Molecular Mechanisms of Male Sterility and their Applications in Biotechnology-based Male-sterility Hybrid Seed Production in Maize

doi:10.11983/CBB24078

Abstract

Abstract: Maize (Zea mays) is the major grain crop with the largest planting area and the highest total yield in China, and it is also a model of heterosis utilization. However, compared with developed countries, China is still facing several outstanding problems in maize production, such as low average yield, lack of breakthrough varieties and high cost of hybrid seed production. The main solution to these problems is the application of male-sterile lines with better heterosis utilization efficiency and thus increase the yield per unit area of maize. In this review, we summarize the latest advances of male sterility research in maize, including its classification, gene cloning and functional analysis, molecular regulatory network construction, and discuss the strategies of creating novel male-sterility systems and their potential/future application in maize breeding. This review provides guidelines for the male-sterility based/assisted hybrid breeding and seed production in maize.

Key words: maize, male sterility, gene cloning and mechanism analysis, biotechnology-based male-sterility technology, heterosis

Suowei Wu, Xueli An, Xiangyuan Wan. Molecular Mechanisms of Male Sterility and their Applications in Biotechnology-based Male-sterility Hybrid Seed Production in Maize[J]. Chinese Bulletin of Botany, 2024, 59(6): 932-949.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB24078

https://www.chinbullbotany.com/EN/Y2024/V59/I6/932

Figures/Tables 4

References 79

[1]	Albertsen M, Fox T, Leonard A, Li B, Loveland B, Trimnell M (2016). Cloning and use of the ms9 gene from maize. US patent, US 20160024520A1. 2016-01-28.
[2]	An XL, Dong ZY, Tian YH, Xie K, Wu SW, Zhu TT, Zhang DF, Zhou Y, Niu CF, Ma B, Hou QC, Bao JX, Zhang SM, Li ZW, Wang YB, Yan TW, Sun XJ, Zhang YW, Li JP, Wan XY (2019). ZmMs30 encoding a novel GDSL lipase is essential for male fertility and valuable for hybrid breeding in maize. Mol Plant 12, 343-359.
[3]	An XL, Ma B, Duan MJ, Dong ZY, Liu RG, Yuan DY, Hou QC, Wu SW, Zhang DF, Liu DC, Yu D, Zhang YW, Xie K, Zhu TT, Li ZW, Zhang SM, Tian YH, Liu C, Li JP, Yuan LP, Wan XY (2020). Molecular regulation of ZmMs7 required for maize male fertility and development of a dominant male-sterility system in multiple species. Proc Natl Acad Sci USA 117, 23499-23509.
[4]	An XL, Zhang SW, Jiang YL, Liu XZ, Fang CW, Wang J, Zhao LN, Hou QC, Zhang J, Wan XY (2024). CRISPR/ Cas9-based genome editing of 14 lipid metabolic genes reveals a sporopollenin metabolon ZmPKSB-ZmTKPR1- 1/-2 required for pollen exine formation in maize. Plant Biotechnol J 22, 216-232.
[5]	Beckett JB (1971). Classification of male-sterile cytoplasms in maize (Zea mays L.). Crop Sci 11, 724-727.
[6]	Cai CF, Zhu J, Lou Y, Guo ZL, Xiong SX, Wang K, Yang ZN (2015). The functional analysis of OsTDF1 reveals a conserved genetic pathway for tapetal development between rice and Arabidopsis. Sci Bull 60, 1073-1082.
[7]	Chaubal R, Anderson JR, Trimnell MR, Fox TW, Albertsen MC, Bedinger P (2003). The transformation of anthers in the msca1 mutant of maize. Planta 216, 778-788. PMID
[8]	Chen XY, Zhang H, Sun HY, Luo HB, Zhao L, Dong ZB, Yan SS, Zhao C, Liu RY, Xu CY, Li S, Chen HB, Jin WW (2017). IRREGULAR POLLEN EXINE1 is a novel factor in anther cuticle and pollen exine formation. Plant Physiol 173, 307-325. DOI PMID
[9]	Cheng JH, Li YC, Mei DS, Hu Q (2006). Molecular mapping and markers for fertility restorer genes of cytoplasmic male sterility in major crops. Chin Bull Bot 23, 613-624. (in Chinese)
	程计华, 李云昌, 梅德圣, 胡琼 (2006). 几种农作物细胞质雄性不育恢复基因的定位和分子标记研究进展. 植物学报 23, 613-624.
[10]	Cigan AM, Unger E, Xu RJ, Kendall T, Fox TW (2001). Phenotypic complementation of ms45 maize requires tapetal expression of MS45. Sex Plant Reprod 14, 135-142.
