Abstract
Plants have evolved many systems to prevent inappropriate fertilization. Among them, incompatibility is a well-organized system in which pollen germination or pollen-tube growth is inhibited in pistils. Self-incompatibility (SI), rejecting self-pollen, promotes outbreeding in flowering plants. On the other hand, inter-species incompatibility, preventing gene flow among species to restrict outbreeding, usually occurs unilaterally, and is known as unilateral incompatibility (UI). In Brassicaceae, little is known about the molecular mechanism of UI, although S-locus genes involved in recognition of self-pollen have been characterized in the SI system. In the present study, we characterized novel UI observed between members of the same species, Brassica rapa; pollen of Turkish SI lines was specifically rejected by pistils of the Japanese commercial SI variety ‘Osome’. The incompatible phenotype of this intra-species UI closely resembled that of SI. Segregation analysis revealed that the pollen factor of this UI was not linked to the S-locus.
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References
Bateman AJ (1955) Self-incompatibility systems in angiosperms. III. Cruciferae. Heredity 9:52–68
Chetelat CB, De Verna JW (1991) Expression of unilateral incompatibility in pollen of Lycopersicon pennellii is determined by major loci on chromosomes 1, 6 and 10. Theor Appl Genet 82:704–712
Doughty J, Dixon S, Hiscock SJ, Willis AC, Parkin LA, Dickinson HG (1998) PCP-A1, a defensin-like Brassica pollen coat protein that binds the S-locus glycoproteins, is the product of gametophytic gene expression. Plant Cell 10:1333–1347
Doughty J, Wong HY, Dickinson HG (2000) Cysteine-rich pollen coat proteins (PCPs) and their interactions with stigmatic S (incompatibility) and S-related proteins in Brassica; putative roles in SI and pollination. Ann Bot 85:161–169
Gonai H, Hinata K (1971) Growth of pistils in relation to phenotypic expression of self-incompatibility in Brassica. Jpn J Breed 21:137–142
Hardon JJ (1967) Unilateral incompatibility between Solanum pennellii and Lycoperisicon esculentum. Genetics 57:795–808
Harrison BJ, Darby LA (1955) Unilateral hybridization. Nature 176:952
Hatakeyama K, Watanabe M, Takasaki T, Ojima K, Hinata K (1998) Dominance relationships between S-alleles in self-incompatible Brassica campestris L. Heredity 80:241–247
Heslop-Harrison J (1982) Pollen stigma interaction and cross-incompatibility in the grasses. Science 215:1358–1364
Hiscock SJ, Dickinson HG (1993) Unilateral incompatibility within the Brassicaceae: further evidence for the involvement of the self-incompatibility (S)-locus. Theor Appl Genet 86:744–753
Hogenboom NG (1972) Breaking breeding barriers in Lycoperisicon 5. The inheritance of unilateral incompatibility between L. peruvianum (L.) MILL. and L. esculentum MILL. and the genetics of its breakdown. Euphytica 21:405–414
Kachroo A, Schopfer CR, Nasrallah ME, Nasrallah JB (2001) Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 293:1824–1826
Kho YO, Bear J (1968) Observing pollen tubes by means of fluorescence. Euphytica 17:298–302
Lewis D, Crowe LK (1958) Unilateral incompatibility in flowering plants. Heredity 12:233–256
Martin FW (1963) Distribution and interrelationship of incompatibility barriers in the Lycopersicon hirsutum Humb. and Bonpl. complex. Evolution 17:519–528
Martin FW (1964) The inheritance of unilateral incompatibility in Lycopersicon hirsutum. Genetics 50:459-469
Martin FW (1967) The genetic control of unilateral incompatibility between two tomato species. Genetics 56:391–398
Matsuda N, Tsuchiya T, Kishitani S, Tanaka Y, Toriyama K (1996) Partial male sterility in transgenic tobacco carrying antisense and sense PAL cDNA under the control of a tapetum-specific promoter. Plant Cell Physiol 37:215–222
Matsushita M, Watanabe M, Yamakawa S, Takayama S, Isogai A, Hinata K (1996) The SLGs corresponding to the same S24-haplotype are perfectly conserved in three different self-incompatible Brassica campestris L. Genes Genet Syst 71:255–258
Murfett J, Strabala TJ, Zurek DM, Mou BQ, Beecher B, McClure BA (1996) S RNase and inter-species pollen rejection in the genus Nicotiana: multiple pollen-rejection pathways contribute to unilateral incompatibility between self-incompatible and self-compatible species. Plant Cell 8:943–958
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Nettancourt D de (2001) Incompatibility and incongruity in wild and cultivated plants, 2nd edn. Springer, Berlin Heidelberg New York
