植物细胞核雄性不育相关bHLH转录因子研究进展

doi:10.16288/j.yczz.15-229

遗传 ›› 2015, Vol. 37 ›› Issue (12): 1194-1203.doi: 10.16288/j.yczz.15-229

植物细胞核雄性不育相关bHLH转录因子研究进展

刘永明¹, 张玲¹, 周建瑜², 曹墨菊¹

1. 四川农业大学玉米研究所,教育部作物基因资源与遗传改良重点实验室,农业部西南玉米生物学及遗传育种重点实验室,成都 611130;
2. 四川农业大学动物医学院,雅安 625014

收稿日期:2015-05-19 出版日期:2015-12-20 发布日期:2015-10-15
通讯作者: 曹墨菊,教授,研究方向：玉米雄性不育。E-mail: caomj@sicau.edu.cn E-mail:liuluckforever@163.com
作者简介:刘永明,博士研究生,专业方向：玉米生物技术育种。E-mail: liuluckforever@163.com
基金资助:
国家高技术研究发展计划项目(863计划)(编号：2011AA10A103)资助

Research progress of the bHLH transcription factors involved in genic male sterility in plants

Yongming Liu¹, Ling Zhang¹, Jianyu Zhou², Moju Cao¹

1. Key Laboratory of Crop Genetic Resource and Improvement of Ministry of Education, Key Laboratory of Biology and Genetic Improvement of Maize in Southwest Region of Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural University, Chengdu 611130, China;
2. College of Veterinary Medicine, Sichuan Agricultural University, Ya'an 625014, China

Received:2015-05-19 Online:2015-12-20 Published:2015-10-15

摘要/Abstract

摘要： 雄性不育广泛存在于种子植物中。植物雄性不育不仅是植物生殖发育研究的重要内容,同时也可作为杂种优势利用的有效工具,因而具有重要的理论和应用价值。bHLH转录因子家族是植物中成员最多的转录因子家族,在植株的整个生长发育过程中起着重要的调控作用。本文介绍了拟南芥、水稻、玉米等几种重要模式植物bHLH转录因子调控雄蕊发育的作用机制,并重点阐述其功能异常引起细胞核雄性不育的分子机制,以期为作物育种与理论研究提供参考。

关键词: 雄性不育, bHLH转录因子, 细胞程序性死亡, 转录组测序

Abstract: Male sterility exists widely in the spermatophytes. It contributes to the study of plant reproductive development and can be used as an effective tool for hybrid seed production in heterosis utilization. Therefore, the study on male sterility is of great value in both theory and application. As one of the largest transcription factor families in plants, basic helix-loop-helix proteins (bHLHs) play a crucial role in regulating plant growth and development. This paper introduces the mechanism of bHLH regulating stamen development in several important model plants. Furthermore, we discuss the molecular mechanisms of genic male sterility resulting from bHLH dysfunction to provide references for crop breeding and theoretical studies.

Key words: male sterility, bHLH transcription factor, programmed cell death, transcriptome sequencing

刘永明, 张玲, 周建瑜, 曹墨菊. 植物细胞核雄性不育相关bHLH转录因子研究进展[J]. 遗传, 2015, 37(12): 1194-1203.

Yongming Liu, Ling Zhang, Jianyu Zhou, Moju Cao. Research progress of the bHLH transcription factors involved in genic male sterility in plants[J]. HEREDITAS(Beijing), 2015, 37(12): 1194-1203.