[11]	Collinson S, Hamdziripi E, De Groote H, Ndegwa M, Cairns JE, Albertsen M, Ligeyo D, Mashingaidze K, Olsen MS (2022). Incorporating male sterility increases hybrid maize yield in low input African farming systems. Commun Biol 5, 729. DOI PMID
[12]	Cui X, Wise RP, Schnable PS (1996). The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272, 1334-1336. DOI PMID
[13]	Dill CL, Wise RP, Schnable PS (1997). Rf8 and Rf* mediate unique T-urf13-transcript accumulation, revealing a conserved motif associated with RNA processing and restoration of pollen fertility in T-cytoplasm maize. Genetics 147, 1367-1379. DOI PMID
[14]	Djukanovic V, Smith J, Lowe K, Yang MZ, Gao HR, Jones S, Nicholson MG, West A, Lape J, Bidney D, Carl Falco S, Jantz D, Alexander Lyznik L (2013). Male- sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. Plant J 76, 888-899.
[15]	Evans MMS (2007). The indeterminate gamethophyte1gene of maize encodes a LOB domain protein required for embryo sac and leaf development. Plant Cell 19, 46-62.
[16]	Fan MX, Zhang CY, Shi L, Liu C, Ma WJ, Chen MM, Liu KC, Cai FC, Wang GH, Wei ZY, Jiang M, Liu ZC, Javeed A, Lin F (2018). ZmSTK1 and ZmSTK2, encoding receptor-like cytoplasmic kinase, are involved in maize pollen development with additive effect. Plant Biotechnol J 16, 1402-1414.
[17]	Fang CW, Wu SW, Li ZW, Pan SS, Wu YR, An XL, Long Y, Wei X, Wan XY (2023a). A systematic investigation of lipid transfer proteins involved in male fertility and other biological processes in maize. Int J Mol Sci 24, 1660.
[18]	Fang CW, Wu SW, Niu CF, Hou QC, An XL, Wei X, Zhao LN, Jiang YL, Liu XZ, Wan XY (2023b). Triphasic regulation of ZmMs13 encoding an ABCG transporter is sequentially required for callose dissolution, pollen exine and anther cuticle formation in maize. J Adv Res 49, 15-30.
[19]	Feng PCC, Qi YL, Chiu T, Stoecker MA, Schuster CL, Johnson SC, Fonseca AE, Huang JT (2014). Improving hybrid seed production in corn with glyphosate-mediated male sterility. Pest Manag Sci 70, 212-218. DOI PMID
[20]	Fox T, DeBruin J, Haug Collet K, Trimnell M, Clapp J, Leonard A, Li BL, Scolaro E, Collinson S, Glassman K, Miller M, Schussler J, Dolan D, Liu L, Gho C, Albertsen M, Loussaert D, Shen B (2017). A single point mutation in Ms44 results in dominant male sterility and improves nitrogen use efficiency in maize. Plant Biotechnol J 15, 942-952.
[21]	Fu ZY, Qin YT, Tang JH (2018). Reviews of photo-or/and thermo-sensitive genic male sterile gene in major crops. China Biotechnol 38, 115-125. (in Chinese)
	付志远, 秦永田, 汤继华 (2018). 主要作物光温敏核雄性不育基因的研究进展与应用. 中国生物工程杂志 38, 115-125.
[22]	Gabay-Laughnan S, Kuzmin EV, Monroe J, Roark L, Newton KJ (2009). Characterization of a novel thermosensitive restorer of fertility for cytoplasmic male sterility in maize. Genetics 182, 91-103. DOI PMID
[23]	Han YJ, Hu MJ, Ma XX, Yan G, Wang CY, Jiang SQ, Lai JS, Zhang M (2022). Exploring key developmental phases and phase-specific genes across the entirety of anther development in maize. J Integr Plant Biol 64, 1394-1410. DOI
[24]	Hou QC, An XL, Ma B, Wu SW, Wei X, Yan TW, Zhou Y, Zhu TT, Xie K, Zhang DF, Li ZW, Zhao LN, Niu CF, Long Y, Liu C, Zhao W, Ni F, Li JP, Fu DL, Yang ZN, Wan XY (2023). ZmMS1/ZmLBD30-orchestrated transcriptional regulatory networks precisely control pollen exine development. Mol Plant 16, 1321-1338.
[25]	Hu MJ, Li YF, Zhang XB, Song WB, Jin WW, Huang W, Zhao HM (2022). Maize sterility gene DRP1encodes a desiccation-related protein that is critical for Ubisch bodies and pollen exine development. J Exp Bot 73, 6800-6815.
