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Chinese Bulletin of Botany >

2024 , Vol. 59 >Issue 6: 999 - 1006

DOI: https://doi.org/10.11983/CBB24084

INVITED REVIEWS

Research Progress on Cytoplasmic Male Sterility and Fertility Restoration in Maize

  • Mingmin Zheng ,
  • Qiang Huang ,
  • Peng Zhang ,
  • Xiaowei Liu ,
  • Zhuofan Zhao ,
  • Hongyang Yi ,
  • Tingzhao Rong ,
  • Moju Cao
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  • 1Sichuan Provincial Key Laboratory for Development and Utilization of Characteristic Horticultural Biological Resources, College of Chemistry and Life Sciences, Chengdu Normal University, Chengdu 611130, China
    2Sichuan Institute of Atomic Energy, Chengdu 610101, China
    3Maize Research Institute, Sichuan Agricultural University, Chengdu 611130, China

Received date: 2024-05-31

  Accepted date: 2024-07-23

  Online published: 2024-07-29

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Abstract

Cytoplasmic male sterility (CMS) is a maternal genetic trait widely found in higher plants. CMS is not only a favorable material for studying the interaction between cytoplasmic and nuclear genomes, but also a crucial foundation for plant heterosis utilization. Maize is one of the most successful example for the utilization of heterosis in crops, and CMS has become a powerful tool for hybrid production to utilize heterosis in maize. Therefore, the molecular mechanism of CMS in maize has always been a research hotspot. In this paper, CMS related genes and fertility restorer genes discovered in the three major types of CMS in maize were summarized, and the problems that needed to be solved in CMS-related research and development prospects in the application of CMS in maize were discussed. This review provided theoretical reference for better understanding of the molecular mechanism of CMS in plant and the application of CMS system for hybrid seed production in the utilization of heterosis in maize.

Key words： maize; cytoplasmic male sterility; CMS genes; fertility restoration

Cite this article

Mingmin Zheng , Qiang Huang , Peng Zhang , Xiaowei Liu , Zhuofan Zhao , Hongyang Yi , Tingzhao Rong , Moju Cao . Research Progress on Cytoplasmic Male Sterility and Fertility Restoration in Maize[J]. Chinese Bulletin of Botany, 2024 , 59(6) : 999 -1006 . DOI: 10.11983/CBB24084

