Gene, protein, and network of male sterility in rice

Frontiers in Plant Science

Volumn 4, Issue APR, 2013, Pages

  Wang, Kun ^a,b   Peng, Xiaojue ^c   Ji, Yanxiao ^a   Yang, Pingfang ^b   Zhu, Yingguo ^a   Li, Shaoqing ^a  

^a WUHAN UNIVERSITY   (China)

^b Wuhan Institute of Botany Chinese Academy of Sciences   (China)

^c NANCHANG UNIVERSITY   (China)

Author keywords

Gene; Male sterility; Molecular mechanism; Protein; Rice

Indexed keywords

EID: 84896399462     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00092     Document Type: Review

References (85)

1. Akagi, H., Nakamura, A., Yokozeki-Misono, Y., Inagaki, A., Takahashi, H., Mori, K., et al. (2004). Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein. Theor. Appl. Genet. 108, 1449-1457.
2. Akagi, H., Sakamoto, M., Shinjyo, C., Shimada, H., and Fujimura, T. (1994). A unique sequence located downstream from the rice mitochondrial atp6 may cause male sterility. Curr. Genet. 25, 52-58.
3. Aya, K., Ueguchi-Tanaka, M., Kondo, M., Hamada, K., Yano, K., Nishimura, M., et al. (2009). Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21, 1453-1472.
4. Becker, J. D., Boavida, L. C., Carneiro, J., Haury, M., and Feijo, J. A. (2003). Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol. 133, 713-725.
5. Bentolila, S., and Stefanov, S. (2012). A reevaluation of rice mitochondrial evolution based on the complete sequence of male-fertile and male-sterile mitochondrial genomes. Plant Physiol. 158, 996-1017.
6. Bergman, P., Edqvist, J., Farbos, I., and Glimelius, K. (2000). Male-sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio. Plant Mol. Biol. 42, 531-544.
7. Borg, M., and Twell, D. (2010). Life after meiosis: patterning the angiosperm male gametophyte. Biochem. Soc. Trans. 38, 577-582.
8. Borges, F., Gomes, G., Gardner, R., Moreno, N., McCormick, S., Feijo, J. A., et al. (2008). Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol. 148, 1168-1181.
9. Chen, R., Zhao, X., Shao, Z., Wei, Z., Wang, Y., Zhu, L., et al. (2007). Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19, 847-861.
10. Chen, Y., Chen, T., Shen, S., Zheng, M., Guo, Y., Lin, J., et al. (2006). Differential display proteomic analysis of Picea meyeri pollen germination and pollen-tube growth after inhibition of actin polymerization by latrunculin B. Plant J. 47, 174-195.
11. Dai, S., Chen, T., Chong, K., Xue, Y., Liu, S., and Wang, T. (2007). Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen. Mol. Cell. Proteomics 6, 207-230.
12. Dai, S., Li, L., Chen, T., Chong, K., Xue, Y., and Wang, T. (2006). Proteomic analyses of Oryza sativa mature pollen reveal novel proteins associated with pollen germination and tube growth. Proteomics 6, 2504-2529.
13. Daniell, H., Khan, M. S., and Allison, L. (2002). Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology. Trends Plant Sci. 7, 84-91.
14. Das, S., Sen, S., Chakraborty, A., Chakraborti, P., Maiti, M. K., Basu, A., et al. (2010). An unedited 1.1 kb mitochondrial orfB gene transcript in the wild abortive cytoplasmic male sterility (WA-CMS) system of Oryza sativa L. subsp. indica. BMC Plant Biol. 10:39. doi: 10.1186/1471-2229-10-39
15. Ding, J., Lu, Q., Ouyang, Y., Mao, H., Zhang, P., Yao, J., et al. (2012a). A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc. Natl. Acad. Sci. U.S.A. 109, 2654-2659.
16. Ding, J., Shen, J., Mao, H., Xie, W., Li, X., and Zhang, Q. (2012b). RNA-directed DNA methylation is involved in regulating photoperiod-sensitive male sterility in rice. Mol. Plant 5, 1210-1216.
17. Engelke, T., Hirsche, J., and Roitsch, T. (2010). Anther-specific carbohydrate supply and restoration of metabolically engineered male sterility. J. Exp. Bot. 61, 2693-2706.
18. Fang, G., Munera, D., Friedman, D. I., Mandlik, A., Chao, M. C., Banerjee, O., et al. (2012). Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing. Nat. Biotechnol. 30, 1232-1239.
