Abstract
Warming driven by the accumulation of greenhouse gases in the atmosphere is irreversible over at least the next century, unless practical technologies are rapidly developed and deployed at scale to remove and sequester carbon dioxide from the atmosphere. Accepting this reality highlights the central importance for crop agriculture to develop adaptation strategies for a warmer future. While nearly all processes in plants are impacted by above optimum temperatures, the impact of heat stress on photosynthetic processes stand out for their centrality. Here, we review transgenic strategies that show promise in improving the high-temperature tolerance of specific subprocesses of photosynthesis and in some cases have already been shown in proof of concept in field experiments to protect yield from high temperature-induced losses. We also highlight other manipulations to photosynthetic processes for which full proof of concept is still lacking but we contend warrant further attention. Warming that has already occurred over the past several decades has had detrimental impacts on crop production in many parts of the world. Declining productivity presages a rapidly developing global crisis in food security particularly in low income countries. Transgenic manipulation of photosynthesis to engineer greater high-temperature resilience holds encouraging promise to help meet this challenge.
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Notes
The Sahel is a transitional region between the wooded Sudanian savanna to the south and the Sahara to the north. It spans ~6000 km from the Atlantic Ocean on the west coast of Africa to the Red Sea in the east. The Sahel belt from west to east includes parts of northern Senegal, southern Mauritania, central Mali, northern Burkina Faso, the extreme south of Algeria, Niger, the extreme north of Nigeria, Cameroon and Central African Republic, central Chad, central and southern Sudan, the extreme north of South Sudan, Eritrea and Ethiopia. (https://en.wikipedia.org/wiki/Sahel#cite_note-2)
References
Ainsworth EA, Ort DR (2010) How do we improve crop production in a warming world? Plant Physiol 154(2):526–530. https://doi.org/10.1104/pp.110.161349
Aigner H, Wilson RH, Bracher A, Calisse L, Bhat JY, Hartl FU, Hayer-Hartl M (2017) Plant RuBisCo assembly in E. coli with five chloroplast chaperones including BSD2. Sci 358(6368):1272–1278. https://doi.org/10.1126/science.aap9221
Alter RE, Douglas HC, Winter JM, Eltahir EAB (2018) Twentieth century regional climate change during summer in the central United States attributed to agricultural intensification. Geophys Res Lett 45:1586–1594
Arritt R (2016) Climate change in the corn belt. CSCAP-0193-2016. Ames, IA: Cropping Systems Coordinated Agricultural Project (CAP): Climate Change, Mitigation, and Adaptation in Corn-based Cropping Systems. https://store.extension.iastate.edu/Product/Climate-Change-in-the-Corn-Belt
Asseng S, Ewert F, Martre P, Rötter RP, Lobell DB, Cammarano D, Kimball BA, Ottman MJ, Wall GW, White JW, Reynolds MP, Alderman PD, Prasad PVV, Aggarwal PK, Anothai J, Basso B, Biernath C, Challinor AJ, De Sanctis G, Doltra J, Fereres E, Garcia-Vila M, Gayler S, Hoogenboom G, Hunt LA, Izaurralde RC, Jabloun M, Jones CD, Kersebaum KC, Koehler AK, Müller C, Naresh Kumar S, Nendel C, O’Leary G, Olesen JE, Palosuo T, Priesack E, Eyshi Rezaei E, Ruane AC, Semenov MA, Shcherbak I, Stöckle C, Stratonovitch P, Streck T, Supit I, Tao F, Thorburn PJ, Waha K, Wang E, Wallach D, Wolf J, Zhao Z, Zhu Y (2015) Rising temperatures reduce global wheat production. Nat Clim Chang 5(2):143–147. https://doi.org/10.1038/nclimate2470