[26]	Hu YM, Tang JH, Yang H, Xie HL, Lu XM, Niu JH, Chen WC (2006). Identification and mapping of Rf-I an inhibitor of the Rf5restorer gene for CMS-C in maize (Zea mays L.). Theor Appl Genet 113, 357-360. DOI PMID
[27]	Huang W, Li YF, Du Y, Pan LL, Huang YM, Liu HB, Zhao Y, Shi YL, Ruan YL, Dong ZB, Jin WW (2022). Maize cytosolic invertase INVAN6 ensures faithful meiotic progression under heat stress. New Phytol 236, 2172-2188. DOI PMID
[28]	Huo YQ, Pei YR, Tian YH, Zhang ZG, Li K, Liu J, Xiao SL, Chen HB, Liu J (2020). IRREGULAR POLLEN EXINE2 encodes a GDSL lipase essential for male fertility in maize. Plant Physiol 184, 1438-1454.
[29]	Jaqueth JS, Hou ZL, Zheng PZ, Ren RH, Nagel BA, Cutter G, Niu XM, Vollbrecht E, Greene TW, Kumpatla SP (2020). Fertility restoration of maize CMS-C altered by a single amino acid substitution within the Rf4 bHLH transcription factor. Plant J 101, 101-111.
[30]	Jiang YL, An XL, Li ZW, Yan TW, Zhu TT, Xie K, Liu SS, Hou QC, Zhao LN, Wu SW, Liu XZ, Zhang SW, He W, Li F, Li JP, Wan XY (2021). CRISPR/Cas9-based discovery of maize transcription factors regulating male sterility and their functional conservation in plants. Plant Biotechnol J 19, 1769-1784. DOI PMID
[31]	Kelliher T, Walbot V (2012). Hypoxia triggers meiotic fate acquisition in maize. Science 337, 345-348. DOI PMID
[32]	Levings III CS (1990). The Texas cytoplasm of maize: cytoplasmic male sterility and disease susceptibility. Science 250, 942-947. DOI PMID
[33]	Li J, Zhang HW, Si XM, Tian YH, Chen KL, Liu JX, Chen HB, Gao CX (2017). Generation of thermosensitive male-sterile maize by targeted knockout of the ZmTMS5gene. J Genet Genomics 44, 465-468.
[34]	Li YF, Huang YM, Pan LL, Zhao Y, Huang W, Jin WW (2021). Male sterile 28 encodes an ARGONAUTE family protein essential for male fertility in maize. Chromosome Res 29, 189-201.
[35]	Li YF, Huang YM, Sun HY, Wang TY, Ru W, Pan LL, Zhao XM, Dong ZB, Huang W, Jin WW (2022). Heat shock protein 101 contributes to the thermotolerance of male meiosis in maize. Plant Cell 34, 3702-3717.
[36]	Lin YA, Yang HL, Liu HM, Lu XY, Cao HF, Li B, Chang YY, Guo ZY, Ding D, Hu YM, Xue YD, Liu ZH, Tang JH (2024). A P-type pentatricopeptide repeat protein ZmRF5 promotes 5′ region partial cleavages of atp6c transcripts to restore the fertility of CMS-C maize by recruiting a splicing factor. Plant Biotechnol J 22, 1269-1281.
[37]	Liu CX, Wang GQ, Gao J, Li CY, Zhang ZR, Yu TT, Wang JG, Zhou L, Cai YL (2018). Characterization, fine mapping and candidate gene analysis of novel, dominant, nuclear male-sterile gene Ms53 in maize. Euphytica 214, 52.
[38]	Liu SS, Wu SW, Rao LQ, Wan XY (2018). Molecular mechanism and application analysis of genic male sterility in maize. China Biotechnol 38, 100-107. (in Chinese)
	柳双双, 吴锁伟, 饶力群, 万向元 (2018). 玉米核雄性不育的分子机制研究与应用分析. 中国生物工程杂志 38, 100-107.
[39]	Liu XZ, Jiang YL, Wu SW, Wang J, Fang CW, Zhang SW, Xie RR, Zhao LN, An XL, Wan XY (2022a). The ZmMYB84-ZmPKSB regulatory module controls male fertility through modulating anther cuticle-pollen exine trade- off in maize anthers. Plant Biotechnol J 20, 2342-2356.
[40]	Liu XZ, Zhang SW, Jiang YL, Yan TW, Fang CW, Hou QC, Wu SW, Xie K, An XL, Wan XY (2022b). Use of CRISPR/Cas9-based gene editing to simultaneously mutate multiple homologous genes required for pollen development and male fertility in maize. Cells 11, 439.