19. Goldberg, R. B., Beals, T. P., and Sanders, P. M. (1993). Anther development: basic principles and practical applications. Plant Cell 5, 1217-1229.
20. Haerizadeh, F., Wong, C. E., Bhalla, P. L., Gresshoff, P. M., and Singh, M. B. (2009). Genomic expression profiling of mature soybean (Glycine max) pollen. BMC Plant Biol. 9:25. doi: 10.1186/1471-2229-9-25
21. Hafidh, S., Breznenova, K., Ruzicka, P., Fecikova, J., Capkova, V., and Honys, D. (2012). Comprehensive analysis of tobacco pollen transcriptome unveils common pathways in polar cell expansion and underlying heterochronic shift during spermatogenesis. BMC Plant Biol. 12:24. doi: 10.1186/1471-2229-12-24
22. Han, B., Chen, S., Dai, S., Yang, N., and Wang, T. (2010). Isobaric tags for relative and absolute quantification-based comparative proteomics reveals the features of plasma membrane-associated proteomes of pollen grains and pollen tubes from Lilium davidii. J. Integr. Plant Biol. 52, 1043-1058.
23. Hanson, M. R., and Bentolila, S. (2004). Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16(Suppl. 1), S154-S169.
24. He, H., and Yuan, S. (1989). Analyses of plant characterin Hubei photoperiodsensitive genie male-sterile rice(HPGMR)under different light and temperature conditions. Hybrid Rice 5, 42-44.
25. Honys, D., and Twell, D. (2004). Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5, R85.
26. Hord, C. L., Chen, C., Deyoung, B. J., Clark, S. E., and Ma, H. (2006). The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18, 1667-1680.
27. Hu, J., Wang, K., Huang, W., Liu, G., Gao, Y., Wang, J., et al. (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.
28. Hu, L., Liang, W., Yin, C., Cui, X., Zong, J., Wang, X., et al. (2011). Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23, 515-533.
29. Iwabuchi, M., Kyozuka, J., and Shimamoto, K. (1993). Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male sterile rice. EMBO J. 12, 1437-1446.
30. Johnson, M. A., and Bender, J. (2009). Reprogramming the epigenome during germline and seed development. Genome Biol. 10, 232.
31. Jung, K. H., Han, M. J., Lee, D. Y., Lee, Y. S., Schreiber, L., Franke, R., et al. (2006). Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18, 3015-3032.
32. Jung, K. H., Han, M. J., Lee, Y. S., Kim, Y. W., Hwang, I., Kim, M. J., et al. (2005). Rice undeveloped tapetum1 is a major regulator of early tapetum development. Plant Cell 17, 2705-2722.
33. Kazama, T., Nakamura, T., Watanabe, M., Sugita, M., and Toriyama, K. (2008). Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J. 55, 619-628.
34. Kazama, T., and Toriyama, K. (2003). A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett. 544, 99-102.
35. Komori, T., Ohta, S., Murai, N., Takakura, Y., Kuraya, Y., Suzuki, S., et al. (2004). Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J. 37, 315-325.
36. Kubo, T., Yoshimura, A., and Kurata, N. (2011). Hybrid male sterility in rice is due to epistatic interactions with a pollen killer locus. Genetics 189, 1083-1092.
37. Lee, J. Y., and Lee, D. H. (2003). Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiol. 132, 517-529.
38. Levin, Y., and Bahn, S. (2010). Quantification of proteins by label-free LC-MS/MS. Methods Mol. Biol. 658, 217-231.
39. Li, H., Pinot, F., Sauveplane, V., Werck-Reichhart, D., Diehl, P., Schreiber, L., et al. (2010). 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.
40. Li, H., Yuan, Z., Vizcay-Barrena, G., Yang, C., Liang, W., Zong, J., et al. (2011a). PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol. 156, 615-630.
41. Li, X., Gao, X., Wei, Y., Deng, L., Ouyang, Y., Chen, G., et al. (2011b). Rice APOPTOSISINHIBITOR5coupledwithtwoDEAD-boxadenosine5′-triphosphate-dependent RNA helicases regulates tapetum degeneration. Plant Cell 23, 1416-1434.
42. Li, N., Zhang, D. S., Liu, H. S., Yin, C. S., Li, X. X., Liang, W. Q., et al. (2006). The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999-3014.
