Citation: | ZHANG Zhisheng, ZHU Guohui, PENG Xinxiang. Advances in improvement of crop photosynthetic efficiency by optimizing the photosynthetic carbon assimilation[J]. Journal of South China Agricultural University, 2022, 43(6): 69-77. DOI: 10.7671/j.issn.1001-411X.202208012 |
With the continuing growth of population and the decrease in arable lands, the global food crisis is becoming a serious problem for human beings. Therefore, further improving crop yield is important for our country to ensure food production safety. Photosynthesis is the material basis for crop yield, and the crop improvement focusing on increasing photosynthetic efficiency via modern breeding technologies is considered to be a new round of “Green revolution”. In this review, we summarize recent advances, current challenges, and applications in enhancing plant carbon assimilation through different approaches, including improving the carboxylation activity of Rubisco, introducing C4 photosynthesis into C3 crops, and reducing photorespiration. We also propose promising research emphasis and directions for imporving photosynthetic carbon assimilation of plants.
[1] |
ZHU X, LONG S P, ORT D R. Improving photosynthetic efficiency for greater yield[J]. Annual Review of Plant Biology, 2010, 61(1): 235-261. doi: 10.1146/annurev-arplant-042809-112206
|
[2] |
ZHU X, LONG S P, ORT D R. What is the maximum efficiency with which photosynthesis can convert solar energy into biomass?[J]. Current Opinion in Biotechnology, 2008, 19(2): 153-159. doi: 10.1016/j.copbio.2008.02.004
|
[3] |
程建峰, 沈允钢. 作物高光效之管见[J]. 作物学报, 2010, 36(8): 1235-1247.
|
[4] |
LONG S P, MARSHALL-COLON A, ZHU X. Meeting the global food demand of the future by engineering crop photosynthesis and yield potential[J]. Cell, 2015, 161(1): 56-66.
|
[5] |
张立新, 卢从明, 彭连伟, 等. 利用合成生物学原理提高光合作用效率的研究进展[J]. 生物工程学报, 2017, 33(3): 486-493. doi: 10.13345/j.cjb.160486
|
[6] |
ORT D R, ZHU X, MELIS A. Optimizing antenna size to maximize photosynthetic efficiency[J]. Plant Physiology, 2011, 155(1): 79-85. doi: 10.1104/pp.110.165886
|
[7] |
SOUTH P F, CAVANAGH A P, LOPEZ-CALCAGNO P E, et al. Optimizing photorespiration for improved crop productivity[J]. Journal of Integrative Plant Biology, 2018, 60(12): 1217-1230.
|
[8] |
BUICK R. When did oxygenic photosynthesis evolve?[J]. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 2008, 363(1504): 2731-2743.
|
[9] |
KASTING J F, HOWARD M T. Atmospheric composition and climate on the early Earth[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 2006, 361(1474): 1733-1742. doi: 10.1098/rstb.2006.1902
|
[10] |
TABITA F R, HANSON T E, LI H, et al. Function, structure, and evolution of the Rubisco-like proteins and their Rubisco homologs[J]. Microbiology and Molecular Biology Reviews, 2007, 71(4): 576-599.
|
[11] |
BADGER M R, BEK E J. Multiple Rubisco forms in proteobacteria: Their functional significance in relation to CO2 acquisition by the CBB cycle[J]. Journal of Experimental Botany, 2008, 59(7): 1525-1541. doi: 10.1093/jxb/erm297
|
[12] |
PETERHANSEL C, HORST I, NIESSEN M, et al. Photorespiration[J]. The Arabidopsis Book, 2010, 8: e130.
|
[13] |
FERNIE A R, BAUWE H. Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratorypathway[J]. The Plant Journal, 2020, 102(4): 666-677.
|
[14] |
IÑIGUEZ C, CAPÓ BAUÇÀ S, NIINEMETS Ü, et al. Evolutionary trends in Rubisco kinetics and their co-evolution with CO2 concentrating mechanisms[J]. The Plant Journal, 2020, 101(4): 897-918.
|
[15] |
GALMES J, KAPRALOV M V, ANDRALOJC P J, et al. Expanding knowledge of the Rubisco kinetics variability in plant species: Environmental and evolutionary trends[J]. Plant Cell and Environment, 2014, 37(9): 1989-2001.
|
[16] |
WHITNEY S M, HOUTZ R L, ALONSO H. Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme, Rubisco[J]. Plant Physiology, 2011, 155(1): 27-35.
|
[17] |
BUSCH F A. Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism[J]. The Plant Journal, 2020, 101(4): 919-939.
|
[18] |
YOUNG J N, HEUREUX A M, SHARWOOD R E, et al. Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms[J]. Journal of Expermental Botany, 2016, 67(11): 3445-3456.