[41]	Lou Y, Zhou HS, Han Y, Zeng QY, Zhu J, Yang ZN (2018). Positive regulation of AMS by TDF1 and the formation of a TDF1-AMS complex are required for anther development in Arabidopsis thaliana. New Phytol 217, 378-391.
[42]	Lu XD, Liu JS, Ren W, Yang Q, Chai ZG, Chen RM, Wang L, Zhao J, Lang ZH, Wang HY, Fan YL, Zhao JR, Zhang CY (2018). Gene-indexed mutations in maize. Mol Plant 11, 496-504. DOI PMID
[43]	Marchant DB, Walbot V (2022). Anther development—the long road to making pollen. Plant Cell 34, 4677-4695.
[44]	Moon J, Skibbe D, Timofejeva L, Wang CJR, Kelliher T, Kremling K, Walbot V, Cande WZ (2013). Regulation of cell divisions and differentiation by MALE STERILITY32 is required for anther development in maize. Plant J 76, 592-602.
[45]	Nan GL, Teng C, Fernandes J, O'Connor L, Meyers BC, Walbot V (2022). A cascade of bHLH-regulated pathways programs maize anther development. Plant Cell 34, 1207-1225.
[46]	Nan GL, Zhai JX, Arikit S, Morrow D, Fernandes J, Mai L, Nguyen N, Meyers BC, Walbot V (2017). MS23, a master basic helix-loop-helix factor, regulates the specification and development of tapetum in maize. Development 144, 163-172.
[47]	Qi XL, Guo SW, Wang D, Zhong Y, Chen M, Chen C, Cheng DH, Liu ZK, An T, Li JL, Jiao YY, Wang YW, Liu JC, Zhang YL, Chen SJ, Liu CX (2022). ZmCOI2a and ZmCOI2b redundantly regulate anther dehiscence and gametophytic male fertility in maize. Plant J 110, 849-862.
[48]	Qi XT, Zhang CS, Zhu JJ, Liu CL, Huang CL, Li XH, Xie CX (2020). Genome editing enables next-generation hybrid seed production technology. Mol Plant 13, 1262-1269. DOI PMID
[49]	Qin XE, Tian SK, Zhang WL, Zheng Q, Wang H, Feng Y, Lin YN, Tang JH, Wang Y, Yan JB, Dai MQ, Zheng YL, Yue B (2021). The main restorer Rf3 of maize S type cytoplasmic male sterility encodes a PPR protein that functions in reduction of the transcripts of orf355. Mol Plant 14, 1961-1964.
[50]	Shi Z, Ren W, Zhao YX, Wang XQ, Zhang RY, Su AG, Wang S, Li CH, Wang JR, Wang SS, Zhang YX, Ji YL, Song W, Zhao JR (2020). Identification of a locus associated with genic male sterility in maize via EMS mutagenesis and bulked-segregant RNA-seq. Crop J 9, 1263-1269.
[51]	Somaratne Y, Tian YH, Zhang H, Wang MM, Huo YQ, Cao FG, Zhao L, Chen HB (2017). ABNORMAL POLLEN VACUOLATION1 (APV1) is required for male fertility by contributing to anther cuticle and pollen exine formation in maize. Plant J 90, 96-110.
[52]	Su AG, Song W, Wang SS, Zhao JR (2018). Advance on cytoplasmic male sterility and fertility restoration genes in maize. China Biotechnol 38, 108-114. (in Chinese)
	苏爱国, 宋伟, 王帅帅, 赵久然 (2018). 玉米细胞质雄性不育及其育性恢复基因的研究进展. 中国生物工程杂志 38, 108-114.
[53]	Sun QQ, Rong TZ (2003). Study on genic male sterility in maize and use in molecular breeding. Chin Bull Bot 20, 248-253. (in Chinese)
	孙庆泉, 荣廷昭 (2003). 玉米核雄性不育材料的研究及其在分子育种中的利用. 植物学通报 20, 248-253.
[54]	Teng C, Zhang H, Hammond R, Huang K, Meyers BC, Walbot V (2020). Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize. Nat Commun 11, 2912.
[55]	Tian YH, Xiao SL, Liu J, Somaratne Y, Zhang H, Wang MM, Zhang HR, Zhao L, Chen HB (2017). MALE STERILE6021 (MS6021) is required for the development of anther cuticle and pollen exine in maize. Sci Rep 7, 16736.
[56]	Van Der Linde K, Timofejeva L, Egger RL, Ilau B, Hammond R, Teng C, Meyers BC, Doehlemann G, Walbot V (2018). Pathogen Trojan horse delivers bioactive host protein to alter maize anther cell behavior in situ. Plant Cell 30, 528-542.
