干旱胁迫下水稻生殖发育相关分析
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摘要
水稻是我国乃至世界上最重要的粮食作物之一,具有突出的战略意义。近年来随着全球气候的剧变,干旱问题对水稻的正常生产活动产生越来越大的影响。花是水稻的生殖器官,其在干旱情况下的状态直接影响到水稻产量。以前大部分干旱研究集中于水稻营养期的根、叶等器官,而对于花器官应对干旱胁迫的研究甚少。我们通过对处于水稻减数分裂期前后的水稻进行干旱处理,收集处于不同发育时期的花,以正常生长情况下的花作为对照,通过基因芯片实验来调查水稻花的基因表达谱变化。通过多次生物学重复实验获得了大量的数据,对这些数据的分析整理发现,包括激素、能量代谢、生物胁迫等在内的多个信号转导途径受到影响,正负调控作用共同存在,从而使得胁迫下水稻花发育相关器官的形态以及育性异常。对处于减数分裂期前后的水稻3-5mm长度的花的三次基因芯片分析发现,在干旱胁迫下有339个基因的表达水平重复性地上调,118个基因表达水平重复性地下调。对于这些在三次实验中均重复出现的基因,我们按其生物学功能进行了归类,并对其进行了初步分析。结果显示,所发现的这些基因,部分已被验证确实与干旱胁迫相关,有一部分基因则是首次发现；另外一些基因则显示出在于旱过程的多重角色,有些既参与了信号转导也参与了代谢,可能对水稻的生殖发育产生影响。这些基因成为我们的关注点,可能对于改善干旱胁迫下的水稻生殖发育具有重要的作用。通过Real-Time PCR对部分基因的表达水平验证证明了芯片数据的可靠性。在此基础上,挑选了部分基因进行克隆,通过转基因手段来验证它们是否有助于改善干旱胁迫下的水稻育性。
Rice is one of the most important crops in china and even in the world. In recent years, drought has caused severe rice yield loss, especially in those water-deficit areas.Improving rice growth and development under drought stress is important for maintaining grain yield,Previous research mainly focus on the effect of drought on root and leaf development during vegetative growth stage. However, flower, as the reproductive organ, will directly affect the grain production. It remains unclear how rice floral organs respond to water-deficit condition and therefore alter the reproductive development.Our research aims to understand the molecular mechanisms regulating this process, and finally to improve rice yield under drought stress.
Responses of rice florets to drought stress at the molecular level around meiosis stage were studied in order to obtain candidate genes which can improve rice drought tolerance. We treated the rice plants at early reproductive stages with less water than normal, then hold the same SRWC (soil relative water content) for about seven days. After that, we collected the drought-treated and control rice flowers according to the the length of florets. RNA is extracted for microarray analysis. By analysis of the microarray data, we found that some genes and pathways have been induced or inhibited under drought stress, suggesting that the cell status of rice florets, such as energy metabolism, oxireduction status have been altered. The gene-chip analysis experiments were repeated in triplicate.339 genes were found to be repeatedly up-regulated and 118 genes down-regulated under drought stress.
We further classify these genes according to their GO and annotations, as well as the information from published papers. The results show that some of the genes have already been reported to be involved in drought resistance, and others are new. Some genes are involved in multiple pathways such as cell metabolism and flower developement.More experiments will be necessary to further characterize their roles under drought stress.Real-Time PCR was used to confirm the microarry data,and the results are generally consistent. Based on the analysis results, several genes were chosen for further identification. Overexpression of these genes in rice flowers will allow us to understand if they can improve rice reproductive development under drought condition.
Rice is one of the most important crops in china and even in the world. In recent years, drought has caused severe rice yield loss, especially in those water-deficit areas.Improving rice growth and development under drought stress is important for maintaining grain yield,Previous research mainly focus on the effect of drought on root and leaf development during vegetative growth stage. However, flower, as the reproductive organ, will directly affect the grain production. It remains unclear how rice floral organs respond to water-deficit condition and therefore alter the reproductive development.Our research aims to understand the molecular mechanisms regulating this process, and finally to improve rice yield under drought stress.