参考文献

[1] Wu Y, Fox TW, Trimnell MR, Wang L, Xu RJ, Cigan AM, Huffman GA, Garnaat CW, Hershey H, Albertsen MC. Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops. Plant Biotechnol J , 2015: 12477.
[2] Hu JG, Rutger JN. Pollen characteristics and genetics of induced and spontaneous genetic male-sterile mutants in rice. Plant Breed , 1992, 109(2): 97-107.
[3] 杨莉芳, 刁现民. 植物细胞核雄性不育基因研究进展. 植物遗传资源学报, 2013, 14(6): 1108-1117.
[4] Ding JH, Lu Q, Ouyang YD, Mao HL, Zhang PB, Yao JL, Xu CG, Li XH, Xiao JH, Zhang QF. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci USA , 2012, 109(7): 2654-2659.
[5] Zhou H, Zhou M, Yang YZ, Li J, Zhu LY, Jiang DG, Dong JF, Liu QJ, Gu LF, Zhou LY, Feng MJ, Qin P, Hu XC, Song CL, Shi JF, Song XW, Ni ED, Wu XJ, Deng QY, Liu ZL, Chen MS, Liu YG, Cao XF, Zhuang CX. RNase Z S1 processes Ub L40 mRNAs and controls thermosensitive genic male sterility in rice. Nat Commun , 2014, 5: 4884.
[6] Jin JP, Zhang H, Kong L, Gao G, Luo JC. PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res , 2014, 42(Database issue): D1182-D1187.
[7] Shi H, Wang X, Mo XR, Tang C, Zhong SW, Deng XW. Arabidopsis DET1 degrades HFR1 but stabilizes PIF1 to precisely regulate seed germination. Proc Natl Acad Sci USA , 2015, 112(12): 3817-3822.
[8] Castelain M, Hir RL, Bellini C. The non- DNA -binding bHLH transcription factor PRE3/bHLH135/ATBS1/TMO7 is involved in the regulation of light signaling pathway in Arabidopsis . Physiol Plant , 2012, 145(3): 450-460.
[9] Komatsu M, Maekawa M, Shimamoto K, Kyozuka J. The LAX1 and FRIZZY PANICLE 2 genes determine the inflorescence architecture of rice by controlling rachis-branch and spikelet development. Dev Biol , 2001, 231(2): 364-373.
[10] Ohno S, Deguchi A, Hosokawa M, Tatsuzawa F, Doi M. A basic helix-loop-helix transcription factor DvIVS determines flower color intensity in cyanic dahlia cultivars. Planta , 2013, 238(2): 331-343.
[11] Jiang L, Yan SS, Yang WC, Li YQ, Xia MX, Chen ZJ, Wang Q, Yan LY, Song XF, Liu RY, Zhang XL. Transcriptomic analysis reveals the roles of microtubule-related genes and transcription factors in fruit length regulation in cucumber ( Cucumis sativus L.). Sci Rep , 2015, 5: 8031.
[12] Qi TC, Huang H, Wu DW, Yan JB, Qi YJ, Song SS, Xie DX. Arabidopsis DELLA and JAZ proteins bind the WD-repeat/bHLH/MYB complex to modulate gibberellin and jasmonate signaling synergy. Plant Cell , 2014, 26(3): 1118-1133.
[13] Nakata M, Mitsuda N, Herde M, Koo AJK, Moreno JE, Suzuki K, Howe GA, Ohme-Takagi M. A bHLH-type transcription factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, acts as a repressor to negatively regulate jasmonate signaling in Arabidopsis . Plant Cell , 2013, 25(5): 1641-1656.
[14] Fan M, Bai MY, Kim JG, Wang T, Oh E, Chen L, Park CH, Son SH, Kim SK, Mudgett MB, Wang ZY. The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis . Plant Cell , 2014, 26(2): 828-841.
[15] Liu WW, Tai HH, Li SS, Gao W, Zhao M, Xie CX, Li WX. bHLH122 is important for drought and osmotic stress resistance in Arabidopsis and in the repression of ABA catabolism. New Phytol , 2014, 201(4): 1192-1204.