[57]	Vernoud V, Laigle G, Rozier F, Meeley RB, Perez P, Rogowsky PM (2009). The HD-ZIP IV transcription factor OCL4 is necessary for trichome patterning and anther development in maize. Plant J 59, 883-894.
[58]	Wan XY, Wu SW, Li X (2021). Breeding with dominant genic male-sterility genes to boost crop grain yield in the post-heterosis utilization era. Mol Plant 14, 531-534. DOI PMID
[59]	Wan XY, Wu SW, Li ZW, An XL, Tian YH (2020). Lipid metabolism: critical roles in male fertility and other aspects of reproductive development in plants. Mol Plant 13, 955-983. DOI PMID
[60]	Wan XY, Wu SW, Li ZW, Dong ZY, An XL, Ma B, Tian YH, Li JP (2019). Maize genic male-sterility genes and their applications in hybrid breeding: progress and perspectives. Mol Plant 12, 321-342. DOI PMID
[61]	Wang CJR, Nan GL, Kelliher T, Timofejeva L, Vernoud V, Golubovskaya IN, Harper L, Egger R, Walbot V, Cande WZ (2012). Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 139, 2594-2603.
[62]	Wang DX, Skibbe DS, Walbot V (2013). Maize Male sterile 8 (Ms8), a putative β-1,3-galactosyltransferase, modulates cell division, expansion, and differentiation during early maize anther development. Plant Reprod 26, 329-338.
[63]	Wang YB, Liu DC, Tian YH, Wu SW, An XL, Dong ZY, Zhang SM, Bao JX, Li ZW, Li JP, Wan XY (2019). Map- based cloning, phylogenetic, and microsynteny analyses of ZmMs20 gene regulating male fertility in maize. Int J Mol Sci 20, 1411.
[64]	Wu H, Xu H, Liu ZL, Liu YG (2007). Molecular basis of plant cytoplasmic male sterility and fertility restoration. Chin Bull Bot 24, 399-413. (in Chinese)
	吴豪, 徐虹, 刘振兰, 刘耀光 (2007). 植物细胞质雄性不育及其育性恢复的分子基础. 植物学通报 24, 399-413.
[65]	Wu SW, Wan XY (2018). Construction of male-sterility system using biotechnology and application in crop breeding and hybrid seed production. China Biotechnol 38, 78-87. (in Chinese)
	吴锁伟, 万向元 (2018). 利用生物技术创建主要作物雄性不育杂交育种和制种的技术体系. 中国生物工程杂志 38, 78-87.
[66]	Wu YZ, Fox TW, Trimnell MR, Wang LJ, Xu RJ, Cigan AM, Huffman GA, Garnaat CW, Hershey H, Albertsen MC (2016). Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops. Plant Biotechnol J 14, 1046-1054. DOI PMID
[67]	Xiao SL, Zang J, Pei YR, Liu J, Liu J, Song W, Shi Z, Su AG, Zhao JR, Chen HB (2020). Activation of mitochondrial orf355 gene expression by a nuclear-encoded DREB transcription factor causes cytoplasmic male sterility in maize. Mol Plant 13, 1270-1283.
[68]	Xie K, Wu SW, Li ZW, Zhou Y, Zhang DF, Dong ZY, An XL, Zhu TT, Zhang SM, Liu SS, Li JP, Wan XY (2018). Map-based cloning and characterization of Zea mays male sterility33 (ZmMs33) gene, encoding a glycerol-3- phosphate acyltransferase. Theor Appl Genet 131, 1363-1378. DOI PMID
[69]	Xu QL, Yang L, Kang D, Ren ZJ, Liu YJ (2021). Maize MS2 encodes an ATP-binding cassette transporter that is essential for anther development. Crop J 9, 1301-1308.
[70]	Yang HL, Xue YD, Li B, Lin YN, Li HC, Guo ZY, Li WH, Fu ZY, Ding D, Tang JH (2022). The chimeric gene atp6c confers cytoplasmic male sterility in maize by impairing the assembly of the mitochondrial ATP synthase complex. Mol Plant 15, 872-886.
[71]	Yang HP, Qi YL, Goley ME, Huang JT, Ivashuta S, Zhang YJ, Sparks OC, Ma JY, Van Scoyoc BM, Caruano-Yze- rmans AL, King-Sitzes J, Li X, Pan AH, Stoecker MA, Wiggins BE, Varagona MJ (2018). Endogenous tassel-specific small RNAs-mediated RNA interference enables a novel glyphosate-inducible male sterility system for commercial production of hybrid seed in Zea mays L. PLoS One 13, e0202921.