Badger MR, Andrews TJ (1974) Effects of CO2, O2 and temperature on a high-affinity form of ribulose diphosphate carboxylase-oxygenase from spinach. Biochem Biophys Res Commun 60(1):204–210. https://doi.org/10.1016/0006-291X(74)90192-2
Bailey-Serres J, Parker JE, Ainsworth EA, Oldroyd GED, Schroeder JI (2019) Genetic strategies for improving crop yields. Nature 575(7781):109–118. https://doi.org/10.1038/s41586-019-1679-0
Bao H, Morency M, Rianti W, Saeheng S, Roje S, Weber APM, Walker BJ (2021) Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana. Plant Direct 5(12):e366. https://doi.org/10.1002/pld3.366
Bernacchi CJ, Leakey ADB, Heady LE, Morgan PB, Dohleman FG, McGrath JM, Gillespie KM, Wittig VE, Rogers A, Long SP, Ort DR (2006) Hourly and seasonal variation in photosynthesis and stomatal conductance of soybean grown at future CO2 and ozone concentrations for 3 years under fully open-air field conditions. Plant Cell Environ 29(11):2077–2090. https://doi.org/10.1111/j.1365-3040.2006.01581.x
Bernacchi CJ, Morgan PB, Ort DR, Long SP (2005) The growth of soybean under free air [CO2] enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity. Planta 220(3):434–446. https://doi.org/10.1007/s00425-004-1320-8
Betti M, Bauwe H, Busch FA, Fernie AR, Keech O, Levey M, Ort DR, Parry MAJ, Sage R, Timm S, Walker B, Weber APM (2016) Manipulating photorespiration to increase plant productivity: recent advances and perspectives for crop improvement. J Exp Bot 67(10):2977–2988. https://doi.org/10.1093/jxb/erw076
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:1–18
Breuer L, Eckhardt K, Frede HG (2003) Plant parameter values for models in temperate climates. Ecol Model 169:237–293
Burgess AJ, Masclaux-Daubresse C, Strittmatter G, Weber APM, Taylor SH, Harbinson J, Yin X, Long S, Paul MJ, Westhoff P, Loreto F, Ceriotti A, Saltenis VLR, Pribil M, Nacry P, Scharff LB, Jensen PE, Muller B, Cohan J-P, Foulkes J, Rogowsky P, Debaeke P, Meyer C, Nelissen H, Inzé D, Klein Lankhorst R, Parry MAJ, Murchie EH, Baekelandt A (2023) Improving crop yield potential: underlying biological processes and future prospects. Food Energy Secur 12(1):e435. https://doi.org/10.1002/fes3.435
Burke MB, Lobell DB, Guarino L (2009) Shifts in African crop climates by 2050, and the implications for crop improvement and genetic resources conservation. Glob Environ Chang 19(3):317–325. https://doi.org/10.1016/j.gloenvcha.2009.04.003
Busch FA, Sage RF (2017) The sensitivity of photosynthesis to O2 and CO2 concentration identifies strong Rubisco control above the thermal optimum. New Phytol 213(3):1036–1051. https://doi.org/10.1111/nph.14258
Carmo-Silva E, Scales JC, Madgwick PJ, Parry MAJ (2015) Optimizing Rubisco and its regulation for greater resource use efficiency. Plant Cell Environ 38(9):1817–1832. https://doi.org/10.1111/pce.12425
Cavanagh AP, Slattery R, Kubien DS (2023) Temperature-induced changes in Arabidopsis Rubisco activity and isoform expression. J Exp Bot 74(2):651–663. https://doi.org/10.1093/jxb/erac379
Cavanagh AP, South PF, Bernacchi CJ, Ort DR (2022) Alternative pathway to photorespiration protects growth and productivity at elevated temperatures in a model crop. Plant Biotechnol J 20(4):711–721. https://doi.org/10.1111/pbi.13750
Ciais P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, … Thornton P. 2013. Carbon and other biogeochemical cycles. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (eds T.F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S.K. Allen, J. Boschung, … P.M. Midgley), pp. 465–570. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA.
