Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

Nature Plants

Volumn 1, Issue , 2015, Pages

  Kubo, Ken Ichi ^a   Paape, Timothy ^b   Hatakeyama, Masaomi ^b,c   Entani, Tetsuyuki ^a   Takara, Akie ^a   Kajihara, Kie ^a   Tsukahara, Mai ^a   Shimizu Inatsugi, Rie ^b   Shimizu, Kentaro K ^b   Takayama, Seiji ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c FUNCTIONAL GENOMICS CENTER ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84928889562     PISSN: None     EISSN: 20550278     Source Type: Journal    
DOI: 10.1038/nplants.2014.5     Document Type: Article

References (50)

1. Takayama, S. & Isogai, A. Self-incompatibility in plants. Annu. Rev. Plant Biol. 56, 467-489 (2005).
2. Franklin-Tong, V. E. Self-Incompatibility in Flowering Plants: Evolution, Diversity, and Mechanisms (Springer, 2008).
3. Iwano, M. & Takayama, S. Self/non-self discrimination in angiosperm self-incompatibility. Curr. Opin. Plant Biol. 15, 78-83 (2012).
4. Sims, T. L. & Robbins, T. P. in Petunia. Evolutionary, Developmental and Physiological Genetics (ed. Gerats, T. & Strommer, J. ) 85-106 (Springer, 2009).
5. Sato, K. et al. Coevolution of the S-locus genes SRK, SLG and SP11/SCR in Brassica oleracea and B. rapa. Genetics 162, 931-940 (2002).
6. Ushijima, K. et al. Structural and transcriptional analysis of self-incompatibility (S) locus of almond (Prunus dulcis): identification of a pollen-expressed F-box gene with haplotype-specific polymorphism. Plant Cell 15, 771-781 (2003).
7. Sassa, H. et al. 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 (2007).
8. Entani, T. et al. Ubiquitin-proteasome-mediated degradation of S-RNase in a solanaceous cross-compatibility reaction. Plant J. 78, 1014-1021 (2014).
9. Kubo, K. et al. Collaborative non-self recognition system in S-RNase-based self-incompatibility. Science 330, 796-799 (2010).
10. Bergelson, J. , Kreitman, M. , Stahl E. A. & Tian, D. Evolutionary dynamics of plant R-genes. Science 292, 2281-2285 (2001).
11. Newbigin, E. , Paape, T. & Kohn, J. R. RNase-based self-incompatibility: Puzzled by pollen S. Plant Cell 20, 2286-2292 (2008).
12. The Potato Genome Sequencing Consortium. Genome sequence and analysis of the tuber crop potato. Nature 475, 189-195 (2011).
13. The Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635-641 (2012).
14. Tanksley, S. D. & Loaiza-Figueroa, F. Gametophytic self-incompatibility is controlled by a single major locus on chromosome 1 in Lycopersicon peruvianum. Proc. Natl Acad. Sci. USA 82, 5093-5096 (1985).
15. Gebhardt, C. et al. RFLP maps of potato and their alignment with the homoeologous tomato genome. Theor. Appl. Genet. 83, 49-57 (1991).
16. Goubet, P. M. et al. Contrasted patterns of molecular evolution in dominant and recessive self-incompatibility haplotypes in Arabidopsis. PLoS Genet. 8, e1002495 (2012).
17. Richman, A. Evolution of balanced genetic polymorphism. Mol. Ecol. 9, 1953-1963 (2000).
18. Goldberg, E. E. et al. Species selection maintains self-incompatibility. Science 330, 493-495 (2010).
19. McVean, G. , Awadalla, P. & Fearnhead, P. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160, 1231-1241 (2002).
20. Sawyer, S. Statistical tests for gene conversion. Mol. Biol. Evol. 6, 526-538 (1989).
21. Tsukamoto, T. , Ando, T. ,Watanabe, H. , Marchesi, E. & Kao, T-h. Duplication of the S-locus F-box gene is associated with breakdown of pollen function in an S-haplotype identified in a natural population of self-incompatible Petunia axillaris. Plant Mol. Biol. 57, 141-153 (2005).
22. Sijacic, P. et al. Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429, 302-305 (2004).
23. Williams, J. S. et al. Four previously identified Petunia inflata S-locus F-box genes are involved in pollen specificity in self-incompatibility. Mol. Plant 7, 567-569 (2014).
24. Gervais, C. E. , Castric, V. , Ressayre, A. & Billiard, S. Origin and diversification dynamics of self-incompatibility haplotypes. Genetics 188, 625-636 (2011).