[72]	Zhang DF, Wu SW, An XL, Xie K, Dong ZY, Zhou Y, Xu LW, Fang W, Liu SS, Liu SS, Zhu TT, Li JP, Rao LQ, Zhao JR, Wan XY (2018a). Construction of a multicontrol sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-finger transcription factor. Plant Biotechnol J 16, 459-471.
[73]	Zhang L, Luo HB, Zhao Y, Chen XY, Huang YM, Yan SS, Li SX, Liu MS, Huang W, Zhang XL, Jin WW (2018b). Maize male sterile 33 encodes a putative glycerol-3-phosphate acyltransferase that mediates anther cuticle formation and microspore development. BMC Plant Biol 18, 318.
[74]	Zhang SM, Wu SW, Niu CF, Liu DC, Yan TW, Tian YH, Liu SS, Xie K, Li ZW, Wang YB, Zhao W, Dong ZY, Zhu TT, Hou QC, Ma B, An XL, Li JP, Wan XY (2021). ZmMs25encoding a plastid-localized fatty acyl reductase is critical for anther and pollen development in maize. J Exp Bot 72, 4298-4318.
[75]	Zheng MM, Huang Q, Zhang P, Liu XW, Zhao ZF, Yi HY, Rong TZ, Cao MJ (2024). Research progress on cytoplasmic male sterility and fertility restoration in maize. Chin Bull Bot 59, 999-1006. (in Chinese)
	郑名敏, 黄强, 张鹏, 刘孝伟, 赵卓凡, 易洪杨, 荣廷昭, 曹墨菊 (2024). 玉米细胞质雄性不育及育性恢复研究进展. 植物学报 59, 999-1006. DOI
[76]	Zheng YL (1982). Study on the mechanism of the fertility about several types of cytoplasmic male-sterility in maize (Zea mays L.). J Huazhong Agri Coll (1), 44-68. (in Chinese)
	郑用琏 (1982). 若干玉米细胞质雄性不育类型(CMS)育性机理的研究. 华中农学院学报 (1), 44-68.
[77]	Zhu TT, Li ZW, An XL, Long Y, Xue XF, Xie K, Ma B, Zhang DF, Guan YJ, Niu CF, Dong ZY, Hou QC, Zhao LN, Wu SW, Li JP, Jin WW, Wan XY (2020). Normal structure and function of endothecium chloroplasts maintained by ZmMs33-mediated lipid biosynthesis in Tapetal cells are critical for anther development in maize. Mol Plant 13, 1624-1643. DOI PMID
[78]	Zhu TT, Wu SW, Zhang DF, Li ZW, Xie K, An XL, Ma B, Hou QC, Dong ZY, Tian YH, Li JP, Wan XY (2019). Genome-wide analysis of maize GPAT gene family and cytological characterization and breeding application of ZmMs33/ZmGPAT6 gene. Theor Appl Genet 132, 2137-2154.
[79]	Zhu YH, Shi ZW, Li SZ, Liu HY, Liu FX, Niu QK, Li C, Wang J, Rong TZ, Yi HY, Cao MJ (2018). Fine mapping of the novel male-sterile mutant gene ms39in maize originated from outer space flight. Mol Breed 38, 125.

序号	不育基因	基因ID	编码蛋白	参考文献
I 转录因子类
1	ZmMs1/ZmLBD30	Zm00001d036435	LBD转录因子	Hou et al., 2023
2	ZmIG1	Zm00001d042560	LBD转录因子	Evans, 2007
3	ZmLBD10	Zm00001d033335	LBD转录因子	Jiang et al., 2021
4	ZmLBD27	Zm00001d013732	LBD转录因子	Jiang et al., 2021
5	ZmMs7	Zm00001d020680	PHD-finger转录因子	Zhang et al., 2018a
6	ZmPHD11	Zm00001d013416	PHD-finger转录因子	Jiang et al., 2021
7	ZmMs9	Zm00001d028777	MYB转录因子	Albertsen et al., 2016
