Abstract
Reproductive barriers are important for the maintenance of species identity. We discovered a reproductive barrier via hybrid breakdown among the progeny of a cross between the japonica rice cultivar Koshihikari and the indica rice cultivar Habataki. Genetic analysis indicated that the hybrid breakdown is regulated by the interaction of two recessive genes: hbd2 in Habataki and hbd3 in Koshihikari. Linkage mapping showed that hbd2 is located near the 100 cM region of chromosome 2 in Habataki, whereas hbd3 is located near the 60 cM region of chromosome 11 in Koshihikari. Construction of nearly isogenic lines for hbd2 and Hbd3 (NIL-hbd2 and NIL-Hbd3), as well as a pyramiding line (NIL-hbd2 + Hbd3), confirmed that the hybrid breakdown is induced by the interaction of these two recessive genes. Our results indicate that these genes are novel for the induction of hybrid breakdown in rice.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amemiya A, Akamine H (1963) Biochemical genetic studies on the root growth inhibiting complementary lethal genes on rice plant. Bull Nat Inst Agric Sci Ser D 10:139–226
Ashikari M, Matsuoka M (2006) Identification, isolation and pyramiding of quantitative trait loci for rice breeding. Trends Plant Sci 11:344–350
Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745
Barbash DA, Siino DF, Tarone AM, Roote J (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci USA 100:5302–5307
Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA (2006) Two Dobzhansky–Muller genes interact to cause hybrid lethality in Drosophila. Science 314:1292–1295
Chen X, Temnykh S, Xu Y, Cho YG, McCouch SR (1997) Development of a microsatellite framework map providing genome-wide coverage in rice (Oryza sativa L.). Theor Appl Genet 95:553–567
Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York
Fukuoka S, Namai H, Okuno K (1998) RFLP mapping of the genes controlling hybrid breakdown in rice. Theor Appl Genet 97:446–449
Fukuoka S, Newingham MCV, Ishtaq M, Nagamine T, Kawase M, Okuno K (2005) Identification and mapping of two new loci for hybrid breakdown in cultivated rice. Rice Genet Newsl 22:29
Guyot R, Keller B (2004) Ancestral genome duplication in rice. Genome 47:610–614
Jennings PR (1966) Evaluation of partial sterility in indica × japonica rice hybrids. IRRI Tech Bull 5:1–63
Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4:403–410
Kubo T, Yoshimura A (2002) Genetic basis of hybrid breakdown in a japonica/indica cross of rice, Oryza sativa L. Theor Appl Genet 105:906–911
Li Z, Pinson SRM, Paterson AH, Park WD, Stancel JW (1997) Genetics of hybrid sterility and hybrid breakdown in an intersubspecific rice (Oryza sativa L.) population. Genetics 145:1139–1148
Mayr E. (1942) Systematics and the origin of species. Columbia University Press, New York
McCouch SR, Teytelman L, Xu Y, Lobos KB, 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 9:199–207
Muller HJ (1940) Bearing of the Drosophila work on systematics. In: Huxley JS (ed) The new systematics. Clarendon Press, Oxford, pp 185–268
Oka HI (1957) Phylogenetic differentiation of cultivated rice. XV. Complementary lethal genes in rice. Jpn J Genet 32:83–87
Oka HI (1958) Intervarietal variation and classification of cultivated rice. Indian J Genet Plant Breed 18:79–89
Oka HI (1974) Analysis of genes controlling F1 sterility in rice by the use of isogenic lines. Genetics 77:521–534
Oka HI (1978) Phylogenetic differentiation of cultivated rice. XXI. The sporophytic pollen sterility: its genetic basis and interval relationship as shown by F2 sterility. Jpn J Genet 53:397–410
Oka HI, Doida Y (1962) Phylogenetic differentiation of cultivated rice. XX. Analysis of the genetic basis of hybrid breakdown in rice. Jpn J Genet 37:24–35
