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Reproductive Isolation Between indica and japonica Subspecies

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Genetics and Genomics of Rice

Part of the book series: Plant Genetics and Genomics: Crops and Models ((PGG,volume 5))

Abstract

The indica and japonica subspecies of cultivated rice (Oryza sativa L.) have strong genetic differentiations, which result in divergence in phenotypes and adaptations. Hybrid sterility between these two subspecies is frequently observed, which is a major form of postzygotic reproductive isolation in plants. Findings from molecular characterization of genes controlling indica–japonica hybrid sterility can summarize the genetic and molecular mechanism of reproductive barriers in rice. The understandings of the evolutionary process underlying reproductive isolation are illustrated based on the supporting evidences. The approaches for identifying hybrid incompatibility genes are also discussed in this chapter.

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References

  1. Oka H (1988) Origin of cultivated rice. Japan Scientific Societies Press, Tokyo, pp 181–209

    Google Scholar 

  2. McCouch SR, Kovach MJ, Sweeney MT (2007) New insights into the history of rice domestication. Trends Genet 23:578

    Article  PubMed  Google Scholar 

  3. Sang T, Ge S (2007) Genetics and phylogenetics of rice domestication. Curr Opin Genet Dev 17:533

    Article  PubMed  CAS  Google Scholar 

  4. Sweeney M, McCouch S (2007) The complex history of the domestication of rice. Ann Bot 100:951

    Article  PubMed  Google Scholar 

  5. Liu L, Lee GA, Jiang LP, Zhang JZ (2007) Evidence for the early beginning (c. 9000 cal. BP) of rice domestication in China: a response. Holocene 17:1059

    Article  Google Scholar 

  6. Higham C, Lu TLD (1998) The origins and dispersal of rice cultivation. Antiquity 72:867

    Google Scholar 

  7. Fuller DQ et al (2010) Consilience of genetics and archaeobotany in the entangled history of rice. Archaeol Anthropol Sci 2:115

    Article  Google Scholar 

  8. Ting Y (1949) Chronological studies of the cultivation and the distribution of rice varieties, Keng and Sen (in Chinese). Agr Bull Col Agr Sun Yatsen Univ 6:1

    Google Scholar 

  9. Ting Y (1949) A preliminary report on the cultivation and distribution of hsien and keng rices in ancient China and the classification of current cultivars (in Chinese). Memoir Coll Agr Sun Yatsen Univ 6:1

    Google Scholar 

  10. Kato S, Kosaka H, Hara S (1928) On the affinity of rice varieties as shown by fertility of hybrid plants. Bull Sci Fac Agric Kyushu Univ 3:132

    Google Scholar 

  11. Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25

    Article  PubMed  CAS  Google Scholar 

  12. Oka H (1988) Origin of cultivated rice. Japan Scientific Societies Press, Tokyo, pp 1–254

    Google Scholar 

  13. Londo JP, Chiang YC, Hung KH, Chiang TY, Schaal BA (2006) Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc Natl Acad Sci U S A 103:9578

    Article  PubMed  CAS  Google Scholar 

  14. Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631

    Article  PubMed  CAS  Google Scholar 

  15. Widmer A, Lexer C, Cozzolino S (2009) Evolution of reproductive isolation in plants. Heredity 102:31

    Article  PubMed  CAS  Google Scholar 

  16. Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8:382

    Article  PubMed  CAS  Google Scholar 

  17. Liu KD, Zhou ZQ, Xu CG, Zhang Q, Saghai Maroof MA (1996) An analysis of hybrid sterility in rice using a diallel cross of 21 parents involving indica, japonica and wide compatibility varieties. Euphytica 90:275

    Article  Google Scholar 

  18. Zhang Q et al (1997) Molecular marker diversity and hybrid sterility in indica-japonica rice crosses. Theor Appl Genet 95:112

    Article  CAS  Google Scholar 

  19. Zhang GQ, Lu YG (1996) In: Khush G (ed) Rice genetics III. Proceedings of the third international rice genetics symposium. International Rice Research Institute, Manila, Philippines. pp. 418–422