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References

[1] 陈庆华 (1997). 玉米“辽2(L2)”型细胞质雄性不育性的选育与利用. 玉米科学 5(2), 1-4.
[2] 陈伟程, 段韶芬 (1988). 玉米C型胞质雄性不育系花药发育的细胞学观察. 作物学报 14, 177-181.
[3] 陈伟程, 罗福和, 季良越 (1979). 玉米C型胞质雄花不育的遗传及其在生产上的应用. 作物学报 5(4), 21-28.
[4] 关淑仙 (2018). 玉米CMS-C不育系及保持系中亚化学计量基因的鉴定及分析. 硕士论文. 成都: 四川农业大学. pp. 28-57.
[5] 秦泰辰, 陈建国, 徐明良, 邓德祥, 卞云龙 (1994). 玉米雄性不育性研究VIII. 玉米YII-1型不育胞质归群初报. 作物学报 20, 677-684.
[6] 汤继华, 胡彦民, 季洪强, 陈伟程, 季良越, 郑永凯 (2001a). 玉米C型CMS育性恢复基因Rf4的SSR标记. 河南农业大学学报 35, 1-3, 8.
[7] 汤继华, 季洪强, 黄中文, 季良越, 王承花 (2001b). 玉米C型胞质不育恢复基因Rf4的RFLP定位. 河南农业大学学报 35, 99-102.
[8] 汤继华, 刘宗华, 陈伟程, 胡彦民, 季洪强, 季良越 (2001c). 玉米C型胞质不育恢复主基因SSR标记. 中国农业科学 34, 592-596.
[9] 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.
[10] 燕振国, 曾孟潜 (1999). 玉米细胞质雄性不育新类型Bao I、Bao II的发现. 遗传 21(6), 37-39.
[11] 赵素贞, 谢惠玲, 吴风华, 牛俊海, 鲁晓民, 曲延英, 汤继华 (2007). 玉米C型胞质雄性不育恢复基因Rf5的抑制基因的发现与鉴定. 玉米科学 15, 67-69.
[12] 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.
[13] Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S, Lin GN, Meyer L, Sun H, Kim K, Wang CY, Du FY, Xu D, Gibson M, Cifrese J, Clifton SW, Newton KJ (2007). Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177, 1173-1192.
[14] Bateson W, Gairdner AE (1921). Male-sterility in flax, subject to two types of segregation. J Genet 11, 269-275.
[15] Beckett JB (1971). Classification of male-sterile cytoplasms in maize (Zea mays L.). Crop Sci 11, 724-727.
[16] Chase CD (2007). Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23, 81-90.
[17] Chen LT, Liu YG (2014). Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65, 579-606.
[18] Cui XQ, Wise RP, Schnable PS (1996). The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272, 1334-1336.
[19] Dewey RE, Levings III CS, Timothy DH (1986). Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell 44, 439-449.
[20] Dewey RE, Siedow JN, Timothy DH, Levings III CS (1988). A 13-kilodalton maize mitochondrial protein in E. coli confers sensitivity to Bipolaris maydis toxin. Science 239, 293-295.
[21] Dewey RE, Timothy DH, Levings III CS (1987). A mitochondrial protein associated with cytoplasmic male sterility in the T cytoplasm of maize. Proc Natl Acad Sci USA 84, 5374-5378.
[22] Dewey RE, Timothy DH, Levings III CS (1991). Chimeric mitochondrial genes expressed in the C male-sterile cytoplasm of maize. Curr Genet 20, 475-482.
[23] 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.
[24] Duvick DN, Snyder RJ, Anderson EG (1961). The chromosomal location of Rf1, a restorer gene for cytoplasmic pollen sterile maize. Genetics 46, 1245-1252.
[25] Feng Y, Zheng Q, Song H, Wang Y, Wang H, Jiang LJ, Yan JB, Zheng YL, Yue B (2015). Multiple loci not only Rf3 involved in the restoration ability of pollen fertility, anther exsertion and pollen shedding to S type cytoplasmic male sterile in maize. Theor Appl Genet 128, 2341-2350.
[26] Gabay-Laughnan S, Chase CD, Ortega VM, Zhao LM (2004). Molecular-genetic characterization of CMS-S restorer-of-fertility alleles identified in Mexican maize and teosinte. Genetics 166, 959-970.
[27] 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.
[28] Gracen VE, Grogan CO (1974). Diversity and suitability for hybrid production of different sources of cytoplasmic male sterility in maize. Agron J 66, 654-657.
[29] Hu J, Huang WC, Huang Q, Qin XJ, Yu CC, Wang LL, Li SQ, Zhu RS, Zhu YG (2014). Mitochondria and cytoplasmic male sterility in plants. Mitochondrion 19, 282-288.
[30] Hu J, Wang K, Huang WC, Liu G, Gao Y, Wang JM, Huang Q, Ji YX, Qin XJ, Wan L, Zhu RS, Li SQ, Yang DC, Zhu YG (2012). The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24, 109-122.