8	ZmMYB33-1	Zm00001d012544	MYB转录因子	Jiang et al., 2021
9	ZmMYB33-2	Zm00001d043131	MYB转录因子	Jiang et al., 2021
10	ZmMYB84	Zm00001d025664	MYB转录因子	Jiang et al., 2021
11	ZmMs23	Zm00001d008174	bHLH转录因子	Nan et al., 2017
12	ZmMs32	Zm00001d006564	bHLH转录因子	Moon et al., 2013
13	ZmbHLH51	Zm00001d053895	bHLH转录因子	Jiang et al., 2021
14	ZmbHLH122	Zm00001d017724	bHLH转录因子	Jiang et al., 2021
15	ZmOCL4	Zm00001d030069	HD-ZIP转录因子	Vernoud et al., 2009
16	ZmTGA9-1	Zm00001d052543	bZIP转录因子	Jiang et al., 2021
17	ZmTGA9-2	Zm00001d042777	bZIP转录因子	Jiang et al., 2021
18	ZmTGA9-3	Zm00001d012294	bZIP转录因子	Jiang et al., 2021
19	ZmTGA10	Zm00001d020938	bZIP转录因子	Jiang et al., 2021
20	ZmMs53	Zm00001d053890	SBP转录因子	Liu et al., 2018
II 脂代谢类
21	ZmMs26	Zm00001d027837	细胞色素P450单加氧酶, CYP704B1	Djukanovic et al., 2013
22	ZmMs10/APV1	Zm00001d024712	细胞色素P450单加氧酶, CYP703A2	Somaratne et al., 2017
23	ZmMs30	Zm00001d052403	GDSL酯酶/脂肪酶	An et al., 2019
24	ZmMs5/IPE2	Zm00001d015960	GDSL酯酶/脂肪酶	Huo et al., 2020
25	ZmMs33/GPAT6	Zm00001d007714	甘油-3-磷酸酰基转移酶	Xie et al., 2018; Zhang et al., 2018b; Zhu et al., 2020
26	ZmMs45	Zm00001d047859	异胡豆苷合成酶	Cigan et al., 2001
27	ZmMs20/IPE1*	Zm00001d029683	GMC氧化还原酶	Chen et al., 2017; Wang et al., 2019
28	ZmMs25/ZmMs6021	Zm00001d048337	脂肪酰还原酶	Tian et al., 2017; Zhang et al., 2021
29	ZmMs44	Zm00001d052736	非特异性脂质转移蛋白	Fox et al., 2017
30	ZmABCG26	Zm00001d046537	ABCG转运蛋白	Jiang et al., 2021
31	ZmMs13	Zm00001d013960	ABCG转运蛋白	Fang et al., 2023b
32	ZmPKSB	Zm00001d019478	聚酮合酶B	Liu et al., 2022a
33	ZmTKPR1-1	Zm00001d031488	四肽α-吡咯酮还原酶	An et al., 2024
34	ZmTKPR1-2	Zm00001d020970	四肽α-吡咯酮还原酶	An et al., 2024
III 糖代谢类
35	ZmMs8	Zm00001d012234	β-1,3-半乳糖基转移酶	Wang et al., 2013
36	ZmMs39	Zm00001d043909	胼胝质合成酶	Zhu et al., 2018
37	ZmSTK1	Zm00001d045056	丝氨酸苏氨酸激酶1	Fan et al., 2018
38	ZmSTK2	Zm00001d052067	丝氨酸苏氨酸激酶2	Fan et al., 2018
39	ZmINVAN6/Mei025	Zm00001d015094	胞质转化酶	Huang et al., 2022
IV 其它途径类
40	ZmMs22/MSCA1	Zm00001d018802	谷氧还蛋白	Kelliher and Walbot, 2012
41	ZmMAC1	Zm00001d023681	小分泌蛋白配体	Wang et al., 2012
42	ZmMSP1	Zm00001d042362	富亮氨酸重复受体激酶	van der Linde et al., 2018
43	ZmDRP1	Zm00001d035791	干燥相关蛋白	Hu et al., 2022
44	ZmCOI2a	Zm00001d042833	茉莉酸受体	Qi et al., 2022
45	ZmCOI2b	Zm00001d010082	茉莉酸受体	Qi et al., 2022
46	ZmMs28/AGO5c	Zm00001d013063	ARGONAUTE蛋白	Li et al., 2021
47	ZmMs42/HSP101	Zm00001d038806	热激蛋白	Li et al., 2022
48	ZmTMS5	Zm00001d053351	RNA酶ZS1	Li et al., 2017
49	ZmDCL5	Zm00001d032655	Dicer类似蛋白	Teng et al., 2020

序号	不育基因	基因ID	编码蛋白	参考文献
I 转录因子类
1	ZmMs1/ZmLBD30	Zm00001d036435	LBD转录因子	Hou et al., 2023
2	ZmIG1	Zm00001d042560	LBD转录因子	Evans, 2007
3	ZmLBD10	Zm00001d033335	LBD转录因子	Jiang et al., 2021