Responses of rice florets to drought stress at the molecular level around meiosis stage were studied in order to obtain candidate genes which can improve rice drought tolerance. We treated the rice plants at early reproductive stages with less water than normal, then hold the same SRWC (soil relative water content) for about seven days. After that, we collected the drought-treated and control rice flowers according to the the length of florets. RNA is extracted for microarray analysis. By analysis of the microarray data, we found that some genes and pathways have been induced or inhibited under drought stress, suggesting that the cell status of rice florets, such as energy metabolism, oxireduction status have been altered. The gene-chip analysis experiments were repeated in triplicate.339 genes were found to be repeatedly up-regulated and 118 genes down-regulated under drought stress.
We further classify these genes according to their GO and annotations, as well as the information from published papers. The results show that some of the genes have already been reported to be involved in drought resistance, and others are new. Some genes are involved in multiple pathways such as cell metabolism and flower developement.More experiments will be necessary to further characterize their roles under drought stress.Real-Time PCR was used to confirm the microarry data,and the results are generally consistent. Based on the analysis results, several genes were chosen for further identification. Overexpression of these genes in rice flowers will allow us to understand if they can improve rice reproductive development under drought condition.
引文
[1]Muhammad, AbdulWahid, Dong, Osamu, and Kadambot H. M. Siddique. Advances in drought resistance of rice [J]. Critical Reviews in Plant Science,2009, 28:199-217.
[2]王贺正,马均,刘慧远.水稻抗旱性研究现状与展望[J]. Chinese Agricultural Science Bulletin,2005,21:110-113.
[3]蒋明义,郭绍川.渗透胁迫下稻苗中铁催化的膜脂过氧化作用[J].植物生理学报,1996,22：6-12.
[4]王万里.植物对水分胁迫的反应[M].植物生理学专题讲座,北京：科学出版社,1986：357-369
[5]李艳,马均,王贺正.水稻品种苗期抗旱性鉴定指标筛选及其综合评价[J].西南农业学报,2005,18：250-255.
[6]戴高兴,邓国富,周萌.干旱胁迫对水稻生理生化的影响[J].广西农业科学,2006,37(1)：4-6.
[7]王玉玲,陈清西.植物生殖发育及环境胁迫相关特异蛋白质的研究进展[J].中国农业科技导报,2006,8(2)：32-35.
[8]杨弘远.水稻生殖生物学[M].浙江大学出版社,2005：58-70.
[9]刘坚,郭龙彪,钱前.水稻花器官发育基因的研究进展[J].中国稻米,2007,3：8-9.
[10]Chen. Cell biological characterization of male meiosis and pollen development in rice [J]. Journal of Integrative Plant Biology Formerly Acta Botanica Sinica,2005, 47(6):734-744.
[11]Zoe A. Wilsonl, and Zhang.From Arabidopsis to rice:pathways in pollen development [J]. J. Experimental Botany,2009,60(5):1479-1492.
[12]Zhou, Wang, Jiao, and Deng. Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle [J]. Plant Mol Biol,2007,63:591-608.
[13]Yue., Xiong, Xue, and Xu. Genetic analysis for drought resistance of rice at reproductive stage in field with different types of soil [J]. Theor Appl Genet,2005,3: 1127-1136.
[14]Ji., M.Raveendran, R.Oane, and J.Bennett. Tissue-specific expression and drought responsiveness of cell-wall invertase genes of rice at flowering [J]. Plant Molecular Biology,2005,59:945-964.
[15]Wang., Guan, andChu. Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice [J]. Plant Mol Biol,2008,67:589-602.
[16]沈忠伟,许昱,夏犇、李建粤.植物类黄酮次生代谢生物合成相关转录因子及其在基因工程中的应用[J].分子植物育种,2008,6(3)：542-548.
[17]张松焕,郭惠明,裴熙祥,李春奇,程红梅.紫茎泽兰类黄酮3’-羟化酶在烟草中的表达[J].中国农业科学,2009,,42(12)：4182-4186.
[18]范敏,金黎平,黄三文,谢开云,刘庆昌,屈冬玉.干旱胁迫对马铃薯类黄酮和类胡萝卜素合成关键酶基因表达的影响[J].园艺学报,2008,.35(4)：535-542.
[19]Zhu., Verslues.PE, and Zheng. HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plant [J]. Proc. Natl. Acad. Sci.-USA, 2005,102(28):9966-9971.
[20]Wang., Li., Chen, and Xia. Characterization and pilotfunctional study of a rootspecific MYB transcription factor of Arabidopsis [J]. Chinese Science Bulletin, 2002,47(4):
[21]唐益苗,赵昌平,高世庆,田立平,单福华,吴敬新.植物抗旱相关基因研究进展[J].麦类作物学报,2009,29(1)：166-173.