    Google Scholar 

  20. Zhang GQ, Lu YG (1993) Genetic studies on the hybrid sterility in cultivated rice (Oryza sativa). II (in Chinese with English abstract). Genic mode for F1 pollen sterility. Acta Genet Sinica 20:222

    Google Scholar 

  21. Jing W et al (2007) Two novel loci for pollen sterility in hybrids between the weedy strain Ludao and the Japonica variety Akihikari of rice (Oryza sativa L.). Theor Appl Genet 114:915

    Article  PubMed  Google Scholar 

  22. Zhang ZS, Lu YG, Liu XD, Feng JH, Zhang GQ (2006) Cytological mechanism of pollen abortion resulting from allelic interaction of F1 pollen sterility locus in rice (Oryza sativa L.). Genetica 127:295

    Article  PubMed  CAS  Google Scholar 

  23. Song X, Qiu SQ, Xu CG, Li XH, Zhang Q (2005) Genetic dissection of embryo sac fertility, pollen fertility, and their contributions to spikelet fertility of intersubspecific hybrids in rice. Theor Appl Genet 110:205

    Article  PubMed  Google Scholar 

  24. Zhao ZG et al (2007) Fine mapping of S31, a gene responsible for hybrid embryo-sac abortion in rice (Oryza sativa L.). Planta 226:1087

    Article  PubMed  CAS  Google Scholar 

  25. Liu HY, Xu CG, Zhang Q (2004) Male and female gamete abortions, and reduced affinity between the uniting gametes as the causes for sterility in an indica/japonica hybrid in rice. Sex Plant Reprod 17:55

    Article  Google Scholar 

  26. Morinaga T, Kuriyama H (1958) Intermediate type of rice in the subcontinent of India and Java. Jpn J Breed 7:253

    Google Scholar 

  27. Ikehashi H, Araki H (1986) Genetics of F1 sterility in remote crosses of rice. In: International Rice Research Institute (ed) Rice genetics. Philippines International Rice Research Institute, Manila, pp 119–130

    Google Scholar 

  28. Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A 101:12404

    Article  PubMed  CAS  Google Scholar 

  29. Vitte C, Ishii T, Lamy F, Brar D, Panaud O (2004) Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L.). Mol Gen Genomics 272:504

    Article  CAS  Google Scholar 

  30. Zhu Q, Ge S (2005) Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytol 167:249

    Article  PubMed  CAS  Google Scholar 

  31. Chang TT (1976) Origin, evolution, cultivation, dissemination, and Asian and African rice. Euphytica 25:425

    Article  Google Scholar 

  32. Gao LZ, Innan H (2008) Nonindependent domestication of the two rice subspecies, Oryza sativa ssp. indica and ssp. japonica, demonstrated by multilocus microsatellites. Genetics 179:965

    Article  PubMed  CAS  Google Scholar 

  33. Molina J et al (2011) Molecular evidence for a single evolutionary origin of domesticated rice. Proc Natl Acad Sci U S A 108:8351

    Article  PubMed  CAS  Google Scholar 

  34. Li C, Zhou A, Sang T (2006) Rice domestication by reducing shattering. Science 311:1936

    Article  PubMed  CAS  Google Scholar 

  35. Tan L et al (2008) Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet 40:1360

    Article  PubMed  CAS  Google Scholar 

  36. Second G (1982) Origin of the genetic diversity of cultivated rice: study of the polymorphism scored at 40 isozyme loci. Jpn J Genet 57:25

    Article  Google Scholar 

  37. Bautista NS, Solis R, Kamijima O, Ishii T (2001) RAPD, RFLP and SSLP analyses of phylogenetic relationships between cultivated and wild species of rice. Genes Genet Syst 76:71