43. Li, S., Wan, C., Kong, J., Zhang, Z., Li, Y., and Zhu, Y. (2004). Programmed cell death during microsporogenesis in a Honglian CMS line of rice is correlated with oxidative stress in mitochondria. Funct. Plant Biol. 31, 369-376.
44. Lin, S., and Yuan, L. (1980). "Hybrid rice breeding in China, " in Innovative Approaches to Rice Breeding, eds G. Argosino, V. S. Durvasula, and W. H. Smith (Manila: International Rice Research Institute), 35-51.
45. Ling, D. H., Tao, L. Z., Ma, Z. R., Zhang, S. P., and Datta, S. K. (1998). Engineered male sterile transgenic plants of rice (Oryza sativa L.) with PS1-barnase gene transformation by particle bombardment. J. Genet. Genomics 25, 433-442.
46. Linke, B., and Borner, T. (2005). Mitochondrial effects on flower and pollen development. Mitochondrion 5, 389-402.
47. Liu, G., Tian, H., Huang, Y. Q., Hu, J., Ji, Y. X., Li, S. Q., et al. (2012). Alterations of mitochondrial protein assembly and jasmonic acid biosynthesis pathway in Honglian (HL)-type cytoplasmic male sterility rice. J. Biol. Chem. 287, 40051-40060.
48. Liu, X. Q., Xu, X., Tan, Y. P., Li, S. Q., Hu, J., Huang, J. Y., et al. (2004). Inheritance and molecular mapping of two fertility-restoring loci for Honglian gametophytic cytoplasmic male sterility in rice (Oryza sativa L.). Mol. Genet. Genomics 271, 586-594.
49. Lopez-Casado, G., Covey, P. A., Bedinger, P. A., Mueller, L. A., Thannhauser, T. W., Zhang, S., et al. (2012). Enabling proteomic studies with RNA-Seq: the proteome of tomato pollen as a test case. Proteomics 12, 761-774.
50. Lu, C., Zou, J., Hu, N., and Yao, K. (2007). Plant temperature for sterile alteration of a temperature-sensitive genic male sterile rice, Pei'ai 64S. Sci. Agric. Sin. 6, 1283-1290.
51. Luo, X., Qiu, Z., and Li, R. (1992). Pei'ai 64S, a dual purpose sterile line whose sterility is induced by low critical temperature. Hybrid Rice 1, 27-29.
52. Mayank, P., Grossman, J., Wuest, S., Boisson-Dernier, A., Roschitzki, B., Nanni, P., et al. (2012). Characterization of the phosphoproteome of mature Arabidopsis pollen. Plant J. 72, 89-101.
53. Mayfield, J. A., Fiebig, A., Johnstone, S. E., and Preuss, D. (2001). Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292, 2482-2485.
54. Nonomura, K., Miyoshi, K., Eiguchi, M., Suzuki, T., Miyao, A., Hirochika, H., et al. (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.
55. Nonomura, K.-I., Nakano, M., Fukuda, T., Eiguchi, M., Miyao, A., Hirochika, H., et al. (2004). The novel gene homologous pairing aberration in rice meiosis1 of rice encodes a putative coiled-coil proteinrequired for homologous chromosome pairing in Meiosis. Plant Cell 16, 1008-1020.
56. Peng, X., Wang, K., Hu, C., Zhu, Y., Wang, T., Yang, J., et al. (2010). The mitochondrial gene orfH79 plays a critical role in impairing both male gametophyte development and root growth in CMS-Honglian rice. BMC Plant Biol. 10:125. doi: 10.1186/1471-2229-10-125
57. Pertl, H., Schulze, W. X., and Obermeyer, G. (2009). The pollen organelle membrane proteome reveals highly spatial-temporal dynamics during germination and tube growth of lily pollen. J. Proteome Res. 8, 5142-5152.
58. Pina, C., Pinto, F., Feijo, J. A., and Becker, J. D. (2005). Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol. 138, 744-756.
59. Ruiz, O. N., and Daniell, H. (2005). Engineering cytoplasmic male sterility via the chloroplast genome by expression of β-ketothiolase. Plant Physiol. 138, 1232-1246.
60. Sheoran, I. S., Ross, A. R., Olson, D. J., and Sawhney, V. K. (2007). Proteomic analysis of tomato (Lycopersicon esculentum) pollen. J. Exp. Bot. 58, 3525-3535.
61. Shi, M. (1985). The discovery and study of the photosensitive recessive male-sterile rice (Oryza sativa L. subsp. japonica). Sci. Agric. Sin. 2, 44-48.