Nou IS, Watanabe M, Isogai A, Shinozawa H, Suzuki A, Hinata K (1991) Variation of S-alleles and S-glycoproteins in a naturalized population of self-incompatible Brassica campestris L. Jpn J Genet 66:227–239
Nou IS, Watanabe M, Isuzugawa K, Isogai A, Hinata K (1993a) Isolation of S-alleles from a wild population of Brassica campestris L. at Balcesme, Turkey and their characterization by S-glycoproteins. Sex Plant Reprod 6:71–78
Nou IS, Watanabe M, Isogai A, Hinata K (1993b) Comparison of S-alleles and S-glycoproteins between two wild populations of Brassica campestris in Turkey and Japan. Sex Plant Reprod 6:79–86
Ockendon DJ (2000) The S-allele collection of Brassica oleracea. Acta Hortic 539:25–30
Sampson DR (1962) Intergeneric pollen-stigma incompatibility in Cruciferae. Can J Genet Cytol 4:38–49
Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700
Shiba H, Takayama S, Iwano M, Shimosato H, Funato M, Nakagawa T, Suzuki G, Watanabe M, Hinata K, Isogai A (2001) An anther-expressed gene SP11 determines the pollen S-specificity in the self-incompatibility of Brassica rapa. Plant Physiol 125:2095–2103
Shiba H, Iwano M, Entani T, Ishimoto K, Shimosato H, Che F-S, Satta Y, Ito A, Takada Y, Watanabe M, Isogai A, Takayama S (2002) The dominance of alleles controlling self-incompatibility in Brassica pollen is regulated at the RNA level. Plant Cell 14:491–504
Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci USA 88:8816–8820
Suzuki G, Kai N, Hirose T, Fukui K, Nishio T, Takayama S, Isogai A, Watanabe M, Hinata K (1999) Genomic organization of the S locus: identification and characterization of genes in SLG/SRK region of S9 haplotype of Brassica campestris (syn. rapa). Genetics 153:391–400
Takada Y, Ito A, Ninomiya C, Kakizaki T, Takahata Y, Suzuki G, Hatakeyama K, Hinata K, Shiba H, Takayama S, Isogai A, Watanabe M (2001) Characterization of expressed genes in the SLL2 region of self-compatible Arabidopsis thaliana. DNA Res 8:215–219
Takasaki T, Hatakeyama K, Watanabe M, Toriyama K, Isogai A, Hinata K (1999) Introduction of SLG (S-locus glycoproteins) alters the phenotype of endogenous S-haplotype, but confers no new S-haplotype specificity in Brassica rapa L. Plant Mol Biol 40:659–668
Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai A, Hinata K (2000) The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403:913–916
Takayama S, Shiba H, Iwano M, Asano K, Hara M, Che FS, Watanabe M, Hinata K, Isogai A (2000a) Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoproteins 1 involved in pollen-stigma adhesion. Proc Natl Acad Sci USA 97:3765–3770
Takayama S, Shiba H, Iwano M, Shimosato H, Che FS, Kai N, Watanabe M, Suzuki G, Hinata K, Isogai A (2000b) The pollen determinant of self-incompatibility in Brassica campestris. Proc Natl Acad Sci USA 97:1920–1925
Takayama S, Shimosato H, Shiba H, Funato M, Che FS, Watanabe M, Iwano M, Isogai A (2001) Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413:524–538
Watanabe M, Hatakeyama K, Takada Y, Hinata K (2001) Molecular aspects of self-incompatibility in Brassica species. Plant Cell Physiol 42:560–565
Watanabe M, Takayama S, Isogai A, Hinata K (2003) Recent progresses on self-incompatibility research in Brassica species. Breed Sci 53:199–208
Acknowledgements
This work was supported in part by Grants-in-Aid for Special Research on priority Areas (Nos. 11238201 and 14360002) and Grants-in-Aid for the 21st Century Center of Excellence Program to Nara Institute of Science and Technology and Iwate University from the Ministry of Education, Culture, Sports, Science, and Technology of Japan and a Grant-in-Aid for Creative Scientific Research (No. 16G3016) from Japan Society for Promotion of Science (JSPS). Y.T. and T.K. are the recipients of a Research Fellowship of the Japan Society for the Promotion of Science for Young Scientists. The authors are grateful to Ayako Chiba, Yukiko Ohyama, and Hiroyuki Ishikawa (Iwate University) for technical assistance. We also thank Dr. Kokichi Hinata (Iwate Biotechnology Research Center) for his helpful discussion.
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Takada, Y., Nakanowatari, T., Sato, J. et al. Genetic analysis of novel intra-species unilateral incompatibility in Brassica rapa (syn. campestris) L.. Sex Plant Reprod 17, 211–217 (2005). https://doi.org/10.1007/s00497-004-0235-7
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DOI: https://doi.org/10.1007/s00497-004-0235-7