    Article  PubMed  CAS  Google Scholar 

  38. Cheng C et al (2003) Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs. Mol Biol Evol 20:67

    Article  PubMed  CAS  Google Scholar 

  39. Kovach MJ, Sweeney MT, McCouch SR (2007) New insights into the history of rice domestication. Trends Genet 23:578

    Article  PubMed  CAS  Google Scholar 

  40. Ge S, Sang T (2011) Inappropriate model rejects independent domestications of indica and japonica rice. Proc Natl Acad Sci U S A 108:E755, author reply E756 (2011)

    Article  PubMed  CAS  Google Scholar 

  41. Caicedo AL et al (2007) Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3:1745

    Article  PubMed  CAS  Google Scholar 

  42. Wang Z, Second G, Tanksley S (1992) Polymorphism and phylogenetic relationship among species in the genus Oryza as determined by analysis of nuclear RFLPs. Theor Appl Genet 113:885

    Google Scholar 

  43. Tang T et al (2006) Genomic variation in rice: genesis of highly polymorphic linkage blocks during domestication. PLoS Genet 2:e199

    Article  PubMed  Google Scholar 

  44. Rakshit S et al (2007) Large-scale DNA polymorphism study of Oryza sativa and O. rufipogon reveals the origin and divergence of Asian rice. Theor Appl Genet 114:731

    Article  PubMed  CAS  Google Scholar 

  45. Du H, Ouyang Y, Zhang C, Zhang Q (2011) Complex evolution of S5, a major reproductive barrier regulator, in the cultivated rice Oryza sativa and its wild relatives. New Phytol 191:275

    Article  PubMed  CAS  Google Scholar 

  46. Yang J et al (2012) A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337:1336

    Article  PubMed  CAS  Google Scholar 

  47. Huang X et al (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497

    Article  PubMed  CAS  Google Scholar 

  48. Glaszmann JC (1987) Isozymes and classification of Asian rice varieties. Theor Appl Genet 74:21

    Article  CAS  Google Scholar 

  49. Zhang Q, Saghai Maroof MA, Lu TY, Shen BZ (1992) Genetic diversity and differentiation of indica and japonica rice detected by RFLP analysis. Theor Appl Genet 83:495

    Article  Google Scholar 

  50. Yang GP, Saghai Maroof MA, Xu CG, Zhang Q, Biyashev RM (1994) Comparative analysis of microsatellite DNA polymorphism in landraces and cultivars of rice. Mol Gen Genet 245:187

    Article  PubMed  CAS  Google Scholar 

  51. Mackill DJ (1995) Classifying japonica rice cultivars with RAPD markers. Crop Sci 35:889

    Article  CAS  Google Scholar 

  52. Liu KD et al (1996) Extraordinary polymorphic ribosomal DNA in wild and cultivated rice. Genome 39:1109

    Article  PubMed  CAS  Google Scholar 

  53. Nakano M, Yoshimura A, Iwata N (1992) Phylogenetic study of cultivated rice and its wild relatives by RFLP. Rice Genet Newsl 9:132

    Google Scholar 

  54. Han B, Xue Y (2003) Genome-wide intraspecific DNA-sequence variations in rice. Curr Opin Plant Biol 6:134

    Article  PubMed  CAS  Google Scholar 

  55. Feng Q et al (2002) Sequence and analysis of rice chromosome 4. Nature 420:316

    Article  PubMed  CAS  Google Scholar 

  56. Huang X et al (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961

    Article  PubMed  CAS  Google Scholar 

  57. Huang X et al (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39

    Article  Google Scholar 

  58. Xu X et al (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105

    Article  CAS  Google Scholar 

  59. Ouyang Y, Chen J, Ding J, Zhang Q (2009) Advances in the understanding of inter-subspecific hybrid sterility and wide-compatibility in rice. Chin Sci Bull 54:2332

    Article  CAS  Google Scholar 

  60. Chen J et al (2008) A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrids in rice. Proc Natl Acad Sci U S A 105:11436

    Article  PubMed  CAS  Google Scholar 

  61. Wang J, Liu KD, Xu CG, Li XH, Zhang Q (1998) The high level of wide-compatibility of variety ‘Dular’ has a complex genetic basis. Theor Appl Genet 97:407

