
Molecular Markers and Candidate Genes for Thermo-Sensitive Genic Male Sterile in Rice
Received date: 2018-07-09
Accepted date: 2018-08-24
Online published: 2019-01-25
The discovery of thermo-sensitive genic male sterility (TGMS) has led to development of a simple and highly efficient two-line breeding system. In this study, genetic analysis was conducted using three F2 populations derived from crosses between IR68301S, an indica TGMS rice line, and IR14632 (tropical japonica), Supanburi 91062 (indica) and IR67966-188-2-2-1 (tropical japonica), respectively. Approximately 1:3 ratio between sterile and normal pollen of F2 plants from the three populations revealed that TGMS is controlled by a single recessive gene. Bulked segregant analysis using simple sequence repeat (SSR) and insertion-deletion (InDel) markers were used to identify markers linked to the tms gene. The linkage analysis based on the three populations indicated that the tms locus was located on chromosome 2 covering the same area. Using IR68301S × IR14632 F2 population, the results showed that the tms locus was located between SSR marker RM12676 and InDel marker 2gAP0050058. The genetic distance from the tms gene to these two flanking markers were 1.10 and 0.82 cM, respectively. InDel marker 2gAP004045 located between these two markers showed complete co-segregation with the TGMS phenotype. In addition, InDel marker vf0206114052 showed 2.94 cM linked to the tms gene using F2 populations of IR68301S × Supanburi 91062. These markers are useful tool for developing new TGMS lines by marker-assisted selection. There were ten genes located between the two flanking markers RM12676 and 2gAP0050058. Using quantitative real-time PCR for expression analysis, 7 of the 10 genes showed expression in panicles, and response to temperatures. These genes could be the candidate gene controlling TGMS in IR68301S.
Khlaimongkhon Sudthana, Chakhonkaen Sriprapai, Pitngam Keasinee, Ditthab Khanittha, Sangarwut Numphet, Panyawut Natjaree, Wasinanon Thiwawan, Mongkolsiriwatana Chareerat, Chunwongse Julapark, Muangprom Amorntip . Molecular Markers and Candidate Genes for Thermo-Sensitive Genic Male Sterile in Rice[J]. Rice Science, 2019 , 26(3) : 147 -156 . DOI: 10.1016/j.rsci.2018.08.006
| [1] | Bai B, Wu J, Sheng W T, Zhou B, Zhou L J, Zhuang W, Yao D P, Deng Q Y.2015. Comparative analysis of anther transcriptome profiles of two different rice male sterile lines genotypes under cold stress.Int J Mol Sci, 16(5): 11398-11416. |
| [2] | Borkakati R R, Virmani S S.1996. Genetics of thermosensitive genic male sterility in rice.Euphytica, 88(1): 1-7. |
| [3] | Bruinsma J.2003. World Agriculture: Towards 2015/2030. London, UK: Earthscan. |
| [4] | Cao L Y, Zhan X D.2014. Chinese experiences in breeding three-line, two-line and super hybrid rice. In: Yan W G, Bao J S. Rice: Germplasm, Genetics and Improvement. Intech: 279-308. |
| [5] | Chueasiri C, Chunthong K, Pitnjam K, Chakhonkaen S, Sangarwut N, Sangsawang K, Suksangpanomrung M, Michaelson L V, Napier J A, Muangprom A.2014. Rice ORMDL controls sphingolipid homeostasis affecting fertility resulting from abnormal pollen development.PLoS One, 9(9): e106386. |