|
[19] |
FLAMHOLZ A I, PRYWES N, MORAN U, et al. Revisiting trade-offs between Rubisco kinetic parameters[J]. Biochemistry, 2019, 58(31): 3365-3376.
|
[20] |
HERMIDA-CARRERA C, KAPRALOV M V, GALMES J. Rubisco catalytic properties and temperature response in crops[J]. Plant Physiology, 2016, 171(4): 2549-2561.
|
[21] |
DONG-KYUNG Y, KEIKI I, MAO S, et al. Transgenic rice overproducing Rubisco exhibits increased yields with improved nitrogen-use efficiency in an experimental paddy field[J]. Nature Food, 2020, 1: 134-139.
|
[22] |
SALESSE-SMITH C E, SHARWOOD R E, BUSCH F A, et al. Overexpression of Rubisco subunits with RAF1 increases Rubisco content in maize[J]. Nature Plants, 2018, 4(10): 802-810.
|
[23] |
MUELLER-CAJAR O. The diverse AAA+ machines that repair inhibited Rubisco active sites[J]. Frontiers in Molecular Biosciences, 2017, 4: 31.
|
[24] |
SCAFARO A P, ATWELL B J, MUYLAERT S, et al. A thermotolerant variant of Rubisco activase from a wild relative improves growth and seed yield in rice under heat stress[J]. Frontiers in Plant Science, 2018, 9: 1663.
|
[25] |
KUMAR A, LI C, PORTIS A J. Arabidopsis thaliana expressing a thermostable chimeric Rubisco activase exhibits enhanced growth and higher rates of photosynthesis at moderately high temperatures[J]. Photosynthesis Research, 2009, 100(3): 143-153.
|
[26] |
ZHU X G, PORTIS A R, LONG S P. Would transformation of C3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis[J]. Plant Cell and Environment, 2004, 27(2): 155-165.
|
[27] |
MORITA K, HATANAKA T, MISOO S, et al. Unusual small subunit that is not expressed in photosynthetic cells alters the catalytic properties of Rubisco in rice[J]. Plant Physiology, 2014, 164(1): 69-79.
|
[28] |
MATSUMURA H, SHIOMI K, YAMAMOTO A, et al. Hybrid Rubisco with complete replacement of rice Rubisco small subunits by sorghum counterparts confers C4 plant-like high catalytic activity[J]. Molecular Plant, 2020, 13(11): 1570-1581.
|
[29] |
TCHERKEZ G G, FARQUHAR G D, ANDREWS T J. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized[J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(19): 7246-7251.
|
[30] |
ISHIKAWA C, HATANAKA T, MISOO S, et al. Screening of high kcat Rubisco among poaceae for improvement of photosynthetic CO2 assimilation in rice[J]. Plant Production Science, 2009, 12(3): 345-350.
|
[31] |
CARMO-SILVA E, SCALES J C, MADGWICK P J, et al. Optimizing Rubisco and its regulation for greater resource use efficiency[J]. Plant, Cell and Environment, 2015, 38(9): 1817-1832.
|
[32] |
LIN M T, OCCHIALINI A, ANDRALOJC P J, et al. A faster Rubisco with potential to increase photosynthesis in crops[J]. Nature, 2014, 513(7519): 547-550.
|
[33] |
SAGE R F, SAGE T L, KOCACINAR F. Photorespiration and the evolution of C4 photosynthesis[M]. Annual Review of Plant Biology, 2012, 63: 19-47.
|
[34] |
VON CAMMERER S, QUICK W P, FURBANK R T. The development of C4 rice: Current progress and future challenges[J]. Science, 2012, 336(6089): 1671-1672.
|
[35] |
GOWIK U, WESTHOFF P. The path from C3 to C4 photosynthesis[J]. Plant Physiology, 2011, 155(1): 56-63.
|
[36] |
VON CAEMMERER S, FURBANK R T. Strategies for improving C4 photosynthesis[J]. Current Opinion in Plant Biology, 2016, 31: 125-134.
|
[37] |
HIBBERD J M, SHEEHY J E, LANGDALE J A. Using C4 photosynthesis to increase the yield of rice-rationale and feasibility[J]. Current Opinion in Plant Biology, 2008, 11(2): 228-231.
|
[38] |
KAJALA K, COVSHOFF S, KARKI S, et al. Strategies for engineering a two-celled C4 photosynthetic pathway into rice[J]. Journal of Experimental Botany, 2011, 62(9): 3001-3010.
|
[39] |
SCHULER M L, MANTEGAZZA O, WEBER A P. Engineering C4 photosynthesis into C3 chassis in the synthetic biology age[J]. The Plant Journal, 2016, 87(1): 51-65.
