RESEARCH PAPER

Identification and Mapping of a Rice Male Sterility Mutant ms102

Expand
  • 1Guangdong Provincial Key Laboratory of Biotechnology for Plant Development/School of Life Sciences, South China Normal University, Guangzhou 510631, China
    2Shenzhen Institute of Molecular Crop Design, Shenzhen 518107, China

Received date: 2021-09-14

  Accepted date: 2021-11-17

  Online published: 2021-11-17

Abstract

The recessive nuclear male sterility line is the base of the third-generation hybrid rice breeding technology. To explore new male sterility lines suitable for the breeding technology, we screened an ethyl methylsulfonate (EMS) mutant library derived from the elite xian variety Huanghuazhan (HHZ) and identified male sterility mutant 102 (ms102). The ms102 showed a normal vegetative development, but exhibited defective anther dehiscence and pollen abortion. Cytological analyses revealed that the degradation of the tapetum was abnormal in ms102, resulting in the abortion of microspores. Genetic analyses showed that the male sterile phenotype of ms102 was resulted from the mutation of a known male sterility gene Defective Pollen Wall 2 (DPW2), which encodes an acyl transferase. Thus, this study identified a recessive nuclear male sterility mutant, and further confirmed the function of DPW2 in rice pollen development.

Cite this article

Xia Wang, Wei Yan, Zhiqin Zhou, Zhenyi Chang, Minting Zheng, Xiaoyan Tang, Jianxin Wu . Identification and Mapping of a Rice Male Sterility Mutant ms102[J]. Chinese Bulletin of Botany, 2022 , 57(1) : 42 -55 . DOI: 10.11983/CBB21158

