Balancing selection in the wild: Testing population genetics theory of self-incompatibility in the rare species Brassica insularis

Genetics

Volumn 171, Issue 1, 2005, Pages 279-289

  Glémin, Sylvain ^a   Gaude, Thierry ^b   Guillemin, Marie Laure ^c   Lourmas, Mathieu ^d   Olivieri, Isabelle ^e   Mignot, Agnès ^e  

^a UNIV MONTPELLIER   (France)

^b UNIVERSITÉ DE LYON   (France)

^c STATION BIOLOGIQUE   (France)

^d CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^e INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; MICROSATELLITE DNA;

ALLELE; ARTICLE; BRASSICA; GENETIC VARIABILITY; GENOTYPE; NONHUMAN; PHENOTYPE; POPULATION GENETICS; PRIORITY JOURNAL; SPECIES DIFFERENTIATION; WESTERN BLOTTING;

ALLELES; BLOTTING, WESTERN; BRASSICA; FERTILITY; FRANCE; GENE FREQUENCY; GENETICS, POPULATION; GENOTYPE; GEOGRAPHY; GLYCOPROTEINS; MODELS, GENETIC; PLANT PROTEINS; SELECTION (GENETICS); VARIATION (GENETICS);

BRASSICA; BRASSICA INSULARIS;

EID: 26444450074     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.104.035915     Document Type: Article

References (56)