    Article  CAS  Google Scholar 

  62. Liu A, Zhang Q, Li H (1992) Location of a gene for wide-compatibility in the RFLP linkage map. Rice Genet Newsl 9:134

    Google Scholar 

  63. Yanagihara S et al (1995) Molecular analysis of the inheritance of the S-5 locus, conferring wide compatibility in indica/japonica hybrids of rice (Oryza sativa L.). Theor Appl Genet 90:182

    Article  CAS  Google Scholar 

  64. Wang C, Zhu C, Zhai H, Wan J (2005) Mapping segregation distortion loci and quantitative trait loci for spikelet sterility in rice (Oryza sativa L.). Genet Res 86:97

    Article  PubMed  CAS  Google Scholar 

  65. Liu KD et al (1997) A genome-wide analysis of wide compatibility in rice and the precise location of the S5 locus in the molecular map. Theor Appl Genet 95:809

    Article  CAS  Google Scholar 

  66. Qiu SQ et al (2005) Delimitation of the rice wide compatibility gene S5 n to a 40-kb DNA fragment. Theor Appl Genet 111:1080

    Article  PubMed  CAS  Google Scholar 

  67. Ji Q, Lu J, Chao Q, Gu M, Xu M (2005) Delimiting a rice wide-compatibility gene S5 n to a 50 kb region. Theor Appl Genet 111:1495

    Article  PubMed  CAS  Google Scholar 

  68. Ikehashi H, Araki H (1986) Genetics of F1 sterility in remote crosses of rice. In: Rice genetics: proceedings of the international rice genetics symposium. International Rice Research Institute, Manila, pp 119–130

    Google Scholar 

  69. Fujinaga M, Chernaia MM, Tarasova NI, Mosimann SC, James MN (1995) Crystal structure of human pepsin and its complex with pepstatin. Protein Sci 4:960

    Article  PubMed  CAS  Google Scholar 

  70. Kervinen J, Wlodawer A, Zdanov A (2004) 17. Phytepsin. In: Barrett A, Rawlings N, Woessner J (eds) Handbook of proteolytic enzymes. Academic, Amsterdam, pp 77–84

    Chapter  Google Scholar 

  71. Long Y et al (2008) Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci U S A 105:18871

    Article  PubMed  CAS  Google Scholar 

  72. Mizuta Y, Harushima Y, Kurata N (2010) Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc Natl Acad Sci U S A 107:20417

    Article  PubMed  CAS  Google Scholar 

  73. Yamagata Y et al (2010) Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Proc Natl Acad Sci U S A 107:1494

    Article  PubMed  CAS  Google Scholar 

  74. Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York

    Google Scholar 

  75. Oka HI (1957) Genetic analysis for the sterility of hybrids between distantly related varieties of cultivated rice. J Genet 55:397

    Article  Google Scholar 

  76. Oka HI (1974) Analysis of genes controlling F1 sterility in rice by the use of isogenic lines. Genetics 77:521

    PubMed  CAS  Google Scholar 

  77. Masly JP, Jones CD, Noor MA, Locke J, Orr HA (2006) Gene transposition as a cause of hybrid sterility in Drosophila. Science 313:1448

    Article  PubMed  CAS  Google Scholar 

  78. Lynch M, Force AG (2000) The origin of interspecific genomic incompatibility via gene duplication. Am Nat 156:590

    Article  Google Scholar 

  79. Scannell DR, Byrne KP, Gordon JL, Wong S, Wolfe KH (2006) Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440:341

    Article  PubMed  CAS  Google Scholar 

  80. Bikard D et al (2009) Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323:623

    Article  PubMed  CAS  Google Scholar 

  81. Kitamura E (1962) Genetics studies on sterility observed in hybrids between distantly related varieties of rice, Oryza sativa L. Bull Chugoku Agric Exp Stn Ser A 8:141