[31] 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 Rf5 restorer gene for CMS-C in maize (Zea mays L.). Theor Appl Genet 113, 357-360.
[32] 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.
[33] Jaqueth JS, Li BL, Vollbrecht E (2024). Pentatricopeptide repeat 153 (PPR153) restores maize C-type cytoplasmic male sterility in conjunction with RF4. PLoS One 19, e0303436.
[34] Kamps TL, Chase CD (1997). RFLP mapping of the maize gametophytic restorer-of-fertility locus (rf3) and aberrant pollen transmission of the nonrestoring rf3 allele. Theor Appl Genet 95, 525-531.
[35] Kheyr-Pour A, Gracen VE (1980). Genetics of CMS-C fertility restoration. Maize Genet Coop News Lett 54, 57-59.
[36] Kheyr-Pour A, Gracen VE, Everett HL (1981). Genetics of fertility restoration in the C-group of cytoplasmic male sterility in maize. Genetics 98, 379-388.
[37] Kohls S, Stamp P, Knaak C, Messmer R (2011). QTL involved in the partial restoration of male fertility of C-type cytoplasmic male sterility in maize. Theor Appl Genet 123, 327-338.
[38] Korth KL, Levings III CS (1993). Baculovirus expression of the maize mitochondrial protein URF13 confers insecticidal activity in cell cultures and larvae. Proc Natl Acad Sci USA 90, 3388-3392.
[39] Laughnan JR, Gabay SJ (1978). Nuclear and cytoplasmic mutations to fertility in S male-sterile maize. In: Walden DB, ed. Maize Breeding and Genetics. New York: John Wiley & Sons Press. pp. 427-447.
[40] Laughnan JR, Gabay-Laughnan S (1983). Cytoplasmic male sterility in maize. Annu Rev Genet 17, 27-48.
[41] Lee SLJ, Earle ED, Gracen VE (1980). The cytology of pollen abortion in S cytoplasmic male-sterile corn anthers. Am J Bot 67, 237-245.
[42] Lee SLJ, Gracen VE, Earle ED (1979). The cytology of pollen abortion in C-cytoplasmic male-sterile corn anthers. Am J Bot 66, 656-667.
[43] Levings III CS (1993). Thoughts on cytoplasmic male sterility in CMS-T maize. Plant Cell 5, 1285-1290.
[44] Lin YN, 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.
[45] Liu F, Cui XQ, Horner HT, Weiner H, Schnable PS (2001). Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell 13, 1063-1078.
[46] Liu YM, Zhao ZF, Lu YL, Li C, Wang J, Dong BX, Liang B, Qiu T, Zeng WB, Cao MJ (2016). A preliminary identification of Rf*-A619, a novel restorer gene for CMS-C in maize (Zea mays L.). PeerJ 4, e2719.
[47] Matera JT, Monroe J, Smelser W, Gabay-Laughnan S, Newton KJ (2011). Unique changes in mitochondrial genomes associated with reversions of S-type cytoplasmic male sterility in maize mar. PLoS One 6, e23405.
[48] Meyer LJ (2009). Investigations Into the Cause of Pollen Abortion in Maize CMS-C. PhD dissertation. Columbia: University of Missouri. pp. 23-40.
[49] 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 the tapetum in maize. Development 144, 163-172.
[50] Qin TC, Xu ML, Dun DX (1990). Cytoplasmic male-sterility: identification of the number of the restorer genes. Maize Genet Coop News Lett 64, 124.
[51] 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.
[52] Qin XE, Zhang WL, Dong X, Tian SK, Zhang PP, Zhao YX, Wang Y, Yan JB, Yue B (2020). Identification of fertility-related genes for maize CMS-S via bulked segregant RNA-Seq. PeerJ 8, e10015.
[53] Rhoades MM (1931). Cytoplasmic inheritance of male sterility in Zea mays. Science 73, 340-341.
[54] Sisco PH (1991). Duplications complicate genetic mapping of Rf4, a restorer gene for CMS-C cytoplasmic male sterility in corn. Crop Sci 31, 1263-1266.
[55] Snyder RJ, Duvick DN (1969). Chromosomal location of Rf2, a restorer gene for cytoplasmic pollen sterile maize. Crop Sci 9, 156-157.
[56] Stamp P, Chowchong S, Menzi M, Weingartner U, Kaeser O (2000). Increase in the yield of cytoplasmic male sterile maize revisited. Crop Sci 40, 1586-1587.