25. Shimizu, K. K. , Kudoh, H. & Kobayashi, M. J. Plant sexual reproduction during climate change: gene function in natura studied by ecological and evolutionary systems biology. Ann Bot. 108, 777-787 (2011).
26. Uyenoyama, M. K. , Zhang, Y. & Newbigin, E. On the origin of selfincompatibility haplotypes: Transition through self-compatible intermediates. Genetics 157, 1805-1817 (2001).
27. Bomblies, K. et al. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol. 5, e236 (2007).
28. Bomblies, K. & Weigel, D. Hybrid necrosis: Autoimmunity as a potential gene-flow barrier in plant species. Nature Rev. Genet. 8, 382-393 (2007).
29. Kokubun, H. et al. Distribution of self-compatible and self-incompatible populations of Petunia axillaris (Solanaceae) outside Uruguay. J. Plant. Res. 119, 419-430 (2006).
30. Darwin, C. The Effects of Cross and Self Fertilisation in the Vegetable Kingdom (J. Murray, 1876).
31. Fisher, R. A. Average excess and average effect of a gene substitution. Ann. Eugen. 11, 53-63 (1941).
32. Busch, J. W. & Schoen, D. J. The evolution of self-incompatibility when mates are limiting. Trends Plant Sci. 13,128-136 (2008).
33. Tsuchimatsu, T. & Shimizu, K. K. Effects of pollen availability and the mutation bias on the fixation of mutations disabling the male specificity of self-incompatibility. J. Evol. Biol. 26, 2221-2232 (2013).
34. Boggs, N. A. et al. Expression of distinct self-incompatibility specificities in Arabidopsis thaliana. Genetics 182: 1313-1321 (2009).
35. Tsuchimatsu, T. et al. Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature 464, 1342-1346 (2010).
36. Tsuchimatsu, T. , Kaiser, P. , Yew, C. L. , Bachelier, J. B. & Shimizu, K. K. Recent loss of self-incompatibility by degradation of the male component in allotetraploid Arabidopsis kamchatica. PLoS Genet. 8, e1002838 (2012).
37. Wang, Y. , Wang, X. , McCubbin, A. G. & Kao, T-h. Genetic mapping and molecular characterization of the self-incompatibility (S) locus in Petunia inflata. Plant Mol. Biol. 53, 565-580 (2003).
38. Entani, T. et al. Centromeric localization of an S-RNase gene in Petunia hybrida Vilm. Theor. Appl. Genet. 99, 391-397 (1999).
39. Talbert, P. B. & Henikoff, S. Centromeres convert but don't cross. PLoS Biol. 8, e1000326 (2010).
40. Wang X. , Hughes, A. L. , Tsukamoto, T. , Ando, A. & Kao, T-h. Evidence that intragenic recombination contributes to allelic diversity of the S-RNase gene at the self-incompatibility (S) locus in Petunia inflata. Plant Physiol. 125, 1012-1022 (2001).
41. Vieira, C. P. , Charlesworth, D. & Vieira, J. Evidence for rare recombination at the gametophytic self-incompatibility locus. Heredity 91, 262-267 (2003).
42. Kaessmann, H. , Vinckenbosch, N. & Long, M. RNA-based gene duplication: mechanistic and evolutionary insight. Nature Rev. Genet. 10, 19-31 (2009).
43. Wang, Y. et al. Chromosome walking in the Petunia inflata self-incompatibility (S-) locus and gene identification in an 881-kb contig containing S2-RNase. Plant Mol. Biol. 54, 727-742 (2004).
44. Charlesworth, D. How can two-gene models of self-incompatibility generate new specificities? Plant Cell 12, 309-310 (2000).
45. Uyenoyama, M. K. & Newbigin, E. Evolutionary dynamics of dual-specificity self-incompatibility alleles. Plant Cell 12, 310-312 (2000).
46. Cipar, M. S. , Peloquin, S. J. & Hougas, R. W. Variability in the expression of self-incompatibility in tuber-bearing diploid Solanum species. Am. Potato J. 41, 155-162 (1964).
47. Schultz, J. , Milpetz, F. , Bork, P. & Ponting, C. P. SMART, a simple modular architecture research tool: Identification of signaling domains. Proc. Natl Acad. Sci. USA 95, 5857-5864 (1998).
48. Tamura K. et al. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).
49. Librado, P. & Rozas, J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452 (2009).
50. Williams, J. S. , Der, J. P. , de Pamphilis, C. W. & Kao, T-h. Transcriptome analysis reveals the same 17 S-locus F-box genes in two haplotypes of the selfincompatibility locus of Petunia inflata. Plant Cell 26, 2873-2888 (2014).