|
[40] |
KUBIS A, BAR-EVEN A. Synthetic biology approaches for improving photosynthesis[J]. Journal of Experimental Botany, 2019, 70(5): 1425-1433.
|
[41] |
KU M S, AGARIE S, NOMURA M, et al. High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants[J]. Nature Biotechnology, 1999, 17(1): 76-80.
|
[42] |
TANIGUCHI Y, OHKAWA H, MASUMOTO C, et al. Overproduction of C4 photosynthetic enzymes in transgenic rice plants: An approach to introduce the C4-like photosynthetic pathway into rice[J]. Journal of Experimental Botany, 2008, 59(7): 1799-1809.
|
[43] |
MIYAO M, MASUMOTO C, MIYAZAWA S, et al. Lessons from engineering a single-cell C4 photosynthetic pathway into rice[J]. Journal of Experimental Botany, 2011, 62(9): 3021-3029.
|
[44] |
ERMAKOVA M, DANILA F R, FURBANK R T, et al. On the road to C4 rice: Advances and perspectives[J]. The Plant Journal, 2020, 101(4): 940-950.
|
[45] |
TSUCHIDA H, TAMAI T, FUKAYAMA H, et al. High level expression of C4-specific NADP-malic enzyme in leaves and impairment of photoautotrophic growth in a C3 plant, rice[J]. Plant and Cell Physiology, 2001, 42(2): 138-145.
|
[46] |
FAHNENSTICH H, SAIGO M, NIESSEN M, et al. Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C4 NADP-malic enzyme causes accelerated senescence during extended darkness[J]. Plant Physiology, 2007, 145(3): 640-652.
|
[47] |
BATISTA-SILVA W, DA FONSECA-PERETRA P, MARTINS A O, et al. Engineering improved photosynthesis in the era of synthetic biology[J]. Plant Communications, 2020, 1(2): 100032.
|
[48] |
盛阳阳, 徐秀美, 张巧红, 等. 光合作用碳同化的合成生物学研究进展[J/OL]. 合成生物学, [2022-09-06]. http://kns.cnki.net/kcms/detail/10.1687.q.20220630.1823.002.html.
|
[49] |
许大全, 朱新广. 创造“玉米稻”: 禾谷作物高产优质的一个新战略[J]. 植物生理学报, 2020, 56(7): 1313-1320.
|
[50] |
WANG P, KHOSHRAVESH R, KARKI S, et al. Re-creation of a key step in the evolutionary switch from C3 to C4 leaf anatomy[J]. Current Biology, 2017, 27(21): 3278-3287.
|
[51] |
LI X, WANG P, LI J, et al. Maize GOLDEN2-LIKE genes enhance biomass and grain yields in rice by improving photosynthesis and reducing photoinhibition[J]. Communications Biology, 2020, 3(1): 151.
|
[52] |
YEH S, LIN H, CHANG Y, et al. Maize Golden2-like transcription factors boost rice chloroplast development, photosynthesis, and grain yield[J]. Plant Physiology, 2022, 188(1): 442-459.
|
[53] |
WANG P, KARKI S, BISWAL A K, et al. Candidate regulators of early leaf development in maize perturb hormone signaling and secondary cell wall formation when constitutively expressed in rice[J]. Scientific Reports, 2017, 7: 4535.
|
[54] |
LO S F, CHATTERJEE J, BISWAL A K, et al. Closer vein spacing by ectopic expression of nucleotide-binding and leucine-rich repeat proteins in rice leaves[J]. Plant Cell Reports, 2022, 41(2): 319-335.
|
[55] |
LI J, WERADUWAGE S M, PREISER A L, et al. A cytosolic bypass and G6P shunt in plants lacking peroxisomal hydroxypyruvate reductase[J]. Plant Biology, 2019, 180(2): 783-792.
|
[56] |
FLUGEL F, TIMM S, ARRIVAULT S, et al. The photorespiratory metabolite 2-phosphoglycolate regulates photosynthesis and starch accumulation in Arabidopsis[J]. Plant Cell, 2017, 29(10): 2537-2551. doi: 10.1105/tpc.17.00256
|
[57] |
HAGEMANN M, BAUWE H. Photorespiration and the potential to improve photosynthesis[J]. Current Opinion in Chemical Biology, 2016, 35: 109-116.