References

[1] 陈竹锋, 卢嘉威, 卢启清, 王娜, 王成旭, 谢刚, 周向阳, 唐晓艳 (2014). 优质水稻黄华占雄性不育突变体的筛选及初步分析. 广东农业科学 41(19), 1-4.
[2] 邓兴旺, 王海洋, 唐晓艳, 周君莉, 陈浩东, 何光明, 陈良碧, 许智宏 (2013). 杂交水稻育种将迎来新时代. 中国科学: 生命科学 43, 864-868.
[3] 李文杰 (2019). 水稻花粉发育基因LSP2的克隆及功能研究. 硕士论文. 成都: 四川农业大学. pp. 1-2.
[4] 倪浩凌, 吴文诗, 颜艳敏, 方亦圆, 王嘉茵, 陈碧湖, 李芷怡, 唐晓艳, 吴建新 (2020). 水稻穗发芽突变体的筛选及候选基因鉴定. 植物遗传资源学报 21, 1214-1220.
[5] 张彤, 郭亚璐, 陈悦, 马金姣, 兰金苹, 燕高伟, 刘玉晴, 徐珊, 李莉云, 刘国振, 窦世娟 (2019). 水稻OsPR10A的表达特征及其在干旱胁迫应答过程中的功能. 植物学报 54, 711-722.
[6] Abbas A, Yu P, Sun LP, Yang ZF, Chen DB, Cheng SH, Cao LY (2021). Exploiting genic male sterility in rice: from molecular dissection to breeding applications. Front Plant Sci 12, 629314.
[7] Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M, Innan H, Cano L, Kamoun S, Terauchi R (2012). Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30, 174-178.
[8] Ali Z, Raza Q, Atif RM, Aslam U, Ajmal M, Chung G (2019). Genetic and molecular control of floral organ iden- tity in cereals. Int J Mol Sci 20, 2743
[9] Ariizumi T, Toriyama K (2011). Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62, 437-460.
[10] Bai WT, Wang PR, Hong J, Kong WY, Xiao YJ, Yu XW, Zheng H, You SM, Lu JY, Lei DK, Wang CL, Wang QM, Liu SJ, Liu X, Tian YL, Chen LM, Jiang L, Zhao ZG, Wu CY, Wan JM (2019). Earlier Degraded Tapetum 1 (EDT1) encodes an ATP-citrate lyase required for tapetum programmed cell death. Plant Physiol 181, 1223-1238.
[11] Bayer A, Ma XY, Stöckigt J (2004). Acetyltransfer in natural product biosynthesis-functional cloning and molecular analysis of vinorine synthase. Bioorg Med Chem 12, 2787-2795.
[12] Chang ZY, Chen ZF, Wang N, Xie G, Lu JW, Yan W, Zhou JL, Tang XY, Deng XW (2016a). Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene. Proc Natl Acad Sci USA 113, 14145-14150.
[13] Chang ZY, Chen ZF, Yan W, Xie G, Lu JW, Wang N, Lu QQ, Yao N, Yang GZ, Xia JX, Tang XY (2016b). An ABC transporter, OsABCG26, is required for anther cuticle and pollen exine formation and pollen-pistil interactions in rice. Plant Sci 253, 21-30.
[14] Chang ZY, Jin MN, Yan W, Chen H, Qiu SJ, Fu S, Xia JX, Liu YC, Chen ZF, Wu JX, Tang XY (2018). The ATP- binding cassette (ABC) transporter OsABCG3 is essential for pollen development in rice. Rice 11, 58.
[15] Chang ZY, Xu CJ, Huang XY, Yan W, Qiu SJ, Yuan ST, Ni HL, Chen SJ, Xie G, Chen ZF, Wu JX, Tang XY (2020). The plant-specific ABERRANT GAMETOGENESIS 1 gene is essential for meiosis in rice. J Exp Bot 71, 204-218.
[16] Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010). Food security: the challenge of feeding 9 billion people. Science 327, 812-818.
[17] Gómez JF, Talle B, Wilson ZA (2015). Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57, 876-891.
[18] Greene EA, Codomo CA, Taylor NE, Henikoff JG, Till BJ, Reynolds SH, Enns LC, Burtner C, Johnson JE, Odden AR, Comai L, Henikoff S (2003). Spectrum of chemically induced mutations from a large-scale reverse- genetic screen in Arabidopsis. Genetics 164, 731-740.
[19] Ji CH, Li HY, Chen LB, Xie M, Wang FP, Chen YL, Liu YG (2013). A novel rice bHLH transcription factor, DTD, acts coordinately with TDR in controlling tapetum function and pollen development. Mol Plant 6, 1715-1718.
[20] Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005). Rice Undeveloped Tapetum 1 is a major regulator of early tapetum development. Plant Cell 17, 2705-2722.
[21] Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M, Matsuoka M (2004). Loss-of-function mutations of the rice GAMYB gene impair α-amylase expression in aleurone and flower development. Plant Cell 16, 33-44.
[22] Kim YS, Schumaker KS, Zhu JK (2006). EMS mutagenesis of Arabidopsis. In: Salinas J, Sanchez-Serrano JJ, eds. Arabidopsis Protocols. Totowa: Humana Press. pp. 101- 103.
[23] Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao YW, Liang WQ, Zhang DB (2010a). Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22, 173-190.
[24] Li H, Yuan Z, Vizcay-Barrena G, Yang CY, Liang WQ, Zong J, Wilson ZA, Zhang DB (2011). PERSISTENT TAPETAL CELL 1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156, 615-630.
[25] Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006). The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999-3014.
[26] Li YD, Chu ZZ, Liu XG, Jing HC, Liu YG, Hao DY (2010b). A cost-effective high-resolution melting approach using the EvaGreen dye for DNA polymorphism detection and genotyping in plants. J Integr Plant Biol 52, 1036-1042.
[27] Liao CC, Yan W, Chen ZF, Xie G, Deng XW, Tang XY (2021). Innovation and development of the third-generation hybrid rice technology. Crop J 9, 693-701.