1. AGUILAR, A., G. ROEMER, S. DEBENHAM, M. BINNS, D. GARCELON et al., 2004 High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc. Natl. Acad. Sci. USA 101: 3490-3494.
2. ASPINWALL, N., and T. CHRISTIAN, 1992 Pollination biology, seed production, and population structure in queen-of-the-prairie, Filipendula rubra (Rosaceae) at Botkin fen, Missouri. Am. J. Bot. 79: 488-494.
3. AWADALLA, P., and D. CHARLESWORTH, 1999 Recombination and selection at Brassica self-incompatibility loci. Genetics 152: 413-425.
4. BECHSGAARD, J., T. BATAILLON and M. H. SCHIERUP, 2004 Uneven segregation of sporophytic self-incompatibility alleles in Arabidopsis lyrata. J. Evol. Biol. 17: 554-561.
5. BELL, C. J., and J. R. ECKER, 1994 Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19: 137-144.
6. BOYCE, W. M., P. W. HEDRICK, N. E. MUGGLI-COCKETT, S. KALINOWSKI, M. C. PENEDO et al., 1997 Genetic variation of major histocompatibility complex and microsatellite loci: a comparison in bighorn sheep. Genetics 145: 421-433.
7. BRENNAN, A. C., S. A. HARRIS and S. J. HISCOCK, 2003 Population genetics of sporophytic self-incompatibility in Senecio squalidus L. (Asteraceae) II: a spatial autocorrelation approach to determining mating behaviour in the presence of low S allele diversity. Heredity 91: 502-509.
8. BYERS, D. L., 1995 Pollen quantity and quality as explanations for low seed set in small populations exemplified by Eupatorium (Asteraceae). Am. J. Bot. 82: 1000-1006.
9. BYERS, D. L., and T. R. MEAGHER, 1992 Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility. Heredity 68: 353-359.
10. CAMPBELL, J. M., and M. J. LAWRENCE, 1981 The population genetics of the self-incompatibility polymorphism in Papaver rhoeas. 1. The number and distribution of S-alleles in families from three localities. Heredity 46: 69-79.
11. CASSELMAN, A. L., J. VREBALOV, J. A. CONNER, A. SINGHAL, J. GIOVANNONI et al., 2000 Determining the physical limits of the Brassica S locus by recombination analysis. Plant Cell 12: 23-33.
12. CORNUET, J. M., and G. LUIKART, 1996 Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.
13. DE NETTANCOURT, D., 2001 Incompatibility and Incongruity in Wild and Cultivated Plants. Springer, Berlin.
14. DEMAURO, M. M., 1993 Relationship of breeding system to rarity in the Lakeside Daisy (Hymenoxys acaulis var. glabra). Conserv. Biol. 7: 542-550.
15. DOYLE, J. J., and J. L. DOYLE, 1987 A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11-15.
16. ELLEGREN, H., 2004 Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5: 435-445.
17. GAUDE, T., L. DENOROY and C. DUMAS, 1991 Use of a fast protein electrophoretic purification procedure for N-terminal sequence analysis to identity S-locus related proteins in stigmas of Brassica oleracea. Electrophoresis 12: 646-653.
18. GAUDE, T., A. FRIRY, P. HEIZMANN, C. MARIAC, M. ROUGIER et al., 1993 Expression of a self-incompatibility gene in a self-compatible line of Brassica oleracea. Plant Cell 5: 75-86.
19. GAUDE, T., M. ROUGIER, P. HEIZMANN, D. J. OCKENDON and C. DUMAS, 1995 Expression level of the SLG gene is not correlated with the self-incompatibility phenotype in the class II S haplotypes of Brassica oleracea. Plant Mol. Biol. 27: 1003-1014.
20. GIRANTON, J. L., M. J. ARIZA, C. DUMAS, J. M. COCK and T. GAUDE, 1995 The S locus receptor kinase gene encodes a soluble glycoprotein corresponding to the SKR extracellular domain in Brassica oleracea. Plant J. 8: 827-834.
21. GLÉMIN, S., T. BATAILLON, J. RONFORT, A. MIGNOT and I. OLIVIERI, 2001 Inbreeding depression in small populations of self-incompatible plants. Genetics 159: 1217-1229.
22. HATAKEYAMA, K., M. WATANABE, T. TAKASAKI, K. OJIMA and K. HINATA, 1998 Dominance relationships between S-alleles in self-incompatible Brassica campestris L. Heredity 80: 241-247.
23. HISCOCK, S. J., and S. M. MCINNIS, 2003 Pollen recognition and rejection during the sporophytic self-incompatibility response: Brassica and beyond. Trends Plant Sci. 8: 606-613.
24. HURTREZ-BOUSSES, S., 1996 Genetic differentiation among natural populations of the rare Corsican endemic Brassica insularis Moris: implications for conservation guidelines. Biol. Conserv. 76: 25-30.
25. KACHROO, A., C. R. SCHOPFER, M. E. NASRALLAH and J. B. NASRALLAH, 2001 Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 293: 1824-1826.
26. KIMURA, M., and T. OHTA, 1978 Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc. Natl. Acad. Sci. USA 75: 2868-2872.
27. KUSABA, M., T. NISHIO, Y. SATTA, K. HINATA and D. OCKENDON, 1997 Striking sequence similarity in inter- and intra-specific comparisons of class 1 SLG alleles from Brassica oleracea and Brassica campestris: implications for the evolution and recognition mechanism. Proc. Natl. Acad. Sci. USA 94: 7673-7678.