[16] Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martinez-Garcia JF, Bilbao-Castro JR, Robertson DL. Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis , poplar, rice, moss, and algae. Plant Physiol , 2010, 153(3): 1398-1412.
[17] Li XX, Duan XP, Jiang HX, Sun YJ, Tang YP, Yuan Z, Guo JK, Liang WQ, Chen L, Yin JY, Ma H, Wang J, Zhang DB. Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis . Plant Physiol , 2006, 141(4): 1167-1184.
[18] Toledo-Ortiz G, Huq E, Quail PH. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell , 2003, 15(8): 1749-1770.
[19] Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC. The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol , 2003, 20(5): 735-747.
[20] Bailey PC, Martin C, Toledo-Ortiz G, Quail PH, Huq E, Heim MA, Jakoby M, Werber M, Weisshaar B. Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana . Plant Cell , 2003, 15(11): 2497- 2502.
[21] Song XM, Huang ZN, Duan WK, Ren J, Liu TK, Li Y, Hou XL. Genome-wide analysis of the bHLH transcription factor family in Chinese cabbage ( Brassica rapa ssp. pekinensis ). Mol Genet Genomics , 2014, 289(1): 77-91
[22] Hudson KA, Hudson ME. A classification of basic helix-loop-helix transcription factors of soybean. Int J Genomics , 2015, 2015: 603182.
[23] Hudson KA, Hudson ME. The basic helix-loop-helix transcription factor family in the sacred lotus, Nelumbo nucifera . Trop Plant Biol , 2014, 7(2): 65-70.
[24] Sun H, Fan HJ, Ling HQ. Genome-wide identification and characterization of the bHLH gene family in tomato. BMC Genomics , 2015, 16: 9.
[25] Wang JY, Hu ZZ, Zhao TM, Yang YW, Chen TZ, Yang ML, Yu WG, Zhang BL. Genome-wide analysis of bHLH transcription factor and involvement in the infection by yellow leaf curl virus in tomato ( Solanum lycopersicum ). BMC Genomics , 2015, 16: 39.
[26] Chen ZY, Guo XJ, Chen ZX, Chen WY, Liu DC, Zheng YL, Liu YX, Wei YM, Wang JR. Genome-wide characterization of developmental stage- and tissue-specific transcription factors in wheat. BMC Genomics , 2015, 16: 125.
[27] Jiang Y, Zeng B, Zhao HN, Zhang M, Xie SJ, Lai JS. Genome-wide transcription factor gene prediction and their expressional tissue-specificities in maize. J Integr Plant Biol , 2012, 54(9): 616-630.
[28] Zhang X, Luo HM, Xu ZC, Zhu YJ, Ji AJ, Song JY, Chen SL. Genome-wide characterisation and analysis of bHLH transcription factors related to tanshinone biosynthesis in Salvia miltiorrhiz a. Sci Rep , 2015, 5: 11244.
[29] Kavas M, Baloğlu MC, Atabay ES, Ziplar UT, Daşgan HY, Ünver T. Genome-wide characterization and expression analysis of common bean bHLH transcription factors in response to excess salt concentration. Mol Genet Genomics , 2015: 1-15.
[30] Chen YY, Li MY, Wu XJ, Huang Y, Ma J, Xiong AS. Genome-wide analysis of basic helix-loop-helix family transcription factors and their role in responses to abiotic stress in carrot. Mol Breed , 2015, 35(5), doi:10.1007/s11032-015-0319-0.
[31] Ma PCM, Rould MA, Weintraub H, Pabo CO. Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell , 1994, 77(3): 451-459.
[32] Ko SS, Li MJ, Sun-Ben Ku M, Ho YC, Lin YJ, Chuang MH, Hsing HX, Lien YC, Yang HT, Chang HC, Chan MT. The bHLH142 transcription factor coordinates with TDR1 to modulate the expression of EAT1 and regulate pollen development in rice. Plant Cell , 2014, 26(6): 2486-2504.