Chen T, Riaz S, Davey P, Zhao Z, Sun Y, Dykes GF, Zhou F, Hartwell J, Lawson T, Nixon PJ, Lin Y, Liu L-N (2022) Producing fast and active Rubisco in tobacco to enhance photosynthesis. Plant Cell 35(2):795–807. https://doi.org/10.1093/plcell/koac348
Coumou D, Robinson A (2013) Historic and future increase in the global land area affected by monthly heat extremes. Environ Res Lett 8:034018
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. https://doi.org/10.1073/pnas.230451497
Crafts-Brandner SJ, van de Loo FJ, Salvucci ME (1997) The two forms of Ribulose-1,5-bisphosphate carboxylase/oxygenase activase differ in sensitivity to elevated temperature. Plant Physiol 114(2):439–444. https://doi.org/10.1104/pp.114.2.439
Dalal J, Lopez H, Vasani NB, Hu Z, Swift JE, Yalamanchili R, Dvora M, Lin X, Xie D, Qu R, Sederoff HW (2015) A photorespiratory bypass increases plant growth and seed yield in biofuel crop Camelina sativa. Biotechnol Biofuels 8(1):175. https://doi.org/10.1186/s13068-015-0357-1
Degen GE, Worrall D, Carmo-Silva E (2020) An isoleucine residue acts as a thermal and regulatory switch in wheat Rubisco activase. Plant J 103(2):742–751. https://doi.org/10.1111/tpj.14766
Deryng D, Conway D, Ramankutty N, Price J, Warren R (2014) Global crop yield response to extreme heat stress under multiple climate change futures. Environ Res Lett 9:034011
Dusenge ME, Duarte AG, Way DA (2019) Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol 221(1):32–49. https://doi.org/10.1111/nph.15283
Dwyer SA, Ghannoum O, Nicotra A, von Caemmerer S (2007) High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry. Plant, Cell Environ 30:53–66
Eisenhut M, Roell M-S, Weber APM (2019) Mechanistic understanding of photorespiration paves the way to a new green revolution. New Phytol 223(4):1762–1769. https://doi.org/10.1111/nph.15872
Estill K, Delaney RH, Smith WK, Ditterline RL (1991) Water relations and productivity of alfalfa leaf chlorophyll variants. Crop Sci 31:1229–1233
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
Feng L, Wang K, Li Y, Tan Y, Kong J, Li H, Li Y, Zhu Y (2007) Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Rep 26(9):1635–1646. https://doi.org/10.1007/s00299-006-0299-y
Ferguson JN, Tidy AC, Murchie EH, Wilson ZA (2021) The potential of resilient carbon dynamics for stabilizing crop reproductive development and productivity during heat stress. Plant Cell Environ 44(7):2066–2089. https://doi.org/10.1111/pce.14015
Flügel F, Timm S, Arrivault S, Florian A, Stitt M, Fernie AR, Bauwe H (2017) The Photorespiratory metabolite 2-phosphoglycolate regulates photosynthesis and starch accumulation in Arabidopsis. Plant Cell 29(10):2537–2551. https://doi.org/10.1105/tpc.17.00256
Forster P, Ramaswamy V, Artaxo P, Berntsen T, Betts R, Fahey D, Haywood J, Lean J, Lowe D, Myhre G, Nganga J, Prinn R, Raga G, Schulz M, Van Dorland R (2008) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the IPCC, S. Solomon et al. (eds.), Cambridge University Press, Cambridge, UK, Chapter 2