    Google Scholar 

  82. Sano Y (1990) The genic nature of gamete eliminator in rice. Genetics 125:183

    PubMed  CAS  Google Scholar 

  83. Sano Y, Chu YE, Oka HI (1979) Genetic studies of speciation in cultivated rice, I. Genic analysis for the F1 sterility between O. sativa L. and O. glaberrima steud. Jpn J Genet 54:121

    Article  Google Scholar 

  84. Koide Y et al (2008) Sex-independent transmission ratio distortion system responsible for reproductive barriers between Asian and African rice species. New Phytol 179:888

    Article  PubMed  CAS  Google Scholar 

  85. Garavito A et al (2010) A genetic model for the female sterility barrier between Asian and African cultivated rice species. Genetics 185:1425

    Article  PubMed  CAS  Google Scholar 

  86. Kubo T, Yoshimura A, Kurata N (2011) Hybrid male sterility in rice is due to epistatic interactions with a pollen killer locus. Genetics 189:1083

    Article  PubMed  Google Scholar 

  87. Ouyang Y, Zhang Q (2013) Understanding reproductive isolation based on the rice model. Annu Rev Plant Biol 64:111–135

    Article  PubMed  CAS  Google Scholar 

  88. Win KT et al (2011) Independent evolution of a new allele of F1 pollen sterility gene S27 encoding mitochondrial ribosomal protein L27 in Oryza nivara. Theor Appl Genet 122:385

    Article  PubMed  CAS  Google Scholar 

  89. Ge S, Sang T, Lu BR, Hong DY (1999) Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proc Natl Acad Sci U S A 96:14400

    Article  PubMed  CAS  Google Scholar 

  90. Zou XH et al (2008) Analysis of 142 genes resolves the rapid diversification of the rice genus. Genome Biol 9:R49

    Article  PubMed  Google Scholar 

  91. Tang L et al (2010) Phylogeny and biogeography of the rice tribe (Oryzeae): evidence from combined analysis of 20 chloroplast fragments. Mol Phylogenet Evol 54:266

    Article  PubMed  CAS  Google Scholar 

  92. Bao Y, Ge S (2008) Historical retrospect and the perplexity on the studies of the Oryza polyploids. Acta Phytotaxonomica Sinica 46:3

    Google Scholar 

  93. Yu H (2011) Huazhong Agriculture University

    Google Scholar 

  94. Harushima Y, Nakagahra M, Yano M, Sasaki T, Kurata N (2001) A genome-wide survey of reproductive barriers in an intraspecific hybrid. Genetics 159:883

    PubMed  CAS  Google Scholar 

  95. Nakazato T, Jung MK, Housworth EA, Rieseberg LH, Gastony GJ (2007) A genomewide study of reproductive barriers between allopatric populations of a homosporous fern, Ceratopteris richardii. Genetics 177:1141

    Article  PubMed  Google Scholar 

  96. Matsubara K et al (2011) Relationship between transmission ratio distortion and genetic divergence in intraspecific rice crosses. Mol Genet Genomics 288(5–6):307–319

    Article  Google Scholar 

  97. Johnson NA, Porter AH (2000) Rapid speciation via parallel, directional selection on regulatory genetic pathways. J Theor Biol 205:527

    Article  PubMed  CAS  Google Scholar 

  98. Maheshwari S, Barbash DA (2011) The genetics of hybrid incompatibilities. Annu Rev Genet 45:331

    Article  PubMed  CAS  Google Scholar 

  99. Ouyang Y, Liu YG, Zhang Q (2010) Hybrid sterility in plant: stories from rice. Curr Opin Plant Biol 13:186

    Article  PubMed  Google Scholar 

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Correspondence to Yidan Ouyang Ph.D. .

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Ouyang, Y. (2013). Reproductive Isolation Between indica and japonica Subspecies. In: Zhang, Q., Wing, R. (eds) Genetics and Genomics of Rice. Plant Genetics and Genomics: Crops and Models, vol 5. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7903-1_21

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