Many postzygotic reproductive barrier forms have been reported in plants: hybrid weakness, hybrid necrosis, and hybrid chlorosis. In this study, linkage analysis of the genes causing hybrid chlorosis in F2 generation in rice, HCA1 and HCA2, was performed. HCA1 and HCA2 are located respectively on the distal regions of the short arms of chromosomes 12 and 11. These regions are known to be highly conserved as a duplicated chromosomal segment. The molecular mechanism causing F2 chlorosis deduced from the location of the two genes was discussed. The possibility of the introgression of the chromosomal segments encompassing HCA1 and/or HCA2 was also discussed from the viewpoint of Indica-Japonica differentiation. 1. Introduction Many post-zygotic reproductive barrier forms have been reported in plants [1]: hybrid weakness, hybrid necrosis, and hybrid chlorosis. The latter has been observed often in the F1 generation from crosses among wheat (Triticum aestivum L.) and its relatives [2–6]. This phenomenon resulted from the complementary action of a pair of dominant genes. Research for distribution of these genes contributed greatly to the study of the origin of wheat. Hybrid chlorosis in F2 generation has been reported only in rice (Oryza sativa L.) [7] and interspecific crosses among Melilotus species [8]. Sato et al. [7] incidentally found a case of hybrid chlorosis in the F2 population from a cross between two Japanese native cultivars: J-147 and J-321. Its first symptom was discoloration of the second or third leaf (Figure 1). The yellowish part expanded gradually. Then the whole plant died within 20 days [9], yielding no seed. The phenomenon was caused by a set of mutually independent duplicated recessive genes, named hca-1 and hca-2 by Sato and Morishima [9]. According to the new gene nomenclature system for rice [10], we changed our description of the gene symbols, as shown in Table 1. Table 1: Gene symbols frequently used in this study according to the new gene nomenclature system for rice [ 10]. Figure 1: Hybrid chlorosis caused by hca1-1 and hca2-1. Seedlings in an F 4 line from the cross between J-147 and IR24 are shown 10 days after sowing date. A chlorotic plant is located at the center. The neighboring green plants are normal. Rice is classified into two types: Indica-type and Japonica-type. Sato and Morishima [9] examined the distribution of HCA1 and HCA2. The experimentally obtained results can be summarized as follows. (1) The hca2-1 gene is widely distributed in native Japonica-type cultivars, whereas many Indica-type cultivars carry its
References
[1]
K. Bomblies and D. Weigel, “Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species,” Nature Reviews Genetics, vol. 8, no. 5, pp. 382–393, 2007.
[2]
K. Tsunewaki, “Gene analysis on chlorosis of the hybrid, Triticum aestivum var. Chenese Spring × T. macha var. subletschchumicum, and its bearing on the genetic basis of necrosis and chlorosis,” Japanese Journal of Genetics, vol. 41, no. 6, pp. 413–426, 1966.
[3]
K. Tsunewaki and J. Hamada, “A new type of hybrid chlorosis found in tetraploid wheats,” Japanese Journal of Genetics, vol. 43, no. 4, pp. 279–288, 1968.
[4]
K. Tsunewaki, “Distribution of necrosis genes in wheat V. Triticum macha, T. spelta and T. vavilovii,” Japanese Journal of Genetics, vol. 46, no. 2, pp. 93–101, 1971.
[5]
K. Tsunewaki and Y. Nakai, “Consideration on the origin and speciation of four groups of wheat from the distribution of necrosis and chlorosis genes,” in Proceedings of the 4th International Wheat Genetics Symposium, pp. 123–129, 1973.
[6]
T. Kawahara, “Genetic analysis of Cs chlorosis in tetraploid wheats,” Japanese Journal of Genetics, vol. 68, no. 2, pp. 147–153, 1993.
[7]
Y. I. Sato, S. Matsuura, and K. Hayashi, “The genetic basis of hybrid chlorosis found in a cross between two Japanese native cultivars,” Rice Genetics Newsletter, vol. 1, p. 106, 1984.
[8]
Y. Sano and F. Kita, “Reproductive barriers distributed in melilotus species and their genetic bases,” Canadian Journal of Genetics and Cytology, vol. 20, no. 2, pp. 275–289, 1978.
[9]
Y. I. Sato and H. Morishima, “Distribution of the genes causing F2 chlorosis in rice cultivars of the Indica and Japonica types,” Theoretical and Applied Genetics, vol. 75, no. 5, pp. 723–727, 1988.
[10]
S. R. McCouch and Committee on Gene Symbolization, Nomenclature and Linkage, Rice Genetics Cooperative (CGSNL), “Gene nomenclature system for rice,” Rice, vol. 1, pp. 72–84, 2008.
[11]
K. Ichitani, Y. Fukuta, S. Taura, and M. Sato, “Chromosomal location of Hwc2, one of the complementary hybrid weakness genes, in rice,” Plant Breeding, vol. 120, no. 6, pp. 523–525, 2001.
[12]
K. Ichitani, K. Namigoshi, M. Sato et al., “Fine mapping and allelic dosage effect of Hwc1, a complementary hybrid weakness gene in rice,” Theoretical and Applied Genetics, vol. 114, no. 8, pp. 1407–1415, 2007.
[13]
T. Kuboyama, T. Saito, T. Matsumoto, et al., “Fine mapping of HWC2, a complementary hybrid weakness gene, and haplotype analysis around the locus in rice,” Rice, vol. 2, pp. 93–103, 2009.
[14]
K. Ichitani, T. Taura, T. Tezuka, Y. Okiyama, and T. Kuboyama, “Chromosomal location of HWA1 and HWA2, complementary weakness genes in rice,” Rice., vol. 4, no. 2, pp. 29–38, 2011.