Friedlingstein P, O’Sullivan M, Jones MW, Andrew RM, Gregor L, Hauck J, Le Quéré C, Luijkx IT, Olsen A, Peters GP, Peters W, Pongratz J, Schwingshackl C, Sitch S, Canadell JG, Ciais P, Jackson RB, Alin SR, Alkama R, Arneth A, Arora VK, Bates NR, Becker M, Bellouin N, Bittig HC, Bopp L, Chevallier F, Chini LP, Cronin M, Evans W, Falk S, Feely RA, Gasser T, Gehlen M, Gkritzalis T, Gloege L, Grassi G, Gruber N, Gürses Ö, Harris I, Hefner M, Houghton RA, Hurtt GC, Iida Y, Ilyina T, Jain AK, Jersild A, Kadono K, Kato E, Kennedy D, Klein Goldewijk K, Knauer J, Korsbakken JI, Landschützer P, Lefèvre N, Lindsay K, Liu J, Liu Z, Marland G, Mayot N, McGrath MJ, Metzl N, Monacci NM, Munro DR, Nakaoka SI, Niwa Y, O’Brien K, Ono T, Palmer PI, Pan N, Pierrot D, Pocock K, Poulter B, Resplandy L, Robertson E, Rödenbeck C, Rodriguez C, Rosan TM, Schwinger J, Séférian R, Shutler JD, Skjelvan I, Steinhoff T, Sun Q, Sutton AJ, Sweeney C, Takao S, Tanhua T, Tans PP, Tian X, Tian H, Tilbrook B, Tsujino H, Tubiello F, van der Werf GR, Walker AP, Wanninkhof R, Whitehead C, Willstrand Wranne A, Wright R, Yuan W, Yue C, Yue X, Zaehle S, Zeng J, Zheng B (2022) Global Carbon Budget 2022. Earth Syst Sci Data 14(11):4811–4900. https://doi.org/10.5194/essd-14-4811-2022
Fu X, Gregory LM, Weise SE, Walker BJ (2023) Integrated flux and pool size analysis in plant central metabolism reveals unique roles of glycine and serine during photorespiration. Nat Plants 9(1):169–178. https://doi.org/10.1038/s41477-022-01294-9
Fukayama H, Mizumoto A, Ueguchi C, Katsunuma J, Morita R, Sasayama D, Hatanaka T, Azuma T (2018) Expression level of Rubisco activase negatively correlates with Rubisco content in transgenic rice. Photosynth Res 137(3):465–474. https://doi.org/10.1007/s11120-018-0525-9
Fukayama H, Ueguchi C, Nishikawa K, Katoh N, Ishikawa C, Masumoto C, Hatanaka T, Misoo S (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
Garcia A, Gaju O, Bowerman AF, Buck SA, Evans JR, Furbank RT, Gilliham M, Millar AH, Pogson BJ, Reynolds MP, Ruan Y-L, Taylor NL, Tyerman SD, Atkin OK (2023) Enhancing crop yields through improvements in the efficiency of photosynthesis and respiration. New Phytol 237(1):60–77. https://doi.org/10.1111/nph.18545
Genesio L, Bassi R, Migiletta F (2021) Plants with less chlorophyll. A global change perspective. Glob Chang Biol 27:959–967
Grodzinski B, Butt VS (1976) Hydrogen peroxide production and the release of carbon dioxide during glycolate oxidation in leaf peroxisomes. Planta 128(3):225–231. https://doi.org/10.1007/BF00393233
Gunn LH, Martin Avila E, Birch R, Whitney SM (2020) The dependency of red Rubisco on its cognate activase for enhancing plant photosynthesis and growth. Proc Natl Acad Sci USA 117(41):25890–25896. https://doi.org/10.1073/pnas.2011641117
Hagemann M, Bauwe H (2016) Photorespiration and the potential to improve photosynthesis. Curr Opin Chem Biol 35:109–116. https://doi.org/10.1016/j.cbpa.2016.09.014
Hatfield JL, Boote KJ, Kimball BA, Ziska L, Izaurralde RC, Ort DR, Thomson AM, Wolfe D (2011) Climate impacts on agriculture: implications for crop production. Agron J 103:351–370
Hatfield J, Carlson RE (1979) Light quality distributions and spectral albedo of three maize canopies. Agric Meteorol 20:215–226
Hedhly A, Hormaza JI, Herrero M (2009) Global warming and sexual plant reproduction. Trends Plant Sci 14(1):30–36
Heineke D, Bykova N, Gardeström P, Bauwe H (2001) Metabolic response of potato plants to an antisense reduction of the P-protein of glycine decarboxylase. Planta 212(5):880–887. https://doi.org/10.1007/s004250000460
Hendrickson L, Sharwood R, Ludwig M, Whitney SM, Badger MR, von Caemmerer S (2008) The effects of Rubisco activase on C4 photosynthesis and metabolism at high temperature. J Exp Bot 59:1789–1798
IPCC (2018) Summary for policymakers. In: Global warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change,. (eds V. Masson-Delmotte, P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P.R. Shukla, … T. Waterfield), World Meteorological Organization, Geneva, Switzerland, 32 pp.