[28] Liu ZH, Bao WJ, Liang WQ, Yin JY, Zhang DB (2010). Identification of gamyb-4 and analysis of the regulatory role of GAMYB in rice anther development. J Integr Plant Biol 52, 670-678.
[29] Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408.
[30] Lochlainn SÓ, Amoah S, Graham NS, Alamer K, Rios JJ, Kurup S, Stoute A, Hammond JP, Østergaard L, King GJ, White PJ, Broadley MR (2011). High Resolution Melt (HRM) analysis is an efficient tool to genotype EMS mutants in complex crop genomes. Plant Methods 7, 43.
[31] Luo H, Lee JY, Hu Q, Nelson-Vasilchik K, Eitas TK, Lickwar C, Kausch AP, Chandlee JM, Hodges TK (2006). RTS, a rice anther-specific gene is required for male fertility and its promoter sequence directs tissue- specific gene expression in different plant species. Plant Mol Biol 62, 397-408.
[32] Ma H (2005). Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56, 393-434.
[33] Nonomura KI, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003). The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15, 1728-1739.
[34] Nonomura KI, Nakano M, Eiguchi M, Suzuki T, Kurata N (2006). PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J Cell Sci 119, 217-225.
[35] Nonomura KI, Nakano M, Fukuda T, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004). The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis. Plant Cell 16, 1008-1020.
[36] Pan XY, Yan W, Chang ZY, Xu YC, Luo M, Xu CJ, Chen ZF, Wu JX, Tang XY (2020). OsMYB80 regulates anther development and pollen fertility by targeting multiple biological pathways. Plant Cell Physiol 61, 988-1004.
[37] Peng XQ, Wang ML, Li YQ, Yan W, Chang ZY, Chen ZF, Xu CJ, Yang CW, Deng XW, Wu JX, Tang XY (2020). Lectin receptor kinase OsLecRK-S.7 is required for pollen development and male fertility. J Integr Plant Biol 62, 1227-1245.
[38] Quilichini TD, Grienenberger E, Douglas CJ (2015). The biosynthesis, composition and assembly of the outer pollen wall: a tough case to crack. Phytochemistry 113, 170-182.
[39] Shi J, Tan HX, Yu XH, Liu YY, Liang WQ, Ranathunge K, Franke RB, Schreiber L, Wang YJ, Kai GY, Shanklin J, Ma H, Zhang DB (2011). Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell 23, 2225-2246.
[40] Suzuki H, Nakayama T, Nishino T (2003). Proposed mecha- nism and functional amino acid residues of malonyl-CoA: anthocyanin 5-O-glucoside-6'''-O-malonyltransferase from flowers of Salvia splendens, a member of the versatile plant acyltransferase family. Biochemistry 42, 1764-1771.
[41] Wang B, Fang RQ, Chen FM, Han JL, Liu YG, Chen LT, Zhu QL (2020). A novel CCCH-type zinc finger protein SAW1 activates OsGA20ox3 to regulate gibberellin homeostasis and anther development in rice. J Integr Plant Biol 62, 1594-1606.
[42] Xu DW, Shi JX, Rautengarten C, Yang L, Qian XL, Uzair M, Zhu L, Luo Q, An G, Waßmann F, Schreiber L, Heazlewood JL, Scheller HV, Hu JP, Zhang DB, Liang WQ (2017). DPW2) encodes an acyl transferase required for rice pollen development. Plant Physiol 173, 240-255.
[43] Yan W, Chen ZF, Lu JW, Xu CJ, Xie G, Li YQ, Deng XW, He H, Tang XY (2017). Simultaneous identification of multiple causal mutations in rice. Front Plant Sci 7, 2055.
[44] Yan W, Deng XW, Yang C, Tang X (2021). The genome-wide EMS mutagenesis bias correlates with sequence context and chromatin structure in rice. Front Plant Sci 12, 579675.
[45] Yang XJ, Wu D, Shi JX, He Y, Pinot F, Grausem B, Yin CS, Zhu L, Chen MJ, Luo ZJ, Liang W, Zhang D (2014). Rice CYP703A3, a cytochrome P450 hydroxylase, is essential for development of anther cuticle and pollen exine. J Integr Plant Biol 56, 979-994.
[46] Yang ZF, Liu L, Sun LP, Yu P, Zhang PP, Abbas A, Xiang XJ, Wu WX, Zhang YX, Cao LY, Cheng SH (2019). OsMS1 functions as a transcriptional activator to regulate programmed tapetum development and pollen exine formation in rice. Plant Mol Biol 99, 175-191.
[47] Yi J, Kim SR, Lee DY, Moon S, Lee YS, Jung KH, Hwang I, An G (2012). The rice gene DEFECTIVE TAPETUM AND MEIOCYTES 1 (DTM1) is required for early tapetum development and meiosis. Plant J 70, 256-270.
[48] Zhang DB, Luo X, Zhu L (2011). Cytological analysis and genetic control of rice anther development. J Genet Genomics 38, 379-390.
[49] Zhang HH, Wang ML, Li YQ, Yan W, Chang ZY, Ni HL, Chen ZF, Wu JX, Xu CJ, Deng XW, Tang XY (2020). GDSL esterase/lipases OsGELP34 and OsGELP110/OsGELP115 are essential for rice pollen development. J Integr Plant Biol 62, 1574-1593.
Outlines

/