[15]
Y. Fukuta, K. Tamura, H. Sasahara, and T. Fukuyama, “Genetic and breeding analysis using molecular markers. 18. Variations of gene frequency and the RFLP map of the hybrid population derived from the cross between the rice variety, Milyang 23 and Akihikari,” Breeding Research, vol. 1, supplement 2, p. 176, 1999 (Japanese).
[16]
H. Tsunematsu, A. Yoshimura, Y. Harushima et al., “RFLP framework map using recombinant inbred lines in rice,” Breeding Science, vol. 46, no. 3, pp. 279–284, 1996.
[17]
T. Kubo and A. Yoshimura, “Genetic basis of hybrid breakdown in a Japonica/Indica cross of rice, Oryza sativa L.,” Theoretical and Applied Genetics, vol. 105, no. 6-7, pp. 906–911, 2002.
[18]
T. Kubo and A. Yoshimura, “Epistasis underlying female sterility detected in hybrid breakdown in a Japonica-Indica cross of rice (Oryza sativa L.),” Theoretical and Applied Genetics, vol. 110, no. 2, pp. 346–355, 2005.
[19]
M. Yokoo, S. Saito, T. Higashi, and S. Matsumoto, “Use of a Korean rice cultivar Milyang 23 for improving Japanese rice,” Breeding Science, vol. 44, pp. 219–222, 1994 (Japanese).
[20]
M. Lorieux, “MapDisto, A free user-friendly program for computing genetic maps,” Computer demonstration (P958) given at the Plant and Animal Genome 15th conference, San Diego, Calif, USA, 2007, http://mapdisto.free.fr/.
[21]
D. Kosambi, “The estimation of map distance from recombination values,” Annals of Eugenics, vol. 12, no. 3, pp. 172–175, 1944.
[22]
S. L. Dellaporta, J. Wood, and J. B. Hicks, “A plant DNA minipreparation: version II,” Plant Molecular Biology Reporter, vol. 1, no. 4, pp. 19–21, 1983.
[23]
T. Sasaki, “International Rice Genome Sequencing Project," "The map-based sequence of the rice genome,” Nature, vol. 436, no. 7052, pp. 793–800, 2005.
[24]
Y. Nagamura, T. Inoue, B. A. Antonio et al., “Conservation of duplicated segments between rice chromosomes 11 and 12,” Breeding Science, vol. 45, no. 3, pp. 373–376, 1995.
[25]
B. A. Antonio, T. Inoue, H. Kajiya et al., “Comparison of genetic distance and order of DNA markers in five populations of rice,” Genome, vol. 39, no. 5, pp. 946–956, 1996.
[26]
J. Wu, N. Kurata, H. Tanoue et al., “Physical mapping of duplicated genomic regions of two chromosome ends in rice,” Genetics, vol. 150, no. 4, pp. 1595–1603, 1998.
[27]
Y. Harushima, M. Yano, A. Shomura et al., “A high-density rice genetic linkage map with 2275 markers using a single F2 population,” Genetics, vol. 148, no. 1, pp. 479–494, 1998.
[28]
S. R. McCouch, L. Teytelman, Y. Xu et al., “Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.),” DNA Research, vol. 9, no. 6, pp. 199–207, 2002.
[29]
X. Chen, S. Temnykh, Y. Xu, Y. G. Cho, and S. R. McCouch, “Development of a microsatellite framework map providing genome-wide coverage in rice (Oryza sativa L.),” Theoretical and Applied Genetics, vol. 95, no. 4, pp. 553–567, 1997.
[30]
L. Monna, R. Ohta, H. Masuda, A. Koike, and Y. Minobe, “Genome-wide searching of single-nucleotide polymorphisms among eight distantly and closely related rice cultivars (Oryza sativa L.) and a wild accession (Oryza rufipogon Griff.),” DNA Research, vol. 13, no. 2, pp. 43–51, 2006.
[31]
S. Ouyang, W. Zhu, J. Hamilton et al., “The TIGR Rice Genome Annotation Resource: improvements and new features,” Nucleic Acids Research, vol. 35, no. 1, pp. D883–D887, 2007.
[32]
Y. Yamagata, E. Yamamoto, K. Aya et al., “Mitochondrial gene in the nuclear genome induces reproductive barrier in rice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 4, pp. 1494–1499, 2010.
[33]
Y. Mizuta, Y. Harushima, and N. Kurata, “Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 47, pp. 20417–20422, 2010.
[34]
D. Bikard, D. Patel, C. Le Metté et al., “Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana,” Science, vol. 323, no. 5914, pp. 623–626, 2009.
[35]
Y. Fukuta, H. Sasahara, K. Tamura, and T. Fukuyama, “RFLP linkage map included the information of segregation distortion in a wide-cross population between Indica and Japonica rice (Oryza sativa L.),” Breeding Science, vol. 50, no. 2, pp. 65–72, 2000.
[36]
Y. Kojima, K. Ebana, S. Fukuoka, T. Nagamine, and M. Kawase, “Development of an RFLP-based rice diversity research set of germplasm,” Breeding Science, vol. 55, no. 4, pp. 431–440, 2005.
[37]
K. Ebana, Y. Kojima, S. Fukuoka, T. Nagamine, and M. Kawase, “Development of mini core collection of Japanese rice landrace,” Breeding Science, vol. 58, no. 3, pp. 281–291, 2008.
[38]
K. Zhao, M. Wright, J. Kimball et al., “Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome,” PloS One, vol. 5, no. 5, article e10780, 2010.