28. LANDRY, C., and L. BERNATCHEX, 2001 Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Mol. Ecol. 10: 2525-2539.
29. LAWRENCE, M. J., 2000 Population genetics of the homomorphic self-incompatibility polymorphisms in flowering plants. Ann. Bot. 85 (Suppl. A): 221-226.
30. LES, D. H., J. A. REINARTZ and E. J. ESSELMAN, 1991 Genetic consequences of rarity in Aster furcatus (Asteraceae), a threatened, self-incompatible plant. Evolution 45: 1641-1650.
31. MABLE, B. K., M. H. SCHIERUP and D. CHARLESWORTH, 2003 Estimating the number, frequency, and dominance of S-alleles in a natural population of Arabidopsis lyrata (Brassicaceae) with sporophytic control of self-incompatibility. Heredity 90: 422-431.
32. MIÈGE, C., V. RUFFIO-CHABLE, M. H. SCHIERUP, D. CABRILLAC, C. DUMAS et al., 2001 Intrahaplotype polymorphism at the Brassica S locus. Genetics 159: 811-822.
33. MUIRHEAD, C. A., 2001 Consequences of population structure on genes under balancing selection. Evolution 55: 1532-1541.
34. NASRALLAH, M. E., 1991 The molecular basis for sexual incompatibility, pp. 130-152 in Developmental Regulation of Plant Gene Expression, edited by D. GRIERSON. Blackie & Son, Glasgow, UK.
35. PETIT, C., H. FRÉVILLE, A. MIGNOT, B. COLAS, E. IMBERT et al., 2001 Gene flow and local adaptation in two endemic plant species. Biol. Conserv. 100: 21-34.
36. RAYMOND, M., and F. ROUSSSET, 1995 Genepop (version 1.2), a population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249.
37. RICHMAN, A. D., and J. R. KOHN, 1996 Learning from rejection: the evolutionary biology of single-locus incompatibility. Trends Ecol. Evol. 11: 497-502.
38. RUFFIO-CHÂBLE, V., and T. GAUDE, 2001 S-haplotype polymorphism in Brassica oleracea. Acta Hortic. 546: 257-261.
39. RUFFIO-CHÂBLE, V., Y. HERVÉ, C. DUMAS and T. GAUDE, 1997 Distribution of S-haplotypes and its relationship with self-incompatibility in Brassica oleracea. Part 1. In inbred lines of cauliflower (B. olearacea var 'botrytis'). Theor. Appl. Genet. 94: 338-346.
40. RUFFIO-CHâBLE, V., J. P. LE SAINT and T. GAUDE, 1999 Distribution of S-haplotypes and its relationship with self-incompatibility in Brassica oleracea. 2. In varieties of broccoli and romanesco. Theor. Appl. Genet. 98: 541-550.
41. SATO, K., T. NISHIO, R. KIMURA, M. KUSABA, T. SUZUKI et al., 2002 Coevolution of the S-locus genes SRK, SLG and SP11/ SCR in Brassica oleracea and B. rapa. Genetics 162: 931-940.
42. SCHIERUP, M. H., 1998 The number of self-incompatibility alleles in a finite, subdivided population. Genetics 149: 1153-1162.
43. SCHIERUP, M. H., X. VEKEMANS and F. B. CHRISTIANSEN, 1997 Evolutionary dynamics of sporophytic self-incompatibility alleles in plants. Genetics 147: 835-846.
44. SCHIERUP, M. H., X. VEKEMANS and D. CHARLESWORTH, 2000 The effect of subdivision on variation at multi-allelic loci under balancing selection. Genet. Res. 76: 51-62.
45. SCHOPEER, C. R., M. E. NASRALLAH and J. B. NASRALLAH, 1999 The male determinant of self-incompatibility in Brassica. Science 286: 1697-1700.
46. SNOGERUP, S., M. GUSTAFSSON and R. V. BOTHMER, 1990 Brassica sect. Brassica (Brassicaceae). I. Taxonomy and variation. Willdenowia 19: 271-365.
47. SUZUKI, G., N. KAI, T. HIROSE, K. FUKUI, T. NISHIO et al., 1999 Genomic organization of the S locus: identification and characterization of genes in SLG/SRK region of S(9) haplotype of Brassica campestris (syn. rapa). Genetics 153: 391-400.
48. SZEWC-MCFADEN, A. K., S. KRESOVICH, S. M. BLIEK, S. E. MITCHELL and J. R. MCFERRON, 1996 Identification of polymorphic, conserved simple-sequence repeats (SSRs) in cultivated Brassica species. Theor. Appl. Genet. 93: 534-538.
49. TAKASAKI, T., K. HATAKEYAMA, G. SUZUKI, M. WATANABE, A. ISOGAI et al., 2000 The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403: 913-916.
50. TAKAYAMA, S., H. SHIBA, M. IWANO, H. SHIMOSATO, F. S. CHE et al., 2000 The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl. Acad. Sci. USA 97: 1920-1925.
51. UYENOYAMA, M. K., 2000 Evolutionary dynamics of self-incompatibility alleles in Brassica. Genetics 156: 351-359.
52. VEKEMANS, X., M. H. SCHIERUP and F. B. CHRISTIANSEN, 1998 Mate availability and fecundity selection in multi-allelic self-incompatibility systems in plants. Evolution 52: 19-29.
53. WAHLUND, S., 1928 Zuzammensetzung von populationen und korrelationserscheinungen vom Standpunkt dervererbungslehre aus betrachtet. Hereditas 11: 65-66.
54. WOLFRAM, S., 1996 The Mathematica Book. Cambridge University Press, Cambridge, UK.
55. WRIGHT, S., 1939 The distribution of self-sterility alleles in populations. Genetics 24: 538-552.
56. YOKOYAMA, S., and M. NEI, 1979 Population dynamics of sex-determining alleles in honey bees and self-incompatibility alleles in plants. Genetics 91: 609-626.