[22]Ralf Stracke, Martin, and Bernd. The R2R3-MYB gene family in Arabidopsis thaliana [J].Curr Opin Plant Biol,2001,4(5):47-56.
[23]Ariadna, Ludovic.B, Zhu, Paul, and Teresa. Molecular characterization of the Arginine decarboxylase gene family in rice [J]. Transgenic Research,2010, DOI 10.1007/s11248-009-9354-0.
[24]Sakihito, Kitajima, and Fumihiko.S. Plant Pathogenesis-Related Proteins: Molecular Mechanisms of Gene Expression and Protein Function [J]. J. Biochem, 1999,125:1-8.
[25]张岗,李依民,张毅,董艳玲,王晓杰,魏国荣,黄丽丽,康振生.条锈菌诱导的小麦病程相关蛋白TaPR10基因的克隆及特征分析[J].中国农业科学,2009,42(1)：110-116.
[26]Charlotta filling. Short-chain dehydrogenase/reductase protein-structure, function and motifs [M]. Karolinska institute stockhlom,2002:1-63.
[27]Sylvia Morais de Sousa, Ma'rio del Giu'dice Paniago, Paulo Arruda, Jose' Andre's Yunes.Sugar levels modulate sorbitol dehydrogenase expression in maize [J] Plant Mol Biol,2008,68:203-213.
[28]贺丽虹,赵淑娟,胡之璧.植物细胞色素P450基因与功能研究进展[J]Pharmaceutical Biotechnology,2008,15(2):142-147.
[29]潘雅姣,王迪,朱苓华,傅彬英,黎志康.水稻双组分系统基因干旱胁迫表达谱分析[J]. ACTA AGRONOMICA SINICA 2009,35(9):1628-1636.
[30]何新建,陈健权,张志刚,张劲松,陈受宜.通过cDNA微阵列鉴定水稻盐胁迫应答基因[J].中国科学C辑,2002,32(6)：488-493.
[31]Finnegan EJ, Peacock., Dennis.A cluster of Arabidopsis genes with a coordinate response to an environmental stimulus [J]. Curr Biol,2004,14(10):911-916.
[32]Yang., He, Yu, Chen, Lei, JiJ. Influence of drought on oxidative stress and flavonoid production in cell suspension culture of Glycyrrhiza inflata Batal [J]. Z Naturforsch C,2007,62(5-6):410-416.
[33]Galle A,Csiszar J,Secenji M,Guoth A,Cseuz L,Tari I,Gyorgyey J, Erdei L. Glutathione transferase activity-and expression patterns during grain filling in flag leaves of wheat genotypes differing in drought tolerance:Response to water deficit [J] Plant Physiol,2009,166(17):1878-1891.
[34]Ayman A. Diab, R. V. Kantety, N. Z. Ozturk, D. Benscher, M. M. Nachit and M. E. Sorrells. Drought-inducible genes and differentially expressed sequence tags associated with components of droughttolerance in durum wheat [J]. Scientific Research and Essay,2008,3 (1):009-026.
[35]Nguyen, C.-L.Ho, J.A.Harikrishna, M.wong, and R.Abdul Rahim. Functional screening for salinity tolerant genes from Acanthus ebracteatus Vahl using Escherichia coli as a host [J]. Trees,2007,21:515-520.
[36]高凤华,张洪亮,王海光,高宏,李自超.应用cDNA-AFLP比较干旱胁迫条件下水稻和旱稻转录本表达谱[J].科学通报,2009,54(16)：2305-2319.
[37]Kaoru T. Yoshida, Makoto Endo. Mikio Nakazono, Hiroo Fukuda, Taku Demura. Tohru Tsuchiya, Masao Watanabe. cDNA microarray analysis of gene expression changes during pollination, pollen-tube elongation, fertilization, and early embryogenesis in rice pistils [J]. Sex Plant Reprod,2005,17:269-275.
[38]Lin., XU., Ni, Chu, Xu., and Xue. Identification of ABA-responsive genes in rice shoots via cDNA macroarray [J]. Cell Research,2003,13:59-68.
[39]Kazuo Shinozaki and Kazuko Yamaguchi-Shinozaki. Gene networks involved in drought stress response and tolerance [J]. Journal of Experimental Botany,2007, 58(2):221-227.
[40]Kizis D., Lumbreras V., and Pags M. Role ofAP2/EREBP transcription factors in gene regulation during abiotic stress [J]. FEBS letters,2001,498(2-3):187-189.