| [6] | Chunthong K, Pitnjam K, Chakhonkaen S, Sangarwut N, Panyawut N, Wasinanon T, Ukoskit K, Muangprom A.2017. Differential drought responses in F-box gene expression and grain yield between two rice groups with contrasting drought tolerance.J Plant Growth Regul, 36: 970-982. |
| [7] | Ding J H, Lu Q, Ouyang Y D, Mao H L, Zhang P B, Yao J L, Xu C G, Li X H, Xiao J H, Zhang Q F.2012a. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice.Proc Natl Acad Sci USA, 109(7): 2654-2659. |
| [8] | Ding J H, Shen J Q, Mao H L, Xie W B, Li X H, Zhang Q F.2012b. RNA-directed DNA methylation is involved in regulating photoperiod-sensitive male sterility in rice.Mol Plant, 5(6): 1210-1216. |
| [9] | Dong N V, Subudhi P K, Luong P N, Quang V D, Quy T D, Zheng H G, Wang B, Nguyen H T.2000. Molecular mapping of a rice gene conditioning thermo-sensitive genic male sterility using AFLP, RFLP and SSR techniques.Theor Appl Genet, 100(5): 727-734. |
| [10] | FAO.2018. FAO Statistical Pocketbook 2018: World Food and Agriculture. Rome: FAO. |
| [11] | Hussain A J, Ali J, Siddiq E A, Gupta V S, Reddy U K, Ranjekar P K.2011. Mapping of tms8 gene for temperature-sensitive genic male sterility (TGMS) in rice(Oryza sativa L.). Plant Breeding, 131(1): 42-47. |
| [12] | Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi A K, Khurana J P.2007. F-Box proteins in rice: Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress.Plant Physiol, 143(4): 1467-1483. |
| [13] | Jia J H, Zhang D S, Li C Y, Qu X P, Wang S W, Chamarerk V, Nguyen H T, Wang B Y.2001. Molecular mapping of the reverse thermosensitive genic male-sterile gene (rtms1) in rice. Theor Appl Genet, 103(4): 607-612. |
| [14] | Jiang D G, Lu S, Zhou H, Wu X J, Zhuang C X, Liu Y G, Mei M T.2006. Mapping of the rice (Oryza sativa L.) thermo-sensitive genic male sterile gene tms5 with EST and SSR markers. Chin Sci Bull, 51(4): 417-420. |
| [15] | Jung K H, Han M J, Lee Y S, Kim Y W, Hwang I, Kim M J, Kim Y K, Nahm B H, An G.2005. Rice undeveloped tapetum1 is a major regulator of early tapetum development. Plant Cell, 17(10): 2705-2722. |
| [16] | Jung K H, Han M J, Lee D Y, Lee Y S, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim Y W, Hwang I, An G.2006. Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell, 18(11): 3015-3032. |
| [17] | Lang N T, Subudhi P K, Virmani S S, Brar D S, Khush G S, Li Z, Huang N.1999. Development of PCR-based markers for thermosensitive genetic male sterility gene tms3(t) in rice (Oryza satvai L.). Hereditas, 131(2): 121-127. |
| [18] | Lee D S, Chen L J, Suh H S.2005. Genetic characterization and fine mapping of a novel thermo-sensitive genic male-sterile genetms6 in rice(Oryza sativa L.). Theor Appl Genet, 111(7): 1271-1277. |
| [19] | Li R B, Pandey M P, Sharma P, Ballabh G.2005. Inheritance of thermosensitive genic male sterility in rice (Oryza sativa L.). Curr Sci, 88(11): 1809-1815. |
| [20] | Li N, Zhang D S, Liu H S, Yin C S, Li X X, Liang W Q, Yuan Z, Xu B, Chu H W, Wang J, Wen T Q, Huang H, Luo D, Ma H, Zhang D B.2006. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development.Plant Cell, 18(11): 2999-3014. |
| [21] | Liu N, Shan Y, Wang F P, Xu C G, Peng K M, Li X H, Zhang Q F.2001. Identification of an 85-kb DNA fragment containing pms1, a locus for photoperiod-sensitive genic male sterility in rice. Mol Genet Genom, 266(2): 271-275. |