[33] Chang AT, Liu YJ, Ayyanathan K, Benner C, Jiang YK, Prokop JW, Paz H, Wang D, Li HR, Fu XD, Rauscher FJ, Yang J. An evolutionarily conserved DNA architecture determines target specificity of the TWIST family bHLH transcription factors. Genes Dev , 2015, 29(6): 603-616.
[34] Forrest S, McNamara C. Id family of transcription factors and vascular lesion formation. Arterioscler Thromb Vasc Biol , 2004, 24(11): 2014-2020.
[35] García-Trevijano ER, Torres L, Zaragozá R, Viña JR. The role of Id2 in the regulation of chromatin structure and gene expression. Intech , 2013: 54969.
[36] Sharma P, Chinaranagari S, Chaudhary J. Inhibitor of differentiation 4 (ID4) acts as an inhibitor of ID-1, -2 and-3 and promotes basic helix loop helix (bHLH) E47 DNA binding and transcriptional activity. Biochimie , 2015, 112: 139-150.
[37] 张虹, 梁婉琪, 张大兵. 花药绒毡层细胞程序性死亡研究进展. 上海交通大学学报(农业科学版), 2008, 26(1): 86-90.
[38] Dukowic-Schulze S, Harris A, Li JH, Sundararajan A, Mudge J, Retzel EF, Pawlowski WP, Chen CB. Comparative transcriptomics of early meiosis in Arabidopsis and maize. J Genet Genomics , 2014, 41(3): 139-152.
[39] Yang HX, Lu PL, Wang YX, Ma H. The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J , 2011, 65(4): 503-516.
[40] Zhang LS, Wang L, Yang YL, Cui J, Chang F, Wang YX, Ma H. Analysis of Arabidopsis floral transcriptome: detection of new florally expressed genes and expansion of Brassicaceae -specific gene families. Front Plant Sci , 2014, 5: 802.
[41] Sorensen AM, Krӧber S, Unte US, Huijser P, Dekker K, Saedler H. The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J , 2003, 33(2): 413-423.
[42] Thorstensen T, Grini PE, Mercy IS, Alm V, Erdal S, Aasland R, Aalen RB. The Arabidopsis SET-domain protein ASHR3 is involved in stamen development and interacts with the bHLH transcription factor ABORTED MICROSPORES (AMS). Plant Mol Biol , 2008, 66(1-2): 47-59.
[43] Xu J, Ding ZW, Vizcay-Barrena G, Shi JX, Liang WQ, Yuan Z, Werck-Reichhart D, Schreiber L, Wilson ZA, Zhang DB. ABORTED MICROSPORES acts as a master regulator of pollen wall formation in Arabidopsis . Plant Cell , 2014, 26(4): 1544-1556.
[44] Ma X, Feng BM, Ma H. AMS-dependent and independent regulation of anther transcriptome and comparison with those affected by other Arabidopsis anther genes. BMC Plant Biol , 2012, 12: 23.
[45] Zhang W, Sun YJ, Timofejeva L, Chen CB, Grossniklaus U, Ma H. Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development , 2006, 133(16): 3085-3095.
[46] Feng BM, Lu DH, Ma X, Peng YB, Sun YJ, Ning G, Ma H. Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J , 2012, 72(4): 612-624.
[47] Gu JN, Zhu J, Yu Y, Teng XD, Lou Y, Xu XF, Liu JL, Yang ZN. DYT1 directly regulates the expression of TDF1 for tapetum development and pollen wall formation in Arabidopsis . Plant J , 2014, 80(6): 1005-1013.
[48] Zhu EG, You CJ, Wang SS, Cui J, Niu BX, Wang YX, Qi J, Ma H, Chang F. The DYT1-interacting proteins bHLH010, bHLH089 and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome. Plant J , 2015, 83(6): 976-990.
[49] Nakata M, Ohme-Takagi M. Two bHLH-type transcription factors, JA-ASSOCIATED MYC2-LIKE2 and JAM3, are transcriptional repressors and affect male fertility. Plant Signal Behav , 2013, 8(12): e26473.