62. Shi, M., and Deng, J. (1986). The discovery, determination and utilization of the Hubei photosensitve genic male-sterile rice (Oryza sativa subsp. japonica). Acta Agric. Sin. 13, 107-112.
63. Shinjyo, C. (1969). Cytoplasmic genetic male sterility in cultivated rice, Oryza sativa L. II. The inheritance of male sterility. Jpn. J. Genet. 44, 149-156.
64. Slotkin, R. K., Vaughn, M., Borges, F., Tanurdzic, M., Becker, J. D., Feijo, J. A., et al. (2009). Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461-472.
65. Stuber, C. W. (1994). Heterosis and hybrid rice breeding. Plant Breed. 12, 227-251.
66. Sun, Q., Hu, C., Hu, J., Li, S., and Zhu, Y. (2009). Quantitative proteomic analysis of CMS-related changes in Honglian CMS rice anther. Protein J. 28, 341-348.
67. Tang, X., Zhang, Z.-Y., Zhang, W.-J., Zhao, X.-M., Li, X., Zhang, D., et al. (2010). Global gene profiling of laser-captured pollen mother cells indicates molecular pathways and gene subfamilies involved in rice meiosis. Plant Physiol. 154, 1855-1870.
68. Teixeira, R. T., Knorpp, C., and Glimelius, K. (2005). Modified sucrose, starch, and ATP levels in two alloplasmic male-sterile lines of B. napus. J. Exp. Bot. 56, 1245-1253.
69. Twell, D. (2011). Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod. 24, 149-160.
70. Wan, C., Li, S., Wen, L., Kong, J., Wang, K., and Zhu, Y. (2007). Damage of oxidative stress on mitochondria during microspores development in Honglian CMS line of rice. Plant Cell Rep. 26, 373-382.
71. Wang, Y., Wang, Y. F., and Zhang, D. B. (2006a). Identification of the rice (Oryza sativa L.) mutant msp1-4 and expression analysis of its UDT1 and GAMYB genes. Zhi Wu Sheng Li Yu Fen Zi Sheng Wu Xue Xue Bao 32, 527-534.
72. Wang, Z., Zou, Y., Li, X., Zhang, Q., Chen, L., Wu, H., et al. (2006b). Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18, 676-687.
73. Wei, L. Q., Xu, W. Y., Deng, Z. Y., Su, Z., Xue, Y., and Wang, T. (2010). Genome-scale analysis and comparison of gene expression profiles in developing and germinated pollen in Oryza sativa. BMC Genomics 11:338. doi: 10.1186/1471-2164-11-338
74. Wen, L., Liu, G., Li, S., Wan, C., Tao, J., Xu, K., et al. (2007). Proteomic analysis of anthers from Honglian cytoplasmic male sterility line rice and its corresponding maintainer and hybrid. Bot. Stud. 48, 293-309.
75. Wilson, Z. A., and Zhang, D.-B. (2009). From Arabidopsis to rice: pathways in pollen development. J. Exp. Bot. 60, 1479-1492.
76. Xu, M., Zhou, G., and Chen, L. (1999). Response of fertility of Pei'ai 64S to temperature and photoperiod in rice. Acta Agric. Sin. 25, 772-776.
77. Yamaguchi, T., Lee, D. Y., Miyao, A., Hirochika, H., An, G., and Hirano, H. Y. (2006). Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa. Plant Cell 18, 15-28.
78. Yi, P., Wang, L., Sun, Q., and Zhu, Y. (2002). Discovery of mitochondrial Chimeric gene associated with male sterility of HL-rice. Chinese Sci. Bull. 47, 744-747.
79. Young, E., and Hanson, M. (1987). A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 50, 41-49.
80. Yuan, L. (1994). Purifcation and production of foundation seed of rice PGMS and TGMS lines. Hybird Rice 6, 1-3.
81. Zhang, D., Liang, W., Yin, C., Zong, J., Gu, F., and Zhang, D. (2010a). OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol. 154, 149-162.
82. Zhang, J., Zhang, W., Yen, Y., Long, H., Deng, G., Pan, Z., et al. (2010b). A novel herbicide-inducible male sterility system. J. Sci. Food Agric. 90, 2526-2530.
83. Zhang, D., Luo, X., and Zhu, L. (2011). Cytological analysis and genetic control of rice anther development. J. Genet. Genomics 38, 379-390.
84. Zhao, X., De Palma, J., Oane, R., Gamuyao, R., Luo, M., Chaudhury, A., et al. (2008). OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J. 54, 375-387.
85. Zhou, H., Liu, Q., Li, J., Jiang, D., Zhou, L., Wu, P., et al. (2012). Photoperiod-and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res. 22, 649-660.