[41]Morinaga T. On the microsporogenesis of the various interspecific hybrids of Oryza [J]. Japan J C-enet,1937,13:245.
[42]Klimyuk, V. I. and J. D. G. Jones. AtDMC1, the Arabidopsis homolog of the yeast DMC1 gene:characterization, transposon-induced allelic variation and meiosis-associated expression [J]. The Plant Journal,1997,11:1-14.
[43]Yang, M., Hu, Y., Lodhi, M., McCombie, W. R. and Ma, H. The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation [J]. Proc. Natl. Acad. Sci. USA,1999,96:11416-11421.
[44]I. siddiqi, G. ganesh, U. grossniklaus and V. subbiah. The dyad gene is required for progression through female meiosis in Arabidopsis [J].2000, Development,127: 197-207.
[45]Magnard JL, Yang. M, Chen.YCS, Leary M, and McCormick.S. The Arabidopsis thaliana gene TARDY ASYNCHRONOUS MEIOSIS(TAM) is required for the normal pace and synchrony of cell division during male meiosis [J]. Plant Physiol,2001, 127:1157-1166.
[46]Azumi Y, Liu D, Zhao D, Li W, Wang G, Hu Y, Ma H. Homolog interaction during meiotic prophase Ⅰ in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein [J]. EMBO J,2002,21:3081-3095.
[47]Chen., Adam Marcus, Li., Hu, Jean-Philippe Vielle Calzada, Ueli Grossniklaus, Richard J. Cyr, and Ma. The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis [J].Development,2002,129:2401-2409.
[48]Yang, X.H., Makaro., C.A., Ma, H. The Arabidopsis male meiocyte death1 gene encodes a PHD-finger protein that is required for male meiosis [J].Plant Cell,2003,15: 1281-1295.
[49]James D. Higgins, Susan J. Armstrong, F. Christopher H. Franklin, and Gareth H. Jones. The Arabidopsis MutS homolog AtMSH4functions at an early step in recombination:evidence for two classes of recombination in Arabidopsis [J]. Genes & Dev,2004,18:2557-2570.
[50]Li.,Chen., Ullrich Markmann-Mulisch, LjudmillaTimofejeva, Elmon Schmelzer, Hong Ma, and Bernd Reiss. The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis [J]. Proc. Natl. Acad. Sci. USA,2004, 101:10596-10601.
[51]Bleuyard JY, White CI. The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis [J]. EMBO J,2004,23(2):439-49.
[52]Ding Z, Wang T, Chong K, Bai S. Isolation and characterization of OsDMCl, the rice homologue of the yeast DMC1 gene essential for meiosis [J]. Sex Plant Reprod,2001,13:285-288.
[2]王贺正,马均,刘慧远.水稻抗旱性研究现状与展望[J]. Chinese Agricultural Science Bulletin,2005,21:110-113.
[3]蒋明义,郭绍川.渗透胁迫下稻苗中铁催化的膜脂过氧化作用[J].植物生理学报,1996,22：6-12.
[4]王万里.植物对水分胁迫的反应[M].植物生理学专题讲座,北京：科学出版社,1986：357-369
[5]李艳,马均,王贺正.水稻品种苗期抗旱性鉴定指标筛选及其综合评价[J].西南农业学报,2005,18：250-255.
[6]戴高兴,邓国富,周萌.干旱胁迫对水稻生理生化的影响[J].广西农业科学,2006,37(1)：4-6.
[7]王玉玲,陈清西.植物生殖发育及环境胁迫相关特异蛋白质的研究进展[J].中国农业科技导报,2006,8(2)：32-35.
[8]杨弘远.水稻生殖生物学[M].浙江大学出版社,2005：58-70.
[9]刘坚,郭龙彪,钱前.水稻花器官发育基因的研究进展[J].中国稻米,2007,3：8-9.
[10]Chen. Cell biological characterization of male meiosis and pollen development in rice [J]. Journal of Integrative Plant Biology Formerly Acta Botanica Sinica,2005, 47(6):734-744.
[11]Zoe A. Wilsonl, and Zhang.From Arabidopsis to rice:pathways in pollen development [J]. J. Experimental Botany,2009,60(5):1479-1492.
[12]Zhou, Wang, Jiao, and Deng. Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle [J]. Plant Mol Biol,2007,63:591-608.
