Genetic features of a pollen-part mutation suggest an inhibitory role for the Antirrhinum pollen self-incompatibility determinant
- 251 Downloads
Self-incompatibility (SI), an important barrier to inbreeding in flowering plants, is controlled in many species by a single polymorphic S-locus. In the Solanaceae, two tightly linked S-locus genes, S-RNase and SLF (S-locus F-box)/SFB (S-haplotype-specific F-box), control SI expression in pistil and pollen, respectively. The pollen S-determinant appears to function to inhibit all but self S-RNase in the Solanaceae, but its genetic function in the closely-related Plantaginaceae remains equivocal. We have employed transposon mutagenesis in a member of the Plantaginaceae (Antirrhinum) to generate a pollen-part SI-breakdown mutant Pma1 (Pollen-part mutation in Antirrhinum1). Molecular genetic analyses showed that an extra telocentric chromosome containing AhSLF-S 1 is present in its self-compatible but not in its SI progeny. Furthermore, analysis of the effects of selection revealed positive selection acting on both SLFs and SFBs, but with a stronger purifying selection on SLFs. Taken together, our results suggest an inhibitor role of the pollen S in the Plantaginaceae (as represented by Antirrhinum), similar to that found in the Solanaceae. The implication of these findings is discussed in the context of S-locus evolution in flowering plants.
KeywordsSelf-incompatibility Antirrhinum SLF Pollen-part mutation S-RNase
We thank Enrico Coen and Rosemary Carpenter for providing Antirrhinum plants and constant support and advice, Peter Walker for growing the plants and Ruth McGrath, Gwyneth Ingram and Richard Waites for their involvement in the mutagenesis work. This work was supported by the Ministry of Science and Technology of China (2007CB947603) to Y. Xue and the UK Biotechnology and Biological Sciences Research Council to H.D.
- Anderson MA, Cornish EC, Mau SL, Williams EG, Hogart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penshow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE (1986) Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Nature 321:38–44. doi: 10.1038/321038a0 CrossRefGoogle Scholar
- Burton TL, Husband BC (2000) Fitness differences among diploids, tetraploids, and their triploid progeny in Chamerion angustifolium: mechanisms of inviability and implications for polyploid evolution. Evol Int J Org Evol 54:1182–1191Google Scholar
- de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, HeidelbergGoogle Scholar
- Entani T, Iwano M, Shiba H, Che FS, Isogai A, Takayama S (2003) Comparative analysis of the self-incompatibility (S-) locus region of Prunus mume: identification of a pollen-expressed F-box gene with allelic diversity. Genes Cells 8:203–213. doi: 10.1046/j.1365-2443.2003.00626.x PubMedCrossRefGoogle Scholar
- Qiao H, Wang H, Zhao L, Zhou J, Huang J, Zhang Y, Xue Y (2004b) The F-box protein AhSLF-S2 physically interacts with S-RNases that may be inhibited by the ubiquitin/26S proteasome pathway of protein degradation during compatible pollination in Antirrhinum. Plant Cell 16:582–595. doi: 10.1105/tpc.017673 PubMedCrossRefGoogle Scholar
- Sassa H, Kakui H, Miyamoto M, Suzuki Y, Hanada T, Ushijima K, Kusaba M, Hirano H, Koba T (2007) S locus F-box brothers: Multiple and pollen-specific F-box genes with S haplotype-specific polymorphisms in apple and Japanese pear. Genetics 175:1869–1881. doi: 10.1534/genetics.106.068858 PubMedCrossRefGoogle Scholar
- Straub J (1941) Breakdown of self-incompatibility by polyploidization. (Die Beseitigung der Selbststerilitat durch Polyploidisierung). Ber Dtsch Bot Ges 59:296–304Google Scholar
- Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hirano H (2003) Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-box gene with haplotype-specific polymorphism. Plant Cell 15:771–781. doi: 10.1105/tpc.009290 PubMedCrossRefGoogle Scholar
- Wang Y, Tsukamoto T, Yi KW, Wang X, Huang S, McCubbin AG, Kao T-H (2004) Chromosome walking in the Petunia inflata self-incompatibility (S-) locus and gene identification in an 881-kb contig containing S 2-RNase. Plant Mol Biol 54:727–742. doi: 10.1023/B:PLAN.0000040901.98982.82 PubMedCrossRefGoogle Scholar
- Xue Y (2000) Establishment of the self-incompatibility (S) locus-directed transposon tagging system in Antirrhinum. Acta Bot Sin 42:408–415Google Scholar