Jagadish SVK (2020) Heat stress during flowering in cereals—effects and adaptation strategies. New Phytol 226:1567–1572
Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, Stäbler N, Schönfeld B, Kreuzaler F, Peterhänsel C (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat Biotechnol 25(5):593–599. https://doi.org/10.1038/nbt1299
Kim SY, Slattery RA, Ort DR (2021) A role for differential Rubisco activase isoform expression in C4 bioenergy grasses at high temperature. GCB Bioenergy 13(1):211–223. https://doi.org/10.1111/gcbb.12768
Köhler IH, Ruiz-Vera UM, VanLoocke A, Thomey ML, Clemente T, Long SP, Ort DR, Bernacchi CJ (2016) Expression of cyanobacterial FBP/SBPase in soybean prevents yield depression under future climate conditions. J Exp Bot 68(3):715–726. https://doi.org/10.1093/jxb/erw435
Kubien DS, von Caemmerer S, Furbank RT, Sage RF (2003) C4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of Rubisco. Plant Physiol 132:1577–1585
Kumar A, Li C, Portis AR (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. https://doi.org/10.1007/s11120-009-9438-y
Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L, Lassner MW, Zhu G (2007) Enhanced thermostability of Arabidopsis Rubisco Activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19(10):3230–3241. https://doi.org/10.1105/tpc.107.054171
Law RD, Crafts-Brandner SJ (2001) High temperature stress increases the expression of wheat leaf Ribulose-1,5-Bisphosphate Carboxylase/oxygenase Activase Protein. Arch Biochem Biophys 386(2):261–267. https://doi.org/10.1006/abbi.2000.2225
Lin MT, Occhialini A, Andralojc PJ, Parry MAJ, Hanson MR (2014) A faster Rubisco with potential to increase photosynthesis in crops. Nature 513(7519):547–550. https://doi.org/10.1038/nature13776
Lobell DB, Gourdji SM (2012) The influence of climate change on global crop productivity. Plant Physiol 160:1686–1697
Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–62
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. https://doi.org/10.1016/j.cell.2015.03.019
López-Calcagno PE, Fisk S, Brown KL, Bull SE, South PF, Raines CA (2019) Overexpressing the H-protein of the glycine cleavage system increases biomass yield in glasshouse and field-grown transgenic tobacco plants. Plant Biotechnol J 17(1):141–151. https://doi.org/10.1111/pbi.12953
Maier A, Fahnenstich H, von Caemmerer S, Engqvist M, Weber A, Flügge U-I, Maurino V (2012) Transgenic introduction of a glycolate oxidative cycle into A. thaliana chloroplasts leads to growth improvement. Front Plant Sci. https://doi.org/10.3389/fpls.2012.00038
Manning T, Birch R, Stevenson T, Nugent G, Whitney S (2023) Bacterial Form II Rubisco can support wild-type growth and productivity in Solanum tuberosum cv. Desiree (potato) under elevated CO2. PNAS Nexus. https://doi.org/10.1093/pnasnexus/pgac305
Mao Y, Catherall E, Díaz-Ramos A, Greiff GRL, Azinas S, Gunn L, McCormick AJ (2022) The small subunit of Rubisco and its potential as an engineering target. J Exp Bot 74(2):543–561. https://doi.org/10.1093/jxb/erac309
Martin-Avila E, Lim Y-L, Birch R, Dirk LMA, Buck S, Rhodes T, Sharwood RE, Kapralov MV, Whitney SM (2020) Modifying plant photosynthesis and growth via simultaneous chloroplast transformation of Rubisco large and small subunits. Plant Cell 32(9):2898–2916. https://doi.org/10.1105/tpc.20.00288
McGrath JM, Long SP (2014) Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiol 164(4):2247–2261. https://doi.org/10.1104/pp.113.232611
Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997