[13]Yue., Xiong, Xue, and Xu. Genetic analysis for drought resistance of rice at reproductive stage in field with different types of soil [J]. Theor Appl Genet,2005,3: 1127-1136.
[14]Ji., M.Raveendran, R.Oane, and J.Bennett. Tissue-specific expression and drought responsiveness of cell-wall invertase genes of rice at flowering [J]. Plant Molecular Biology,2005,59:945-964.
[15]Wang., Guan, andChu. Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice [J]. Plant Mol Biol,2008,67:589-602.
[16]沈忠伟,许昱,夏犇、李建粤.植物类黄酮次生代谢生物合成相关转录因子及其在基因工程中的应用[J].分子植物育种,2008,6(3)：542-548.
[17]张松焕,郭惠明,裴熙祥,李春奇,程红梅.紫茎泽兰类黄酮3’-羟化酶在烟草中的表达[J].中国农业科学,2009,,42(12)：4182-4186.
[18]范敏,金黎平,黄三文,谢开云,刘庆昌,屈冬玉.干旱胁迫对马铃薯类黄酮和类胡萝卜素合成关键酶基因表达的影响[J].园艺学报,2008,.35(4)：535-542.
[19]Zhu., Verslues.PE, and Zheng. HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plant [J]. Proc. Natl. Acad. Sci.-USA, 2005,102(28):9966-9971.
[20]Wang., Li., Chen, and Xia. Characterization and pilotfunctional study of a rootspecific MYB transcription factor of Arabidopsis [J]. Chinese Science Bulletin, 2002,47(4):
[21]唐益苗,赵昌平,高世庆,田立平,单福华,吴敬新.植物抗旱相关基因研究进展[J].麦类作物学报,2009,29(1)：166-173.
[22]Ralf Stracke, Martin, and Bernd. The R2R3-MYB gene family in Arabidopsis thaliana [J].Curr Opin Plant Biol,2001,4(5):47-56.
[23]Ariadna, Ludovic.B, Zhu, Paul, and Teresa. Molecular characterization of the Arginine decarboxylase gene family in rice [J]. Transgenic Research,2010, DOI 10.1007/s11248-009-9354-0.
[24]Sakihito, Kitajima, and Fumihiko.S. Plant Pathogenesis-Related Proteins: Molecular Mechanisms of Gene Expression and Protein Function [J]. J. Biochem, 1999,125:1-8.
[25]张岗,李依民,张毅,董艳玲,王晓杰,魏国荣,黄丽丽,康振生.条锈菌诱导的小麦病程相关蛋白TaPR10基因的克隆及特征分析[J].中国农业科学,2009,42(1)：110-116.
[26]Charlotta filling. Short-chain dehydrogenase/reductase protein-structure, function and motifs [M]. Karolinska institute stockhlom,2002:1-63.
[27]Sylvia Morais de Sousa, Ma'rio del Giu'dice Paniago, Paulo Arruda, Jose' Andre's Yunes.Sugar levels modulate sorbitol dehydrogenase expression in maize [J] Plant Mol Biol,2008,68:203-213.
[28]贺丽虹,赵淑娟,胡之璧.植物细胞色素P450基因与功能研究进展[J]Pharmaceutical Biotechnology,2008,15(2):142-147.
[29]潘雅姣,王迪,朱苓华,傅彬英,黎志康.水稻双组分系统基因干旱胁迫表达谱分析[J]. ACTA AGRONOMICA SINICA 2009,35(9):1628-1636.
[30]何新建,陈健权,张志刚,张劲松,陈受宜.通过cDNA微阵列鉴定水稻盐胁迫应答基因[J].中国科学C辑,2002,32(6)：488-493.
[31]Finnegan EJ, Peacock., Dennis.A cluster of Arabidopsis genes with a coordinate response to an environmental stimulus [J]. Curr Biol,2004,14(10):911-916.
[32]Yang., He, Yu, Chen, Lei, JiJ. Influence of drought on oxidative stress and flavonoid production in cell suspension culture of Glycyrrhiza inflata Batal [J]. Z Naturforsch C,2007,62(5-6):410-416.
[33]Galle A,Csiszar J,Secenji M,Guoth A,Cseuz L,Tari I,Gyorgyey J, Erdei L. Glutathione transferase activity-and expression patterns during grain filling in flag leaves of wheat genotypes differing in drought tolerance:Response to water deficit [J] Plant Physiol,2009,166(17):1878-1891.
