Evolution and Functional Analysis of Maize Gene ZmC4NADP-ME

doi:10.7668/hbnxb.20195463

Abstract

Abstract:

To explore the function of key genes in photosynthesis, a functional knockout mutant (zmC₄nadp-me) of ZmC₄NADP-ME, the gene encoding the rate-limiting enzyme of the dark reaction of photosynthesis in maize, was obtained. Evolutionary tree analysis showed that ZmC₄NADP-ME and its homologous genes exist in multiple copies in most plants, with diverse expression patterns. Phenotypic analysis revealed that the entire zmC₄nadp-me plant was yellow-green, and its seedling-stage leaves dried up and died rapidly under light. Chlorophyll fluorescence analysis indicated that Y(Ⅱ) and electron transport rate ETR(Ⅱ) of photosystem Ⅱ (PSⅡ) in zmC₄nadp-me decreased significantly, with little change in Y(NPQ), while the Y(NO) increased notably. Measurement of the absorption capacity (P700) of photosystem Ⅰ (PSⅠ) found that both the electron transport rate (ETR(Ⅰ)) and the actual photoelectron efficiency (Y(Ⅰ)) of zmC₄nadp-me dropped substantially, and the gap widened with increasing light intensity. Under specific light intensities, Y(ND) and Y(NA) of zmC₄nadp-me were greater than those of the wild type (WT). In conclusion, ZmC₄NADP-ME is essential for plant growth and development. Disruption of this gene severely stresses PSⅡ, and the plant can't alleviate this stress by increasing Y(NPQ). Meanwhile, at low light intensities, the inhibition of PSⅠ may originate from the electron donor side of PSⅠ, and as the light intensity increases, the inhibition from the electron acceptor side of PSⅠ becomes a key factor.

Key words: Maize, Photosynthesis, Malate enzyme, PS Ⅰ, PS Ⅱ

CHEN Huafeng, ZHANG Jianing, ZHANG Xiao, YUAN Yue, LIU Xiufeng, LIU Dan. Evolution and Functional Analysis of Maize Gene ZmC₄NADP-ME[J]. Acta Agriculturae Boreali-Sinica, 2025, 40(2): 10-17. doi: 10.7668/hbnxb.20195463.

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Figures/Tables 5

Fig.1 Analysis of ZmC₄NADP-ME and its homologous genes in maize A.The distribution and collinearity of ZmC₄NADP-ME and its homologous genes on maize chromosome; B.Maize ZmC₄NADP-ME and its homologous gene protein sequence similarity; C.Expression level of ZmC₄NADP-ME and its homologous genes in different tissues of maize; D.Expression level of ZmC₄NADP-ME and its homologous genes in mesophyll cells and bundle sheath cells of maize.M.Mesophyll cells;BS.Bundle sheath cells.

Fig.2 Phylogenetic tree analysis of ZmC₄NADP-ME and its homologous genes

Fig.3 Phenotype identification of maize ZmC₄NADP-ME mutant A.Maize ZmC₄NADP-ME gene structure and mu insertion site,black squares represent exons and black lines represent introns,TSS represents transcription start site; B.Maize wild-type (WT) and mutant zmC₄nadp-me phenotype.