| [22] | Livak K J, Schmittgen T D.2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) method.Methods, 25(4): 402-408. |
| [23] | Lopez M T, Toojinda T, Vanavichit A, Tragoonrung S.2003. Microsatellite markers flanking the tms2 gene facilitated tropical TGMS rice line development. Crop Sci, 43(6): 2267-2271. |
| [24] | Matthayatthaworn W, Sripichitt P, Phumichai C, Rungmekarat S, Uckarach S, Sreewongchai T.2011. Development of specific simple sequence repeat (SSR) markers for non-pollen type thermo-sensitive genic male sterile gene in rice (Oryza sativa L.). Afr J Biotechnol, 10: 16437-16442. |
| [25] | McCouch S R, Teytelman L, Xu Y, Lobos K B, Clare K, Walton M, Fu B, Maghirang R, Li Z, Xing Y, Zhang Q, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L.2002. Development and mapping of 2240 new SSR markers for rice ( Oryza sativa L.). DNA Res, 9(6): 199-207. |
| [26] | Murray M G, Thompson W F.1980. Rapid isolation of high molecular weight plant DNA.Nucl Acid Res, 8(19): 4321-4325. |
| [27] | Nas T M S, Sanchez D L, Diaz G Q, Mendioro M S, Vermani S S.2005. Pyramiding of thermosensitive genetic male sterility (TGMS) genes and identification of a candidate tms5 gene in rice. Euphytica, 145: 67-75. |
| [28] | Nonomura K I, 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(8): 1728-1739. |
| [29] | Peng H F, Zhang Z F, Wu B, Chen X H, Zhang G Q, Zhang Z M, Wan B H, Lu Y P.2008. Molecular mapping of two reverse photoperiod-sensitive genic male sterility genes (rpms1 and rpms2) in rice(Oryza sativa L.). Theor Appl Genet, 118(1): 77-83. |
| [30] | Peng H F, Chen X H, Lu Y P, Peng Y F, Wan B H, Chen N D, Wu B, Xin S P, Zhang G Q.2010. Fine mapping of a gene for non-pollen type thermosensitive genic male sterility in rice (Oryza sativa L.). Theor Appl Genet, 120(5): 1013-1020. |
| [31] | Pitnjam K, Chakhonkaen S, Toojinda T, Muangprom A.2008. Identification of a deletion in tms2 and development of gene-based markers for selection. Planta, 228(5): 813-822. |
| [32] | Qi Y B, Liu Q L, Zhang L, Mao B Z, Yan D W, Jin Q S, He Z H.2014. Fine mapping and candidate gene analysis of the novel thermo sensitive genic male sterility tms9-1 gene in rice. Theor Appl Genet, 127(5): 1173-1182. |
| [33] | Sharma M, Pandey G K.2016. Expansion and function of repeat domain proteins during stress and development in plants.Front Plant Sci, 6: 1218. |
| [34] | Sheng Z H, Wei X J, Shao G N, Chen M L, Song J, Tang S Q, Luo J, Hu Y C, Hu P S, Chen L Y.2013. Genetic analysis and fine mapping of tms9, a novel thermosensitive genic male-sterile gene in rice(Oryza sativa L.). Plant Breeding, 132(2): 159-164. |
| [35] | Shin S B, Golovkin M, Reddy A S N.2014. A pollen-specific calmodulin-binding protein, NPG1, interacts with putative pectate lyases.Sci Rep, 4: 5263. |
| [36] | Small I D, Peeters N.2000. The PPR motif: A TPR-related motif prevalent in plant organellar proteins.Trends Biochem Sci, 25(2): 45-47. |
| [37] | Subudhi P K, Borkakati R P, Virmani S S, Huang N.1997. Molecular mapping of a thermo-sensitive genetic male-sterility gene in rice using bulked segregant analysis.Genome, 40(2): 188-194. |
| [38] | Thai Rice Exporters Association. 2018. World Rice Production and Ending Stocks.. |
| [39] | USDA. 2016. World Agricultural Production. . |
