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 Research

Volumn 22, Issue 4, 2012, Pages 649-660

  Zhou, Hai ^a   Liu, Qinjian ^a   Li, Jing ^a   Jiang, Dagang ^a   Zhou, Lingyan ^b   Wu, Ping ^a   Lu, Sen ^a   Li, Feng ^a   Zhu, Liya ^b   Liu, Zhenlan ^a   Chen, Letian ^a   Liu, Yao Guang ^a   Zhuang, Chuxiong ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b ZHONGKAI UNIVERSITY OF AGRICULTURE AND ENGINEERING   (China)

Author keywords

noncoding RNA; PGMS; rice; small RNA; TGMS

Indexed keywords

SMALL UNTRANSLATED RNA;

ARTICLE; CONFORMATION; GENE EXPRESSION REGULATION; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOTOPERIODICITY; PHYSIOLOGY; PLANT INFERTILITY; POINT MUTATION; POLLEN; RICE; TEMPERATURE; TRANSGENIC PLANT;

BASE SEQUENCE; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; ORYZA SATIVA; PHOTOPERIOD; PLANT INFERTILITY; PLANTS, GENETICALLY MODIFIED; POINT MUTATION; POLLEN; RNA, SMALL UNTRANSLATED; TEMPERATURE;

JAPONICA; OSA;

EID: 84862777808     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2012.28     Document Type: Article

References (65)

1. Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY. Progress in research and development on hybrid rice: A super-domesticate in China. Ann Bot 2007; 100:959-966.
2. Wang Z, Zou Y, Li X, et al. 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 2006; 18:676-687.
3. Lin SC, Yuan LP. Hybrid rice breeding in China. In: Innovative approaches to rice breeding. Manila, Philippines: International Rice Research Institute, 1980: 35-52.
4. Yuan LP. Purification and production of foundation seed of rice PGMS and TGMS lines. Hybrid Rice 1994; 6:1-3.
5. Yang Q, Liang C, Zhuang W, et al. Characterization and identification of the candidate gene of rice thermo-sensitive genic male sterile gene tms5 by mapping. Planta 2007; 225:321-330.
6. Si HM, Liu WZ, Fu YP, Sun ZX, Hu GC. Current situation and suggestions for development of two-line hybrid rice in china. Chin J Rice Sci 2011; 25:544-552.
7. Shi MS. The discovery and study of the photosensitive recessive male-sterile rice (Oryza sativa L. subsp. japonica). Sci Agric Sin 1985; 2:44-48.
8. Shi MS, Deng JY. The discovery, determination and utilization of the Hubei photosensitve genic male-sterile rice (Oryza sativa subsp. japonica). Acta Agric Sin 1986; 13:107-112.
9. He HH, Yuan SC. Analyses of plant character in Hubei Photoperiodsensitive Genie Male-sterile Rice (HPGMR) under different light and temperature conditions. Hybrid Rice 1989; 5:42-44.
10. Yang SH, Cheng BY, Shen WF, Xia JH. Progress of application and breeding on two-line hybrid rice in China. Hybrid Rice 2009; 24:5-9.
11. Luo XH, Xia ST, Luo S, Lu ZC, Zhang ZG, Wang GY. Breeding of dual purpose genic male sterile lines and their application in two-line super rice. Hybrid Rice 2010; S1:59-63.
12. Luo XH, Qiu ZZ, Li RH. Pei'ai 64S, a dual purpose sterile line whose sterility is induced by low critical temperature. Hybrid Rice 1992; 1:27-29.
13. Lu CG, Zou JS, Hu N, Yao KM. Plant temperature for sterile alteration of a temperature-sensitive genic male sterile rice, Pei'ai64S. Sci Agric Sin 2007; 6:1283-1290.
14. Xu ML, Zhou GQ, Chen LB. Response of fertility of Pei'ai 64S to temperature and photoperiod in rice. Acta Agric Sin 1999; 25:772-776.
15. Zhang Q, Shen BZ, Dai XK, Mei MH, Saghai Maroof MA, Li ZB. Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. Proc Natl Acad Sci USA 1994; 91:8675-8679.
16. Liu N, Shan Y, Wang FP, et al. Identification of an 85-kb DNA fragment containing pms1, a locus for photoperiod-sensitive genic male sterility in rice. Mol Genet Genomics 2001; 266:271-275.
17. Mei M, Chen L, Zhang Z, Li Z, Xu C, Zhang Q. Pms3 is the locus causing the original photoperiod-sensitive male sterility mutation of 'Nongken 58S'. Sci China C Life Sci 1999; 42:316-322.
18. Mei MH, Dai XK, Xu C, Zhang Q. Mapping and genetic analysis of the genes for photoperiod-sensitive genic male sterility in rice using the original mutant Nongken 58S. Crop Sci 1999; 39:1711-1715.
19. Li XH, Lu Q, Wang FL, Xu CG, Zhang QF. Separation of the two-locus inheritance of photoperiod sensitive genic male sterility in rice and precise mapping the the pms3 locus. Euphytica 2001; 119:343-348.
20. Lu Q, Li XH, Guo D, Xu CG, Zhang Q. Localization of pms3, a gene for photoperiod-sensitive genic male sterility, to a 28.4-kb DNA fragment. Mol Genet Genomics 2005; 273:507-511.
21. Peng HF, Zhang ZF, Wu B, et al. Molecular mapping of two reverse photoperiod-sensitive genic male sterility genes (rpms1 and rpms2) in rice (Oryza sativa L.). Theor Appl Genet 2008; 118:77-83.
22. Wang B, Xu WW, Wang JZ, et al. Tagging and mapping the thermo-sensitive genic male-sterile gene in rice (Oryza sativa L.) with molecular markers. Theor Appl Genet 1995; 91:1111-1114.
23. Yamagushi Y, Ikeda R, Hirasawa H, Minami M, Ujihara P. Linkage analysis of the thermo-sensitive genic male sterility gene tms2 in rice (Oryza sativa L.). Breed Sci 1997; 47:371-377.
24. Lopez MT, Toojinda T, Vanavichit A, Tragoonrung S. Microsatellite markers flanking the tms2 gene facilitated tropical TGMS rice line development. Crop Sci 2003; 43:2267-2271.
25. Subudhi PK, Borkakati RP, Virmani SS, Huang N. Molecular mapping of a thermosensitive genetic male sterility gene in rice using bulked segregant analysis. Genome 1997; 40:188-194.
26. Lang NT, Subudhi PK, Virmani SS, et al. Development of PCR-based markers for thermosensitive genetic male sterility gene tms3(t) in rice (Oryza Sativa L.). Hereditas 1999; 131:121-127.
27. Dong NV, Subudhi PK, Luong PN, et al. Molecular mapping of a rice gene conditioning thermosensitive genic male sterility using AFLP, RFLP and SSR techniques. Theor Appl Genet 2000; 100:727-734.
28. Wang YG, Xing QH, Deng QY, et al. Fine mapping of the rice thermo-sensitive genic male-sterile gene tms5. Theor Appl Genet 2003; 107:917-921.
29. Nas TM, Sanchez DL, Diaz GQ, Mendioro MS, Virmani SS. Pyramiding of thermosensitive genetic male sterility (TGMS) genes and identification of a candidate tms5 gene in rice. Euphytica 2005; 145:67-75.
30. Jiang D, Lu S, Zhou H, et al. Mapping of the rice (Oryza sativa L.) thermo-sensitive genic male sterile gene tms5 with EST and SSR markers. Chin Sci Bull 2006; 51:417-420.