Moore CE, Meacham-Hensold K, Lemonnier P, Slattery RA, Benjamin C, Bernacchi CJ, Lawson T, Cavanagh AP (2021) The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. J Exp Bot 72(8):2822–2844. https://doi.org/10.1093/jxb/erab090
Nayak L, Panda D, Dash GK, Lal MK, Swain P, Baig MJ, Kumar A (2022) A chloroplast glycolate catabolic pathway bypassing the endogenous photorespiratory cycle enhances photosynthesis, biomass and yield in rice (Oryza sativa L.). Plant Sci 314:103. https://doi.org/10.1016/j.plantsci.2021.111103
National Agricultural Statistics Service (2016) United States Department of Agriculture (USDA), “Quick Stats 2.0”. Retrieved from https://quickstats.nass.usda.gov/
Occhialini A, Lin MT, Andralojc PJ, Hanson MR, Parry MAJ (2016) Transgenic tobacco plants with improved cyanobacterial Rubisco expression but no extra assembly factors grow at near wild-type rates if provided with elevated CO2. Plant J 85(1):148–160. https://doi.org/10.1111/tpj.13098
Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Annu Rev Plant Physiol 35(1):415–442. https://doi.org/10.1146/annurev.pp.35.060184.002215
Peterhansel C, Horst I, Niessen M, Blume C, Kebeish R, Kürkcüoglu S, Kreuzaler F 2010. Photorespiration. The Arabidopsis Book 2010 (8)
Peterhansel C, Krause K, Braun H-P, Espie GS, Fernie AR, Hanson DT, Keech O, Maurino VG, Mielewczik M, Sage RF (2013) Engineering photorespiration: current state and future possibilities. Plant Biol 15(4):754–758. https://doi.org/10.1111/j.1438-8677.2012.00681.x
Perdomo JA, Capo-Bauca S, Carmo-Silva E, Galmes J (2017) 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 8:490
Pittermann J, Sage RF (2001) The response of the high altitude C4 grass Muhlenbergia montana (Nutt.) to long- and short-term chilling. J Exp Bot 52:829–838
Population facts (2019) UN Department of Economic and Social Affairs Population Facts Dec 2018 No. 2019/6. Retrieved from: www.un.org › pdf › popfacts
Qu Y, Mueller-Cajar O, Yamori W (2022) Improving plant heat tolerance through modification of Rubisco activase in C3 plants to secure crop yield and food security in a future warming world. J Exp Bot 74(2):591–599. https://doi.org/10.1093/jxb/erac340
Qu Y, Sakoda K, Fukayama H, Kondo E, Suzuki Y, Makino A, Terashima I, Yamori W (2021) Overexpression of both Rubisco and Rubisco activase rescues rice photosynthesis and biomass under heat stress. Plant Cell Environ 44(7):2308–2320. https://doi.org/10.1111/pce.14051
Raines CA (2003) The Calvin cycle revisited. Photosynth Res 75(1):1–10. https://doi.org/10.1023/A:1022421515027
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. J Exp Bot 53(369):609–620
Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30(9):1086–1106. https://doi.org/10.1111/j.1365-3040.2007.01682.x
Scafaro AP, Atwell BJ, Muylaert S, Reusel BV, Ruiz GA, Rie JV, Gallé A (2018) A thermotolerant variant of Rubisco Activase From a wild relative improves growth and seed yield in rice under heat stress. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01663
Scafaro AP, Bautsoens N, den Boer B, Van Rie J, Gallé A (2019) A conserved sequence from heat-adapted species improves Rubisco Activase thermostability in wheat. Plant Physiol 181(1):43–54. https://doi.org/10.1104/pp.19.00425
Scafaro AP, Gallé A, Van Rie J, Carmo-Silva E, Salvucci ME, Atwell BJ (2016) Heat tolerance in a wild Oryza species is attributed to maintenance of Rubisco activation by a thermally stable Rubisco activase ortholog. New Phytol 211(3):899–911. https://doi.org/10.1111/nph.13963