4	ZmLBD27	Zm00001d013732	LBD转录因子	Jiang et al., 2021
5	ZmMs7	Zm00001d020680	PHD-finger转录因子	Zhang et al., 2018a
6	ZmPHD11	Zm00001d013416	PHD-finger转录因子	Jiang et al., 2021
7	ZmMs9	Zm00001d028777	MYB转录因子	Albertsen et al., 2016
8	ZmMYB33-1	Zm00001d012544	MYB转录因子	Jiang et al., 2021
9	ZmMYB33-2	Zm00001d043131	MYB转录因子	Jiang et al., 2021
10	ZmMYB84	Zm00001d025664	MYB转录因子	Jiang et al., 2021
11	ZmMs23	Zm00001d008174	bHLH转录因子	Nan et al., 2017
12	ZmMs32	Zm00001d006564	bHLH转录因子	Moon et al., 2013
13	ZmbHLH51	Zm00001d053895	bHLH转录因子	Jiang et al., 2021
14	ZmbHLH122	Zm00001d017724	bHLH转录因子	Jiang et al., 2021
15	ZmOCL4	Zm00001d030069	HD-ZIP转录因子	Vernoud et al., 2009
16	ZmTGA9-1	Zm00001d052543	bZIP转录因子	Jiang et al., 2021
17	ZmTGA9-2	Zm00001d042777	bZIP转录因子	Jiang et al., 2021
18	ZmTGA9-3	Zm00001d012294	bZIP转录因子	Jiang et al., 2021
19	ZmTGA10	Zm00001d020938	bZIP转录因子	Jiang et al., 2021
20	ZmMs53	Zm00001d053890	SBP转录因子	Liu et al., 2018
II 脂代谢类
21	ZmMs26	Zm00001d027837	细胞色素P450单加氧酶, CYP704B1	Djukanovic et al., 2013
22	ZmMs10/APV1	Zm00001d024712	细胞色素P450单加氧酶, CYP703A2	Somaratne et al., 2017
23	ZmMs30	Zm00001d052403	GDSL酯酶/脂肪酶	An et al., 2019
24	ZmMs5/IPE2	Zm00001d015960	GDSL酯酶/脂肪酶	Huo et al., 2020
25	ZmMs33/GPAT6	Zm00001d007714	甘油-3-磷酸酰基转移酶	Xie et al., 2018; Zhang et al., 2018b; Zhu et al., 2020
26	ZmMs45	Zm00001d047859	异胡豆苷合成酶	Cigan et al., 2001
27	ZmMs20/IPE1*	Zm00001d029683	GMC氧化还原酶	Chen et al., 2017; Wang et al., 2019
28	ZmMs25/ZmMs6021	Zm00001d048337	脂肪酰还原酶	Tian et al., 2017; Zhang et al., 2021
29	ZmMs44	Zm00001d052736	非特异性脂质转移蛋白	Fox et al., 2017
30	ZmABCG26	Zm00001d046537	ABCG转运蛋白	Jiang et al., 2021
31	ZmMs13	Zm00001d013960	ABCG转运蛋白	Fang et al., 2023b
32	ZmPKSB	Zm00001d019478	聚酮合酶B	Liu et al., 2022a
33	ZmTKPR1-1	Zm00001d031488	四肽α-吡咯酮还原酶	An et al., 2024
34	ZmTKPR1-2	Zm00001d020970	四肽α-吡咯酮还原酶	An et al., 2024
III 糖代谢类
35	ZmMs8	Zm00001d012234	β-1,3-半乳糖基转移酶	Wang et al., 2013
36	ZmMs39	Zm00001d043909	胼胝质合成酶	Zhu et al., 2018
37	ZmSTK1	Zm00001d045056	丝氨酸苏氨酸激酶1	Fan et al., 2018
38	ZmSTK2	Zm00001d052067	丝氨酸苏氨酸激酶2	Fan et al., 2018
39	ZmINVAN6/Mei025	Zm00001d015094	胞质转化酶	Huang et al., 2022
IV 其它途径类
40	ZmMs22/MSCA1	Zm00001d018802	谷氧还蛋白	Kelliher and Walbot, 2012
41	ZmMAC1	Zm00001d023681	小分泌蛋白配体	Wang et al., 2012
42	ZmMSP1	Zm00001d042362	富亮氨酸重复受体激酶	van der Linde et al., 2018
43	ZmDRP1	Zm00001d035791	干燥相关蛋白	Hu et al., 2022
44	ZmCOI2a	Zm00001d042833	茉莉酸受体	Qi et al., 2022
45	ZmCOI2b	Zm00001d010082	茉莉酸受体	Qi et al., 2022
46	ZmMs28/AGO5c	Zm00001d013063	ARGONAUTE蛋白	Li et al., 2021
47	ZmMs42/HSP101	Zm00001d038806	热激蛋白	Li et al., 2022
48	ZmTMS5	Zm00001d053351	RNA酶ZS1	Li et al., 2017
49	ZmDCL5	Zm00001d032655	Dicer类似蛋白	Teng et al., 2020