[34]Ayman A. Diab, R. V. Kantety, N. Z. Ozturk, D. Benscher, M. M. Nachit and M. E. Sorrells. Drought-inducible genes and differentially expressed sequence tags associated with components of droughttolerance in durum wheat [J]. Scientific Research and Essay,2008,3 (1):009-026.
[35]Nguyen, C.-L.Ho, J.A.Harikrishna, M.wong, and R.Abdul Rahim. Functional screening for salinity tolerant genes from Acanthus ebracteatus Vahl using Escherichia coli as a host [J]. Trees,2007,21:515-520.
[36]高凤华,张洪亮,王海光,高宏,李自超.应用cDNA-AFLP比较干旱胁迫条件下水稻和旱稻转录本表达谱[J].科学通报,2009,54(16)：2305-2319.
[37]Kaoru T. Yoshida, Makoto Endo. Mikio Nakazono, Hiroo Fukuda, Taku Demura. Tohru Tsuchiya, Masao Watanabe. cDNA microarray analysis of gene expression changes during pollination, pollen-tube elongation, fertilization, and early embryogenesis in rice pistils [J]. Sex Plant Reprod,2005,17:269-275.
[38]Lin., XU., Ni, Chu, Xu., and Xue. Identification of ABA-responsive genes in rice shoots via cDNA macroarray [J]. Cell Research,2003,13:59-68.
[39]Kazuo Shinozaki and Kazuko Yamaguchi-Shinozaki. Gene networks involved in drought stress response and tolerance [J]. Journal of Experimental Botany,2007, 58(2):221-227.
[40]Kizis D., Lumbreras V., and Pags M. Role ofAP2/EREBP transcription factors in gene regulation during abiotic stress [J]. FEBS letters,2001,498(2-3):187-189.
[41]Morinaga T. On the microsporogenesis of the various interspecific hybrids of Oryza [J]. Japan J C-enet,1937,13:245.
[42]Klimyuk, V. I. and J. D. G. Jones. AtDMC1, the Arabidopsis homolog of the yeast DMC1 gene:characterization, transposon-induced allelic variation and meiosis-associated expression [J]. The Plant Journal,1997,11:1-14.
[43]Yang, M., Hu, Y., Lodhi, M., McCombie, W. R. and Ma, H. The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation [J]. Proc. Natl. Acad. Sci. USA,1999,96:11416-11421.
[44]I. siddiqi, G. ganesh, U. grossniklaus and V. subbiah. The dyad gene is required for progression through female meiosis in Arabidopsis [J].2000, Development,127: 197-207.
[45]Magnard JL, Yang. M, Chen.YCS, Leary M, and McCormick.S. The Arabidopsis thaliana gene TARDY ASYNCHRONOUS MEIOSIS(TAM) is required for the normal pace and synchrony of cell division during male meiosis [J]. Plant Physiol,2001, 127:1157-1166.
[46]Azumi Y, Liu D, Zhao D, Li W, Wang G, Hu Y, Ma H. Homolog interaction during meiotic prophase Ⅰ in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein [J]. EMBO J,2002,21:3081-3095.
[47]Chen., Adam Marcus, Li., Hu, Jean-Philippe Vielle Calzada, Ueli Grossniklaus, Richard J. Cyr, and Ma. The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis [J].Development,2002,129:2401-2409.
[48]Yang, X.H., Makaro., C.A., Ma, H. The Arabidopsis male meiocyte death1 gene encodes a PHD-finger protein that is required for male meiosis [J].Plant Cell,2003,15: 1281-1295.
[49]James D. Higgins, Susan J. Armstrong, F. Christopher H. Franklin, and Gareth H. Jones. The Arabidopsis MutS homolog AtMSH4functions at an early step in recombination:evidence for two classes of recombination in Arabidopsis [J]. Genes & Dev,2004,18:2557-2570.
[50]Li.,Chen., Ullrich Markmann-Mulisch, LjudmillaTimofejeva, Elmon Schmelzer, Hong Ma, and Bernd Reiss. The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis [J]. Proc. Natl. Acad. Sci. USA,2004, 101:10596-10601.
[51]Bleuyard JY, White CI. The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis [J]. EMBO J,2004,23(2):439-49.
[52]Ding Z, Wang T, Chong K, Bai S. Isolation and characterization of OsDMCl, the rice homologue of the yeast DMC1 gene essential for meiosis [J]. Sex Plant Reprod,2001,13:285-288.