|
[58] |
BAUWE H, HAGEMANN M, FERNIE A R. Photorespiration: Players, partners and origin[J]. Trends in Plant Science, 2010, 15(6): 330-336. doi: 10.1016/j.tplants.2010.03.006
|
[59] |
WALKER B J, VANLOOCKE A, BERNACCHI C J, et al. The costs of photorespiration to food production now and in the future[J]. Annual Review of Plant Biology, 2016, 67(1): 107-129. doi: 10.1146/annurev-arplant-043015-111709
|
[60] |
张智胜, 彭新湘. 光呼吸的功能及其平衡调控[J]. 植物生理学报, 2016, 52(11): 1692-1702. doi: 10.13592/j.cnki.ppj.2016.1017
|
[61] |
EHLERS I, AUGUSTI A, BETSON T R, et al. Detecting long-term metabolic shifts using isotopomers: CO2-driven suppression of photorespiration in C3 plants over the 20th century[J]. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(51): 15585-15590.
|
[62] |
KEBEISH R, NIESSEN M, THIRUVEEDHI K, et al. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana[J]. Nature Biotechnology, 2007, 25(5): 593-599. doi: 10.1038/nbt1299
|
[63] |
DALAL J, LOPEZ H, VASANI N B, et al. A photorespiratory bypass increases plant growth and seed yield in biofuel crop Camelina sativa[J]. Biotechnology for Biofuels, 2015, 8: 175.
|
[64] |
AHMAD R, BILAL M, JEON J, et al. Improvement of biomass accumulation of potato plants by transformation of cyanobacterial photorespiratory glycolate catabolism pathway genes[J]. Plant Biotechnology Reports, 2016, 10(5): 269-276. doi: 10.1007/s11816-016-0403-x
|
[65] |
SHEN B, WANG L, LIN X, et al. Engineering a new chloroplastic photorespiratory bypass to increase photosynthetic efficiency and productivity in rice[J]. Molecular Plant, 2019, 12(2): 199-214. doi: 10.1016/j.molp.2018.11.013
|
[66] |
SOUTH P F, CAVANAGH A P, LIU H W, et al. Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field[J]. Science, 2019, 363(6422): 45-53/eaat9077. doi: 10.1126/science.aat9077
|
[67] |
WANG L, SHEN B, LI B, et al. A synthetic photorespiratory shortcut enhances photosynthesis to boost biomass and grain yield in rice[J]. Molecular plant, 2020, 13(12): 1802-1815. doi: 10.1016/j.molp.2020.10.007
|
[68] |
MAIER A, FAHNENSTICH H, VON CAEMMERER S, et al. Transgenic introduction of a glycolate oxidative cycle into A. thaliana chloroplasts leads to growth improvement[J]. Frontiers in Plant Science, 2012, 3: 38.
|
[69] |
CAVANAGH A P, SOUTH P F, BERNACCHI C J, et al. Alternative pathway to photorespiration protects growth and productivity at elevated temperatures in a model crop[J]. Plant Biotechnology Journal, 2022, 20(4): 711-721.
|
[70] |
XIN C, THOLEN D, DEVLOO V, et al. The benefits of photorespiratory bypasses: How can they work?[J]. Plant Physiology, 2015, 167(2): 574-585. doi: 10.1104/pp.114.248013
|
[71] |
PETERHANSEL C, KRAUSE K, BRAUN H P, et al. Engineering photorespiration: Current state and future possibilities[J]. Plant Biology, 2013, 15(4): 754-758. doi: 10.1111/j.1438-8677.2012.00681.x
|
[72] |
LUNDGREN M R. C2 photosynthesis: A promising route towards crop improvement?[J]. New Phytologist, 2020, 228: 1679.
|
[73] |
TIMM S, WITTMIß M, GAMLIEN S, et al. Mitochondrial dihydrolipoyl dehydrogenase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana[J]. The Plant Cell, 2015, 27(7): 1968-1984. doi: 10.1105/tpc.15.00105
|
[74] |
LÓPEZ-CALCAGNO P E, FISK S, BROWN K L, et al. Overexpressing the H-protein of the glycine cleavage system increases biomass yield in glasshouse and field-grown transgenic tobacco plants[J]. Plant Biotechnology Journal, 2019, 17(1): 141-151. doi: 10.1111/pbi.12953
|
[75] |
SIMKIN A J, MCAUSLAND L, HEADLAND L R, et al. Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield in tobacco[J]. Journal of Experimental Botany, 2015, 66(13): 4075-4090.
|
[76] |
肖璞, 刘虎虎, 王翀, 等. 植物高光效研究进展[J]. 生物学杂志, 2020, 37(2): 88-91. doi: 10.3969/j.issn.2095-1736.2020.02.088
|
[77] |
WEI S, LI X, LU Z, et al. A transcriptional regulator that boosts grain yields and shortens the growth duration of rice[J]. Science, 2022, 377(6604): eabi8455/386-395.
|