[50] Figueroa P, Browse J. Male sterility in Arabidopsis induced by overexpression of a MYC5-SRDX chimeric repressor. Plant J , 2015, 81(6): 849-860.
[51] Xing SP, Quodt V, Chandler J, Hӧhmann S, Berndtgen R, Huijser P. SPL8 acts together with the brassinosteroid-signaling component BIM1 in controlling Arabidopsis thaliana male fertility. Plants , 2013, 2(3): 416-428.
[52] Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell , 2005, 17(10): 2705-2722.
[53] Zhang DS, Liang WQ, Yuan Z, Li N, Shi J, Wang J, Liu YM, Yu WJ, Zhang DB. Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant , 2008, 1(4): 599-610.
[54] 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. The rice Tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell , 2006, 18(11): 2999-3014.
[55] Niu NN, Liang WQ, Yang XJ, Jin WL, Wilson ZA, Hu JP, Zhang DB. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat Commun , 2013, 4(2): 1445.
[56] Ji CH, Li HY, Chen LB, Xie M, Wang FP, Chen YL, Liu YG. A novel rice bHLH transcription factor, DTD, acts coordinately with TDR in controlling tapetum function and pollen development. Mol Plant , 2013, 6(5): 1715-1718.
[57] Fu ZZ, Yu J, Cheng XW, Zong X, Xu J, Chen MJ, Li ZY, Zhang DB, Liang WQ. The rice basic helix-loop-helix transcription factor TDR INTERACTING PROTEIN2 is a central switch in early anther development. Plant Cell , 2014, 26(4): 1512-1524.
[58] Crismani W, Kapoor S, Able JA. Comparative transcriptomics reveals 129 transcripts that are temporally regulated during anther development and meiotic progression in both bread wheat ( Triticum aestivum ) and rice ( Oryza sativa ). Int J Plant Genomics , 2011: 931898.
[59] Collado-Romero M, Alós E, Prieto P. Unravelling the proteomic profile of rice meiocytes during early meiosis. Front Plant Sci , 2014, 5: 356.
[60] Zhang H, Egger RL, Kelliher T, Morrow D, Fernandes J, Nan GL, Walbot V. Transcriptomes and proteomes define gene expression progression in pre-meiotic maize anthers. G3 (Bethesda) , 2014, 4(6): 993-1010.
[61] Dukowic-Schulze S, Sundararajan A, Mudge J, Ramaraj T, Farmer AD, Wang MH, Sun Q, Pillardy J, Kianian S, Retzel EF, Pawlowski WP, Chen CB. The transcriptome landscape of early maize meiosis. BMC Plant Biol , 2014, 14: 118.
[62] Moon J, Skibbe D, Timofejeva L, Rachel Wang CJ, Kelliher T, Kremling K, Walbot V, Cande WZ. Regulation of cell divisions and differentiation by MALE STERILITY32 is required for anther development in maize. Plant J , 2013, 76(4): 592-602.
[63] Ren RH, Nagel BA, Kumpatla SP, Zheng PZ, Cutter GL, Greene TW, Thompson SA. Maize cytoplasmic male sterility (cms) c-type restorer rf4 gene, molecular markers and their use: U.S. Patent Application 20120090047. 2013-08-14.
[64] Liu TK, Li Y, Zhang CW, Duan WK, Huang FY, Hou XL. Basic helix-loop-helix transcription factor BcbHLHpol functions as a positive regulator of pollen development in non-heading Chinese cabbage. Funct Integr Genomics , 2014, 14(4): 731-739.
[65] Jeong HJ, Kang JH, Zhao MA, Kwon JK, Choi HS, Bae JH, Lee HA, Joung YH, Choi D, Kang BC. Tomato Male sterile 10 35 is essential for pollen development and meiosis in anthers. J Exp Bot , 2014, 65(22): 6693-6709.

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