Schrader SM, Wise RR, Wacholtz WF, Ort DR, Sharkey TD (2004) Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant Cell Environ 27(6):725–735. https://doi.org/10.1111/j.1365-3040.2004.01172.x
Schulz L, Guo Z, Zarzycki J, Steinchen W, Schuller JM, Heimerl T, Prinz S, Mueller-Cajar O, Erb TJ, Hochberg GKA (2022) Evolution of increased complexity and specificity at the dawn of form I Rubiscos. Science 378(6616):155–160. https://doi.org/10.1126/science.abq1416
Shen B-R, Wang L-M, Lin X-L, Yao Z, Xu H-W, Zhu C-H, Teng H-Y, Cui L-L, Liu EE, Zhang J-J, He Z-H, Peng X-X (2019) Engineering a new chloroplastic photorespiratory bypass to Increase photosynthetic efficiency and productivity in rice. Mol Plant 12(2):199–214. https://doi.org/10.1016/j.molp.2018.11.013
Shivhare D, Mueller-Cajar O (2017) In vitro characterization of thermostable CAM Rubisco activase reveals a Rubisco interacting surface loop. Plant Physiol 174(3):1505–1516. https://doi.org/10.1104/pp.17.00554
Siebers MH, Yendrek CR, Drag D, Locke AM, Rios Acosta L, Leakey AD, Ainsworth EA, Bernacchi CJ, Ort DR (2015) Heat waves imposed during early pod development in soybean (Glycine max) cause significant yield loss despite a rapid recovery from oxidative stress. Glob Chang Biol 21:3114–3125
Simkin AJ, Lopez-Calcagno PE, Davey PA, Headland LR, Lawson T, Timm S, Bauwe H, Raines CA (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. https://doi.org/10.1111/pbi.12676
Singarayer JS, Ridgwell A, Irvine P (2009) Assessing the benefits of crop albedo bio-geoengineering. Environ Res Lett 4(4):045110
Slattery RA, Ort DR (2019) Carbon assimilation in crops at high temperatures. Plant Cell Environ 42(10):2750–2758. https://doi.org/10.1111/pce.13572
Slattery RA, Ort DR (2021) Perspectives on improving light energy distribution and light use efficiency in crop canopies. Plant Physiol 185:34–48
Slattery RA, Vanloocke A, Bernacchi CJ, Zhu X-G, Ort DR (2017) Photosynthesis, light use efficiency, and yield of reduced chlorophyll soybean mutants in field conditions. Front Plant Sci 8:549
Solomon S, Plattner GK, Knutti R, Friedlingstein P (2009) Irreversible climate change due to carbon dioxide emissions. Proc Natl Acad Sci USA 106:1704–1709
South PF, Cavanagh AP, Liu HW, Ort DR (2019) Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363(6422):eaat9077. https://doi.org/10.1126/science.aat9077
State of the Climate in Africa (2019) (WMO-No. 1253) Retrieved from: https://library.wmo.int/index.php?lvl=notice_display&id=21778#.Y_PCPrTMLUK
State of the Climate in Africa (2021) (WMO-No.1300) Retrieved from: https://public.wmo.int/en/resources/library/state-of-climate-africa-2021-0
Suganami M, Suzuki Y, Tazoe Y, Yamori W, Makino A (2020) 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
Teixeira EI, Fischer G, van Velthuizen H, Walter C, Ewert F (2013) Global hot-spots of heat stress on agricultural crops due to climate change. Agric for Meteorol 170:206–215
Thomey ML, Slattery RA, Köhler I, Bernacchi CJ, Ort DR (2019) Yield response of field-grown soybean exposed to heat waves under current and elevated [CO2]. Glob Chang Biol 25:4352–4368
Timm S, Bauwe H (2013) The variety of photorespiratory phenotypes—employing the current status for future research directions on photorespiration. Plant Biol 15(4):737–747. https://doi.org/10.1111/j.1438-8677.2012.00691.x
Timm S, Florian A, Arrivault S, Stitt M, Fernie AR, Bauwe H (2012) Glycine decarboxylase controls photosynthesis and plant growth. FEBS Lett 586(20):3692–3697. https://doi.org/10.1016/j.febslet.2012.08.027