[57] Su AG, Song W, Xing JF, Zhao YX, Zhang RY, Li CH, Duan MX, Luo MJ, Shi Z, Zhao JR (2016). Identification of genes potentially associated with the fertility instability of S-type cytoplasmic male sterility in maize via bulked segregant RNA-Seq. PLoS One 11, e0163489.
[58] Tie SG, Xia JH, Qiu FZ, Zheng YL (2006). Genome-wide analysis of maize cytoplasmic male sterility-S based on QTL mapping. Plant Mol Biol Report 24, 71-80.
[59] Ullstrup AJ (1972). The impacts of the southern corn leaf blight epidemics of 1970-1971. Annu Rev Phytopathol 10, 37-50.
[60] Vidakovi? M, Van?etovi? J, Vidakovi? M (1997a). Complementary genes Rf4, Rf5 and Rf6 are not the unique genetic system for fertility restoration in CMS-C of maize (Zea mays L.). Maize Genet Coop News Lett 71, 10.
[61] Vidakovi? M, Van?etovi? J, Vidakovi? M (1997b). The existence of a duplicated or parallel genetic system for fertility restoration in CMS-C of maize (Zea mays L.). Maydica 42, 313-316.
[62] Weider C, Stamp P, Christov N, Hüsken A, Foueillassar X, Camp KH, Munsch M (2009). Stability of cytoplasmic male sterility in maize under different environmental conditions. Crop Sci 49, 77-84.
[63] Wen LY, Chase CD (1999). Pleiotropic effects of a nuclear restorer-of-fertility locus on mitochondrial transcripts in male-fertile and S male-sterile maize. Curr Genet 35, 521-526.
[64] Wise RP, Dill CL, Schnable PS (1996). Mutator-induced mutations of the rf1 nuclear fertility restorer of T-cytoplasm maize alter the accumulation of T-urfl3 mitochondrial transcripts. Genetics 143, 1383-1394.
[65] Wise RP, Fliss AE, Pring DR, Gengenbach BG (1987). urf13-T of T cytoplasm maize mitochondria encodes a 13 kDa polypeptide. Plant Mol Biol 9, 121-126.
[66] Xiao HL, Zhang FD, Zheng YL (2006). The 5' stem-loop and its role in mRNA stability in maize S cytoplasmic male sterility. Plant J 47, 864-872.
[67] Xiao SL, Song W, Xing JF, Su AG, Zhao YX, Li CH, Shi Z, Li ZY, Wang S, Zhang RY, Pei YR, Chen HB, Zhao JR (2023). ORF355 confers enhanced salinity stress adaptability to S-type cytoplasmic male sterility maize by modulating the mitochondrial metabolic homeostasis. J Integr Plant Biol 65, 656-673.
[68] Xiao SL, Xing JF, Nie TG, Su AG, Zhang RY, Zhao YX, Song W, Zhao JR (2022). Comparative analysis of mitochondrial genomes of maize CMS-S subtypes provides new insights into male sterility stability. BMC Plant Biol 22, 469.
[69] 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.
[70] Xu XB, Liu ZX, Zhang DF, Liu Y, Song WB, Li JS, Dai JR (2009). Isolation and analysis of rice Rf1-orthologus PPR genes co-segregating with Rf3 in maize. Plant Mol Biol Report 27, 511-517.
[71] 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.
[72] Zhang SQ, Zhang FD, Xiao HL, Zheng YL (2004). R region of S type of cytoplasmic male sterility in maize mitochondrial DNA is transcribed in both directions and may be associated with male sterility. J Integr Plant Biol 46, 337-341.
[73] Zhang P, Zhao ZF, Zheng MM, Liu YM, Niu QK, Liu XW, Shi ZW, Yi HY, Yu T, Rong TZ, Cao MJ (2023). Fine mapping and candidate gene analysis of a novel fertility restorer gene for C-type cytoplasmic male sterility in maize (Zea mays L.). Theor Appl Genet 136, 234.
[74] Zhang ZF, Wang Y, Zheng YL (2006). AFLP and PCR-based markers linked to Rf3, a fertility restorer gene for S cytoplasmic male sterility in maize. Mol Genet Genomics 276, 162-169.
[75] Zheng MM, Yang T, Liu XW, Lü GH, Zhang P, Jiang B, Zhou SF, Lu YL, Lan H, Zhang SZ, Li C, Rong TZ, Cao MJ (2020). qRf8-1, a novel QTL for the fertility restoration of maize CMS-C identified by QTL-seq. G3(Bethesda) 10, 2457-2464.
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