Fig.4 PSⅡ light response curves of zmC₄nadp-me and wild-type (WT) seedlings

Fig.5 PSⅠ light response curves of zmC₄nadp-me and wild-type (WT) seedlings

References 30

[1]	王金香, 张阿良, 秦敏, 曹江梅, 陈文, 郭瑞瑞. 镉胁迫对玉米幼苗光合特性及活性氧代谢的影响[J]. 天津农业科学, 2023, 29(1):1-6.doi:10.3969/j.issn.1006-6500.2023.01.001.
	Wang J X, Zhang A L, Qin M, Cao J M, Chen W, Guo R R. Effects of cadmium stress on photosynthetic characteristics and active oxygen metabolism of maize seedling[J]. Tianjin Agricultural Sciences, 2023, 29(1):1-6.
[2]	Swift J, Luginbuehl L H, Hua L, Schreier T B, Donald R M, Stanley S, Wang N, Lee T A, Nery J R, Ecker J R, Hibberd J M. Exaptation of ancestral cell-identity networks enables C4 photosynthesis[J]. Nature, 2024, 636(8041):143-150.doi:10.1038/s41586-024-08204-3.
[3]	Aubry S, Brown N J, Hibberd J M. The role of proteins in C3 plants prior to their recruitment into the C4 pathway[J]. Journal of Experimental Botany, 2011, 62(9):3049-3059.doi:10.1093/jxb/err012.
[4]	Langdale J A, Zelitch I, Miller E, Nelson T. Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize[J]. The EMBO Journal, 1988, 7(12): 3643-3651. doi:10.1002/j.1460-2075.1988.tb03245.x.
[5]	Langdale J A.C 4 cycles:past,present,and future research on C4 photosynthesis[J]. The Plant Cell, 2011, 23(11):3879-3892.doi:10.1105/tpc.111.092098. pmid: 22128120
[6]	Zhao H L, Wang Y, Lyu M A, Zhu X G. Two major metabolic factors for an efficient NADP-malic enzyme type C4 photosynthesis[J]. Plant Physiology, 2022, 189(1):84-98.doi:10.1093/plphys/kiac051.
[7]	Bellasio C, Lundgren M R. The operation of PEPCK increases light harvesting plasticity in C4 NAD ME and NADP ME photosynthetic subtypes:a theoretical study[J]. Plant,Cell & Environment, 2024, 47(6):2288-2309.doi:10.1111/pce.14869.
[8]	Badia M B, Mans R, Lis A V, Tronconi M A, Arias C L, Maurino V G, Andreo C S, Drincovich M F, van Maris A J A, Gerrard Wheeler M C. Specific Arabidopsis thaliana malic enzyme isoforms can provide anaplerotic pyruvate carboxylation function in Saccharomyces cerevisiae[J]. The FEBS Journal, 2017, 284(4):654-665.doi:10.1111/febs.14013.
[9]	Arias C L, Pavlovic T, Torcolese G, Badia M B, Gismondi M, Maurino V G, Andreo C S, Drincovich M F, Gerrard Wheeler M C, Saigo M. NADP-dependent malic enzyme 1 participates in the abscisic acid response in Arabidopsis thaliana[J]. Frontiers in Plant Science, 2018, 9:1637.doi:10.3389/fpls.2018.01637.
[10]	付振艳, 苟小清, 张正斌, 肖向文, 王晓军. 小麦TaNADP-ME2基因重组植物表达载体构建及对水稻的遗传转化[J]. 华北农学报, 2013, 28(3):58-61.doi:10.3969/j.issn.1000-7091.2013.03.011.
	Fu Z Y, Gou X Q, Zhang Z B, Xiao X W, Wang X J. The construction of plant overexpression vector of wheat TaNADP-ME2 gene and genetic transformation of rice[J]. Acta Agriculturae Boreali-Sinica, 2013, 28(3):58-61.
[11]	Badia M B, Maurino V G, Pavlovic T, Arias C L, Pagani M A, Andreo C S, Saigo M, Drincovich M F, Gerrard Wheeler M C. Loss of function of Arabidopsis NADP-malic enzyme 1 results in enhanced tolerance to aluminum stress[J]. The Plant Journal, 2020, 101(3):653-665.doi:10.1111/tpj.14571.
[12]	Brown N J, Palmer B G, Stanley S, Hajaji H, Janacek S H, Astley H M, Parsley K, Kajala K, Quick W P, Trenkamp S, Fernie A R, Maurino V G, Hibberd J M. C acid decarboxylases required for C photosynthesis are active in the mid-vein of the C species Arabidopsis thaliana,and are important in sugar and amino acid metabolism[J]. The Plant Journal, 2010, 61(1): 122-133. doi:10.1111/j.1365-313x.2009.04040.x.
[13]	Detarsio E, Maurino V G, Alvarez C E, Müller G L, Andreo C S, Drincovich M F. Maize cytosolic NADP-malic enzyme (ZmCytNADP-ME):a phylogenetically distant isoform specifically expressed in embryo and emerging roots[J]. Plant Molecular Biology, 2008, 68(4):355-367.doi:10.1007/s11103-008-9375-8.
[14]	Voll L M, Zell M B, Engelsdorf T, Saur A, Wheeler M G, Drincovich M F, Weber A P M, Maurino V G. Loss of cytosolic NADP-malic enzyme 2 in Arabidopsis thaliana is associated with enhanced susceptibility to Colletotrichum higginsianum[J]. New Phytologist, 2012, 195(1): 189-202. doi:10.1111/j.1469-8137.2012.04129.x.