| [40] | Virmani S S.2003. Advances in hybrid rice research and development in the tropics. In: Virmani S S, Mao C X, Hardy B. Hybrid Rice for Food Security, Poverty Alleviation, and Environmental Protection . Proceedings of the 4th International Symposium on Hybrid Rice, Hanoi, Vietnam. Los Baños,the Philippines: International Rice Research Institute: 7-20. |
| [41] | Wang B Y, Xu W W, Wang J Z, Wu W, Zheng H G, Yang Z Y, Ray J D, Nguyen H T.1995. Tagging and mapping the thermo-sensitive genic male-sterile gene in rice (Oryza sativa) with molecular markers. Theor Appl Genet, 91: 1111-1114. |
| [42] | Wang Y G, Xing Q H, Deng Q Y, Liang F S, Yuan L P, Weng M L, Wang B.2003. Fine mapping of the rice thermo-sensitive genic male-sterile gene tms5. Theor Appl Genet, 107(5): 917-921. |
| [43] | Xu J J, Wang B H, Wu Y H, Du P N, Wang J, Wang M, Yi C D, Gu M H, Liang G H.2011. 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, 122(2): 365-372. |
| [44] | Yamaguchi Y, Ikeda R, Hirasawa H, Minami M, Ujihara A.1997. Linkage analysis of thermo-sensitive genic male sterility gene tms-2 in rice(Oryza sativa L.). Breeding Sci, 47: 371-373. |
| [45] | Yang Q K, Liang C Y, Zhuang W, Li J, Deng H B, Deng Q Y, Wang B.2007. Characterization and identification of the candidate gene of rice thermo-sensitive genic male sterile gene tms5 by mapping. Planta, 225(2): 321-330. |
| [46] | Yang Y J, Ma C, Xu Y J, Wei Q, Imtiaz M, Lan H B, Gao S, Cheng L N, Wang M Y, Fei Z J, Hong B, Gao J P.2014. A zinc finger protein regulates flowering time and abiotic stress tolerance in Chrysanthemum by modulating gibberellin biosynthesis.Plant Cell, 26(5): 2038-2054. |
| [47] | Yang J, Chen X R, Zhu C L, Peng X S, He X P, Fu J R, Ouyang L J, Bian J M, Hu L F, Sun X T, Xu J, He H H.2015. RNA-Seq reveals differentially expressed genes of rice (Oryza sativa) spikelet in response to interacting with nitrogen at meiosis stage. BMC Genom, 16: 959. |
| [48] | Yuan L P.1998. Hybrid rice breeding in China. In: Virmani S S, Siddiq E A, Muralidharan K. Advances in Hybrid Rice Technology. Proceedings of the 3rd International Symposium on Hybrid Rice. Hyderabad, India. Manila, the Philippines: International Rice Research Institute: 27-33. |
| [49] | Zhang Q F, Shen B Z, Dai X K, Mei M H, Saghai Maroof M A, Li Z B.1994. Using bulked extremes and recessive classes to map genes for photoperiod-sensitive genic male sterility in rice.Proc Natl Acad Sci USA, 91(18): 8675-8679. |
| [50] | Zhang Q S, Li Z, Yang J, Li S Q, Yang D C, Zhu Y G.2012. A calmodulin-binding protein from rice is essential to pollen development.J Plant Biol, 55(1): 8-14. |
| [51] | Zhou Y F, Zhang X Y, Xue Q Z.2011. 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, 12(6): 436-447. |
| [52] | Zhou H, Liu Q J, Li J, Jiang D G, Zhou L Y, Wu P, Lu S, Li F, Zhu L Y, Liu Z L, Chen L T, Liu Y G, Zhuang C X.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(4): 649-660. |
| [53] | Zhou H, Zhou M, Yang Y Z, Li J, Zhu L Y, Jiang D G, Dong J F, Liu Q J, Gu L F, Zhou L Y, Feng M J, Qin P, Hu X C, Song C L, Shi J F, Song X W, Ni E D, Wu X J, Deng Q Y, Liu Z L, Chen M S, Liu Y G, Cao X F, Zhuang C X.2014. RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice.Nat Commun, 5: 4884. |
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