Timm S, Wittmiß M, Gamlien S, Ewald R, Florian A, Frank M, Wirtz M, Hell R, Fernie AR, Bauwe H (2015) Mitochondrial dihydrolipoyl dehydrogenase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana. Plant Cell 27(7):1968–1984. https://doi.org/10.1105/tpc.15.00105
Timm S, Woitschach F, Heise C, Hagemann M, Bauwe H (2019) Faster removal of 2-phosphoglycolate through photorespiration improves abiotic stress tolerance of Arabidopsis. Plants 8(12):563
Uddin MN, Marshal DR (1988) Variation in epicuticular wax content in wheat. Euphytica 38:3–9
von Caemmerer S, Furbank RT (2016) Strategies for improving C4 photosynthesis. Curr Opin Plant Biol 31:125–134
Walker BJ, Drewry DT, Slattery RA, Vanloocke A, Cho YB, Ort DR (2018) Chlorophyll can be reduced in crop canopies with little penalty to photosynthesis. Plant Physiol 176:1215–1232
Walker BJ, VanLoocke A, Bernacchi CJ, Ort DR (2016) The costs of photorespiration to food production now and in the future. Annu Rev Plant Biol 67(1):107–129. https://doi.org/10.1146/annurev-arplant-043015-111709
Wang L, Huang J, Luo Y, Yao Y, Zhao Z (2015) Changes in extremely hot summers over the global land area under various warming targets. PLoS ONE 10:1–11
Wang L-M, Shen B-R, Li B-D, Zhang C-L, Lin M, Tong P-P, Cui L-L, Zhang Z-S, Peng X-X (2020) A synthetic photorespiratory shortcut enhances photosynthesis to boost biomass and grain yield in rice. Mol Plant 13(12):1802–1815. https://doi.org/10.1016/j.molp.2020.10.007
Whitney SM, Andrews TJ (2003) Photosynthesis and growth of tobacco with a substituted bacterial Rubisco mirror the properties of the introduced Enzyme. Plant Physiol 133(1):287–294. https://doi.org/10.1104/pp.103.026146
Xu H, Zhang J, Zeng J, Jiang L, Liu E, Peng C, He Z, Peng X (2009) Inducible antisense suppression of glycolate oxidase reveals its strong regulation over photosynthesis in rice. J Exp Bot 60(6):1799–1809. https://doi.org/10.1093/jxb/erp056
Yoon D-K, Ishiyama K, Suganami M, Tazoe Y, Watanabe M, Imaruoka S, Ogura M, Ishida H, Suzuki Y, Obara M, Mae T, Makino A (2020) Transgenic rice overproducing Rubisco exhibits increased yields with improved nitrogen-use efficiency in an experimental paddy field. Nature Food 1(2):134–139. https://doi.org/10.1038/s43016-020-0033-x
Zelitch I (1989) Selection and characterization of tobacco plants with novel O2-resistant photosynthesis. Plant Physiol 90(4):1457–1464. https://doi.org/10.1104/pp.90.4.1457
Zhu X-G, de Sturler E, Long SP (2007) Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiol 145(2):513–526. https://doi.org/10.1104/pp.107.103713
Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, Huang M, Yao Y, Bassu S, Ciais P, Durand J-L, Elliott J, Ewert F, Janssens IA, Li T, Lin E, Liu Q, Martre P, Müller C, Peng S, Peñuelas J, Ruane AC, Wallach D, Wang T, Wu D, Liu Z, Zhu Y, Zhu Z, Asseng S (2017) Temperature increase reduces global yields of major crops in four independent estimates. Proc Nat Acad Sci 114 (35):9326–9331. https://doi.org/10.1073/pnas.1701762114
Acknowledgements
This work is supported by the research project Realizing Increased Photosynthetic Efficiency (RIPE) that is funded by the Bill & Melinda Gates Foundation, Foundation for Food and Agriculture Research, and U.K. Foreign, Commonwealth & Development Office under grant no. OPP1172157.
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Cavanagh, A.P., Ort, D.R. Transgenic strategies to improve the thermotolerance of photosynthesis. Photosynth Res 158, 109–120 (2023). https://doi.org/10.1007/s11120-023-01024-y
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DOI: https://doi.org/10.1007/s11120-023-01024-y