[15]	Wheeler M C G, Tronconi M A, Drincovich M F, Andreo C S, Fluügge U I, Maurino V G. A comprehensive analysis of the NADP-malic enzyme gene family of Arabidopsis[J]. Plant Physiology, 2005, 139(1):39-51.doi:10.1104/pp.105.065953.
[16]	Suzuki K, Ohmori Y, Ratel E. High root temperature blocks both linear and cyclic electron transport in the dark during chilling of the leaves of rice seedlings[J]. Plant and Cell Physiology, 2011, 52(9):1697-1707.doi:10.1093/pcp/pcr104. pmid: 21803813
[17]	牛永昆, 李军乔, 曲俊儒, 李晨芹, 王鑫慈, 田甜. 铁胁迫对蕨麻叶绿素荧光及生理特性的影响[J]. 天津农业科学, 2022, 28(2):1-6.doi:10.3969/j.issn.1006-6500.2022.02.001.
	Niu Y K, Li J Q, Qu J R, Li C Q, Wang X C, Tian T. Effects of iron stress on chlorophyll fluorescence and physiological characteristics of Potentilla anserina L.[J]. Tianjin Agricultural Sciences, 2022, 28(2):1-6.
[18]	Tikkanen M, Grebe S. Switching off photoprotection of photosystem Ⅰ a novel tool for gradual PS Ⅰ photoinhibition[J]. Physiologia Plantarum, 2018, 162(2):156-161.doi:10.1111/ppl.12618.
[19]	Maxwell K, Johnson G N. Chlorophyll fluorescence-a practical guide[J]. Journal of Experimental Botany, 2000, 51(345):659-668.doi:10.1093/jxb/51.345.659. pmid: 10938857
[20]	姜晓君, 蒋英. 不同LED光质对黄瓜叶片叶绿素荧光、光合参数及SPAD值的影响[J]. 天津农业科学, 2019, 25(9):7-9.doi:10.3969/j.issn.1006-6500.2019.09.002.
	Jiang X J, Jiang Y. Effects of different LED light quality on chlorophyll fluorescence,photosynthetic parameters and SPAD in cucumber leaves[J]. Tianjin Agricultural Sciences, 2019, 25(9):7-9.
[21]	Earl H J, Ennahli S. Estimating photosynthetic electron transport via chlorophyll fluorometry without Photosystem Ⅱ light saturation[J]. Photosynthesis Research, 2004, 82(2):177-186.doi:10.1007/s11120-004-1454-3.
[22]	Chen H F, Qin L, Tian J G, Wang X L. Identification and evolutionary analysis of the GOLDEN 2-LIKE gene family in foxtail millet[J]. Tropical Plant Biology, 2022, 15(4):301-318.doi:10.1007/s12042-022-09324-8.
[23]	Hall B G. Building phylogenetic trees from molecular data with MEGA[J]. Molecular Biology and Evolution, 2013, 30(5):1229-1235.doi:10.1093/molbev/mst012. pmid: 23486614
[24]	Wang Y P, Tang H B, DeBarry J D, Tan X, Li J P, Wang X Y, Lee T H, Jin H Z, Marler B, Guo H, Kissinger J C, Paterson A H. MCScanX:a toolkit for detection and evolutionary analysis of gene synteny and collinearity[J]. Nucleic Acids Research, 2012, 40(7):e49.doi:10.1093/nar/gkr1293.
[25]	Dong P F, Tu X Y, Chu P Y, Lyu P T, Zhu N, Grierson D, Du B J, Li P H, Zhong S L. 3D chromatin architecture of large plant genomes determined by local A/B compartments[J]. Molecular Plant, 2017, 10(12):1497-1509.doi:10.1016/j.molp.2017.11.005. pmid: 29175436
[26]	Seader V H, Thornsberry J M, Carey R E. Utility of the Amborella trichopoda expansin superfamily in elucidating the history of angiosperm expansins[J]. Journal of Plant Research, 2016, 129(2):199-207.doi:10.1007/s10265-015-0772-1.
[27]	Project A G, Albert V A, Barbazuk W B, de Pamphilis C W, Der J P, Leebens-Mack J, et al. The Amborella genome and the evolution of flowering plants[J]. Science, 2013, 342(6165):1241089.doi:10.1126/science.1241089.
[28]	Zhang Y L, Giuliani R, Zhang Y J, Zhang Y, Araujo W L, Wang B C, Liu P, Sun Q, Cousins A, Edwards G, Fernie A, Brutnell T P, Li P H. Characterization of maize leaf pyruvate orthophosphate dikinase using high throughput sequencing[J]. Journal of Integrative Plant Biology, 2018, 60(8):670-690.doi:10.1111/jipb.12656.
[29]	Studer A J, Gandin A, Kolbe A R, Wang L, Cousins A B, Brutnell T P. A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize[J]. Plant Physiology, 2014, 165(2):608-617.doi:10.1104/pp.114.237602. pmid: 24706552
[30]	Kalaji H M, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska I A, Cetner M D, Łukasik I, Goltsev V, Ladle R J, Dᶏbrowski P, Ahmad P. The use of chlorophyll fluorescence kinetics analysis to study the performance of photosynthetic machinery in plants[M]. Amsteradam:Elsevier, Emerging Technologies and Management of Crop Stress Tolerance, 2014, 2:347-384.doi:10.1016/B978-0-12-800875-1.00015-6.

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