSP23.9 in transgenic Arabidopsis conferred tolerance to heat and salt stress. Front Plant Sci 11. https://doi.org/10.3389/fpls.2020.00243
[143]
WangX, HuangW, LiuJ, YangZ, HuangB. Molecular regulation and physiological functions of a novel FaHsfA2c cloned from tall fescue conferring plant tolerance to heat stress. Plant Biotechnol J, 2017, 15: 237-248
CrossRef Google scholar
[144]
WangZY, SnyderGW, EsauBD, PortisAR, OgrenWL. Species-dependent variation in the interaction of substrate-bound ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase. Plant Physiol, 1992, 100: 1858-1862
CrossRef Google scholar
[145]
WatillonB, KettmannR, BoxusP, BurnyA. Developmental and circadian pattern of rubisco activase mRNA accumulation in apple plants. Plant Mol Biol, 1993, 23: 501-509
CrossRef Google scholar
[146]
WeiL, WangQ, XinY, LuY, XuJ. Enhancing photosynthetic biomass productivity of industrial oleaginous microalgae by overexpression of RuBisCO activase. Algal Res, 2017, 27: 366-375
CrossRef Google scholar
[147]
WenJ, JiangF, WengY, SunM, ShiX, ZhouY, YuL, WuZ. Identification of heat-tolerance QTLs and high-temperature stress-responsive genes through conventional QTL mapping, QTL-seq and RNA-seq in tomato. BMC Plant Biol, 2019, 19: 398
CrossRef Google scholar
[148]
WernekeJM, ChatfieldJM, OgrenWL. Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis. Plant Cell, 1989, 1: 815-825
CrossRef Google scholar
[149]
WestonDJ, BauerleWL, Swire-ClarkGA, MooreBD, BairdWV. Characterization of Rubisco activase from thermally contrasting genotypes of Acer rubrum (Aceraceae). Am J Bot, 2007, 94: 926-934
CrossRef Google scholar
[150]
WijewardeneI, MishraN, SunL, SmithJ, ZhuX, PaytonP, ShenG, ZhangH. Improving drought-, salinity-, and heat-tolerance in transgenic plants by co-overexpressing Arabidopsis vacuolar pyrophosphatase gene AVP1 and Larrea Rubisco activase gene RCA. Plant Sci, 2020, 296: 110499
CrossRef Google scholar
[151]
WilsonRH, Thieulin-PardoG, HartlFU, Hayer-HartlM. Improved recombinant expression and purification of functional plant Rubisco. FEBS Lett, 2019, 593: 611-621
CrossRef Google scholar
[152]
Wostrikoff K, Clark A, Sato S, Clemente T, Stern D (2012) Ectopic expression of Rubisco subunits in maize mesophyll cells does not overcome barriers to cell type-specific accumulation. Plant Physiol 160(1):419–432. https://doi.org/10.1104/pp.112.195677
[153]
XuK, HeB, ZhouS, LiY, ZhangY. Cloning and characterization of the Rubisco activase gene from Ipomoea batatas (L.) Lam. Mol Biol Rep, 2010, 37: 661
CrossRef Google scholar
[154]
XueGP, DrenthJ, McintyreCL. TaHsfA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets. J Exp Bot, 2015, 66: 1025-1039
CrossRef Google scholar
[155]
YamoriW, HikosakaK, WayDA. Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res, 2014, 119: 101-117
CrossRef Google scholar
[156]
YamoriW, MasumotoC, FukayamaH, MakinoA. 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, 2012, 71: 871-880
CrossRef Google scholar
[157]
YamoriW, SuzukiK, NoguchiK, NakaiM, TerashimaI. Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Environ, 2006, 29: 1659-1670
CrossRef Google scholar
[158]
YamoriW, Von CaemmererS. Effect of Rubisco activase deficiency on the temperature response of CO2 assimilation rate and Rubisco activation state: insights from transgenic tobacco with reduced amounts of Rubisco activase. Plant Physiol, 2009, 151: 2073-2082
CrossRef Google scholar
[159]
YinZ, MengF, SongH, WangX, XuX, YuD. Expression quantitative trait loci analysis of two genes encoding rubisco activase in soybean. Plant Physiol, 2010, 152: 1625-1637
CrossRef Google scholar
[160]
YinZ, ZhangZ, DengD, ChaoM, GaoQ, WangY, YangZ, BianY, HaoD, XuC. Characterization of RuBisCo activase genes in maize: an α-isoform gene functions alongside a β-isoform gene. Plant Physiol, 2014, 164: 2096-2106
CrossRef Google scholar
[161]
YoonDK, IshiyamaK, SuganamiM, TazoeY, WatanabeM, ImaruokaS, OguraM, IshidaH, SuzukiY, ObaraM, MaeT, MakinoA. Transgenic rice overproducing Rubisco exhibits increased yields with improved nitrogen-use efficiency in an experimental paddy field. Nat Food, 2020, 1(2):134-139
CrossRef Google scholar
[162]
ZangX, GengX, LiuK, WangF, LiuZ, ZhangL, ZhaoY, TianX, HuZ, YaoY. Ectopic expression of TaOEP16-2-5B, a wheat plastid outer envelope protein gene, enhances heat and drought stress tolerance in transgenic Arabidopsis plants. Plant Sci, 2017, 258: 1-11
CrossRef Google scholar
[163]
ZhangJ, DuH, ChaoM, YinZ, YangH, LiY, HuangF, YuD. Identification of two bZIP transcription factors interacting with the promoter of soybean rubisco activase gene (GmRCAα). Front Plant Sci, 2016, 7: 628
CrossRef Google scholar
[164]
ZhangM, LiX, YangY, LuoZ, LiuC, GongM, ZouZ. An acidified thermostabilizing mini-peptide derived from the carboxyl extension of the larger isoform of the plant Rubisco activase. J Biotechnol, 2015, 212: 116-124
CrossRef Google scholar
[165]
ZhangN, KallisRP, EwyRG, PortisAR. Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proc Natl Acad Sci U S A, 2002, 99: 3330-3334
CrossRef Google scholar
[166]
ZhangN, SchürmannP, PortisAR. Characterization of the regulatory function of the 46-kDa isoform of Rubisco activase from Arabidopsis. Photosynth Res, 2001, 68: 29-37
CrossRef Google scholar
[167]
ZhangZ, KomatsuS. Molecular cloning and characterization of cDNAs encoding two isoforms of ribulose-1, 5-bisphosphate carboxylase/oxygenase activase in rice (Oryza sativa L.). J Biochem, 2000, 128(3):383-389
CrossRef Google scholar
[168]
ZhaoG, XuH, ZhangP, SuX, ZhaoH. Effects of 2, 4-epibrassinolide on photosynthesis and Rubisco activase gene expression in Triticum aestivum L. seedlings under a combination of drought and heat stress. Plant Growth Regul, 2017, 81(3):377-384
CrossRef Google scholar

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