Okuno K (1986) Geographical distribution of complementary genes controlling hybrid breakdown in cultivated rice. Jpn J Breed 36(Suppl 1):372–373
Presgraves DC, Balagopalan L, Abmayr SM, Orr HA (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423:715–719
Sato YI, Morishima H (1987) Distribution of complementary genes causing F1 weakness in Asian native cultivars and its wild relatives. II. Distribution of Hwc-1 and Hwc-2 in native cultivars and wild relatives in Southeast Asia. Euphytica 36:425–431
Sato YI, Morishima H (1988) Distribution of the genes causing F2 chlorosis in rice cultivars of the indica and japonica types. Theor Appl Genet 75:723–724
Scannell DR, Byrne KP, Gordon JL, Wong S, Wolfe KH (2006) Multiple rounds of speciation associated with reciprocal gene loss in polyploidy yeasts. Nature 440:341–345
Smith JM (1989) Macroevolution. In: Smith JM (ed) Evolutionary genetics. Oxford University Press, Oxford pp 272–304
Stebbins GL Jr (1950) Isolation and the origin of species. In: Stebbins GL Jr (ed) Variation and evolution in plants. Columbia University Press, New York, pp 189–250
Ting CT, Tsaur SC, Wu ML, Wu CI (1998) A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282:1501–1504
Ware DH, Jaiswal P, Ni J, Yap IV, Pan X, Clark KY, Teytelman L, Schmidt SC, Zhao W, Chang K, Cartinhour S, Stein LD, McCouch SR (2002) Gramene, a tool for grass genomics. Plant Physiol 130:1606–1613
Wittbrodt J, Adam D, Malitschek B, Maueler W, Raulf F, Telling A, Robertson SM, Schartl M (1989) Novel putative receptor tyrosine kinase encoded by the melanoma-inducing Tu locus in Xiphophorus. Nature 341:415–421
Wu P, Zhang G, Huang N, Ladha JK (1995) Non-allelic interaction conditioning spikelet sterility in an F2 population of indica/japonica cross in rice. Theor Appl Genet 91:825–829
Yano M (2001) Genetic and molecular dissection of naturally occurring variation. Curr Opin Plant Biol 4:130–135
Yano M, Sasaki T (1997) Genetic and molecular dissection of quantitative traits in rice. Plant Mol Biol 35:145–153
Yokoo M (1984) Female sterility in an indica–japonica cross of rice. Jpn J Breed 34:219–227
Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C, Zhang J, Zhang Y, Li R, Xu Z, Li S, Li X, Zheng H, Cong L, Lin L, Yin J, Geng J, Li G, Shi J, Liu J, Lv H, Li J, Wang J, Deng Y, Ran L, Shi X, Wang X, Wu Q, Li C, Ren X, Wang J, Wang X, Li D, Liu D, Zhang X, Ji Z, Zhao W, Sun Y, Zhang Z, Bao J, Han Y, Dong L, Ji J, Chen P, Wu S, Liu J, Xiao Y, Bu D, Tan J, Yang L, Ye C, Zhang J, Xu J, Zhou Y, Yu Y, Zhang B, Zhuang S, Wei H, Liu B, Lei M, Yu H, Li Y, Xu H, Wei S, He X, Fang L, Zhang Z, Zhang Y, Huang X, Su Z, Tong W, Li J, Tong Z, Li S, Ye J, Wang L, Fang L, Lei T, Chen C, Chen H, Xu Z, Li H, Huang H, Zhang F, Xu H, Li N, Zhao C, Li S, Dong L, Huang Y, Li L, Xi Y, Qi Q, Li W, Zhang B, Hu W, Zhang Y, Tian X, Jiao Y, Liang X, Jin J, Gao L, Zheng W, Hao B, Liu S, Wang W, Yuan L, Cao M, McDermott J, Samudrala R, Wang J, Wong GK, Yang H (2005) The genomes of Oryza sativa:a history of duplications. PLoS Biol 3:266–281
Acknowledgments
We thank Mr. Naoya Watanabe and Dr. Yasuhiro Kondoh (Honda Research Institute, Japan) for their helpful suggestions regarding the experimental design.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Q. Zhang.
Rights and permissions
About this article
Cite this article
Yamamoto, E., Takashi, T., Morinaka, Y. et al. Interaction of two recessive genes, hbd2 and hbd3, induces hybrid breakdown in rice. Theor Appl Genet 115, 187–194 (2007). https://doi.org/10.1007/s00122-007-0554-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-007-0554-9