31. Peng HF, Chen XH, Lu YP, et al. Fine mapping of a gene for non-pollen type thermosensitive genic male sterility in rice (Oryza sativa L.). Theor Appl Genet 2010; 120:1013-1020.
32. Lee DS, Chen LJ, Suh HS. Genetic characterization and fine mapping of a novel thermo-sensitive genic male-sterile gene tms6 in rice (Oryza sativa L.). Theor Appl Genet 2005; 111:1271-1277.
33. Liu X, Li X, Zhang X, Wang S. Genetic analysis and mapping of a thermosensitive genic male sterility gene, tms6(t), in rice (Oryza sativa L.). Genome 2010; 53:119-124.
34. Xu J, Wang B, Wu Y, et al. Fine mapping and candidate gene analysis of ptgms2-1, the photoperiod-thermo-sensitive genic male sterile gene in rice (Oryza sativa L.). Theor Appl Genet 2011; 122:365-372.
35. Zhou YF, Zhang XY, Xue QZ. Fine mapping and candidate gene prediction of the photoperiod and thermo-sensitive genic male sterile gene pms1(t) in rice. J Zhejiang Univ Sci B 2011; 12:436-447.
36. Jia JH, Zhang DS, Li CY, et al. Molecular mapping of the reverse thermo-sensitive genic male-sterile gene (rtms1) in rice. Theor Appl Genet 2001; 103:607-612.
37. Xie Z, Qi X. Diverse small RNA-directed silencing pathways in plants. Bio Bio Acta 2008; 1779:720-724.
38. Ramachandran V, Chen X. Small RNA metabolism in Arabidopsis. Tren Plant Sci 2008; 13:368-374.
39. Chen X. Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 2009; 25:21-44.
40. Ruiz-Ferrer V, Voinnet O. Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 2009; 60:485-510.
41. Olivier V. Origin, biogenesis, and activity of plant microRNAs. Cell 2009; 136:669-687.
42. Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y. Rice microRNA effector complexes and targets. Plant Cell 2009; 21:3421-3435.
43. Ji L, Liu X, Yan J, et al. ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet 2011; 7:e1001358. doi:10.1371/journal.pgen.1001358
44. Chen X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 2004; 303:2022-2025.
45. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, et al. Widespread translational inhibition by plant miRNAs and siRNAs. Science 2008; 320:1185-1190.
46. Song X, Li P, Zhai J, et al. Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 2012; 69:462-474.
47. Liu B, Li P, Li X, et al. Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol 2005; 139:296-305
48. Liu B, Chen Z, Song X, et al. Oryza sativa Dicer-like4 reveals a key role for small interfering RNA silencing in plant development. Plant Cell 2007; 19:2705-2018.
49. Zhu QH, Spriggs A, Matthew L, et al. A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res 2008; 18:1456-1465.
50. Feng JH, Lu YG, Liu XD, Xu XB. Pollen development and its stages in rice (Oryza sativa L. ). Chinese J Rice Sci 2001; 15:21-28.
51. Zhang D, Luo X, Zhu L. Cytological analysis and genetic control of rice anther development. J Genet Genomics 2011; 38:379-390.
52. Yu YH, Si HM, Hu GC, Fu YP, Sun ZX. Analysis on fertility transformation reaction to photo-thermo treatments of Peiai64S from different sources. Sci Agric Sin 2006; 39:1064-1068.
53. Vaucheret H. Post-transcriptional small RNA pathways in plants: Mechanisms and regulations. Genes Dev 2006; 20:759-771.
54. Liu Z, Bao W, Liang W, Yin J, Zhang D. Identification of gamyb-4 and analysis of the regulatory role of GAMYB in rice anther development. J Integ Plant Biol 2010; 52:670-678.
55. Kaneko M, Inukai Y, Ueguchi-Tanaka M, et al. Loss-of-function mutations of the rice GAMYB gene impair a-Amylase expression in aleurone and flower development. Plant Cell 2004; 16:33-44.
56. Jung KH, Han MJ, Lee YS, et al. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 2005; 17:2705-2722.
57. Li N, Zhang DS, Liu HS, et al. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 2006; 18:2999-3014.
58. Li H, Pinot F, Sauveplane V, et al. Cytochrome P450 family member CYP704B2 catalyzes the ?-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 2010; 22:173-190.
59. Zhang D, Liang W, Yin C, Zong J, Gu F, Zhang D. OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 2010; 154:149-162.
60. Hu L, Liang W, Yin C, et al. Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 2011; 23:515-533.
61. Zhang H, Liang W, Yang X, et al. Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 2010; 22:672-689.
62. Li X, Gao X, Wei Y, et al. Rice APOPTOSIS INHIBITOR5 coupled with two DEAD-Box adenosine 5'-triphosphate-dependent RNA helicases regulates tapetum degeneration. Plant Cell 2011; 23:1416-1434.
63. Nonomuraa K-I, Morohoshia A, Nakanoa M, et al. A germ cell-specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 2007; 19:2583-2594.
64. Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe DC. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 2000; 101:543-553.
65. Li J, Jiang D, Zhou H, et al. Expression of RNA-interference/ antisense transgenes by the cognate promoters of target genes is a better gene-silencing strategy to study gene functions in rice. PLoS ONE 2011; 6:e17444. doi:10.1371/ annotation/6818176e-4f00-4229-a133-a83d0c3b11da