Evidence for rare recombination at the gametophytic self-incompatibility locus

The gametophytic self-incompatibility locus has been thought to be a nonrecombining genomic region. Inferences have been made, however, about the functional importance of different parts of the S-locus, based on differences in the levels of variability along the gene, and this is valid only if recombination occurs. It is thus important to test whether recombination occurs within and near the S-locus. Several recent attempts to test this have reached conflicting conclusions. In this study, we examine a large data set on sequence variation at the S-locus in several species with gametophytic self-incompatibility systems, in the Solanaceae, Rosaceae and Scrophulariaceae. We use the longest sequences available to test for recombination based on linkage disequilibrium between polymorphic sites in the S-locus. The relationship between linkage disequilibrium and physical distance between the sites suggests rare intragenic exchange in the evolutionary history of four species of Solanaceae and two species of Rosaceae.

[1]  R. Lewontin,et al.  On measures of gametic disequilibrium. , 1988, Genetics.

[2]  K. Fukui,et al.  Centromeric localization of an S-RNase gene in Petunia hybrida Vilm. , 1999, Theoretical and Applied Genetics.

[3]  M. Stoneking,et al.  Questioning evidence for recombination in human mitochondrial DNA. , 2000, Science.

[4]  P. Awadalla,et al.  Recombination and selection at Brassica self-incompatibility loci. , 1999, Genetics.

[5]  B. Charlesworth,et al.  Sequence variation: Looking for effects of genetic linkage , 1998, Current Biology.

[6]  G. McVean What do patterns of genetic variability reveal about mitochondrial recombination? , 2001, Heredity.

[7]  A. Clark,et al.  Excess nonsynonymous substitution of shared polymorphic sites among self-incompatibility alleles of Solanaceae. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  H. Dooner,et al.  Recombination occurs uniformly within the bronze gene, a meiotic recombination hotspot in the maize genome. , 1997, The Plant cell.

[9]  J. Stephens,et al.  Statistical methods of DNA sequence analysis: detection of intragenic recombination or gene conversion. , 1985, Molecular biology and evolution.

[10]  M. Uyenoyama,et al.  Allelic Diversity and Gene Genealogy at the Self-Incompatibility Locus in the Solanaceae , 1996, Science.

[11]  D. Charlesworth,et al.  The effect of subdivision on variation at multi-allelic loci under balancing selection. , 2000, Genetical research.

[12]  R. Bernatzky Genetic mapping and protein product diversity of the self-incompatibility locus in wild tomato (Lycopersicon peruvianum) , 1993, Biochemical Genetics.

[13]  A. Clark,et al.  Population Genetic Aspects of Gametophytic Self incompatibility , 1996 .

[14]  S. Sawyer Statistical tests for detecting gene conversion. , 1989, Molecular biology and evolution.

[15]  E. Newbigin,et al.  The S-locus of Nicotiana alata: genomic organization and sequence analysis of two S-RNase alleles , 1995, Plant Molecular Biology.

[16]  B. Charlesworth,et al.  Increased levels of polymorphism surrounding selectively maintained sites in highly selling species , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  P. Dodds,et al.  A genetic map of the Nicotiana alata S locus that includes three pollen-expressed genes , 2000, Theoretical and Applied Genetics.

[18]  J. Hein,et al.  Recombination, balancing selection and phylogenies in MHC and self-incompatibility genes. , 2001, Genetics.

[19]  D. Nettancourt Incompatibility in Angiosperms , 1977, Monographs on Theoretical and Applied Genetics.

[20]  H. Fu,et al.  Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. T. Hoopen,et al.  The self-incompatibility (S) locus in Petunia hybrida is located on chromosome III in a region, syntenic for the solanaceae , 1998 .

[22]  T. Kao,et al.  The flanking regions of twoPetunia inflata S alleles are heterogeneous and contain repetitive sequences , 1992, Plant Molecular Biology.

[23]  M. Slatkin,et al.  Gene and allelic genealogies at a gametophytic self-incompatibility locus. , 1994, Genetics.

[24]  G. Drouin,et al.  Detecting and characterizing gene conversions between multigene family members. , 1999, Molecular biology and evolution.

[25]  M. Oliveira,et al.  The RNase PD2 gene of almond (Prunus dulcis) represents an evolutionarily distinct class of S-like RNase genes , 2000, Molecular and General Genetics MGG.

[26]  A. Hughes,et al.  Evidence that intragenic recombination contributes to allelic diversity of the S-RNase gene at the self-incompatibility (S) locus in Petunia inflata. , 2001, Plant physiology.

[27]  D. Charlesworth,et al.  Molecular variation at the self-incompatibility locus in natural populations of the genera Antirrhinum and Misopates , 2002, Heredity.

[28]  Julio Rozas,et al.  DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis , 1999, Bioinform..

[29]  A. Richman,et al.  Evolutionary genetics of self-incompatibility in the Solanaceae , 2004, Plant Molecular Biology.

[30]  W. Rice ANALYZING TABLES OF STATISTICAL TESTS , 1989, Evolution; international journal of organic evolution.

[31]  M Slatkin,et al.  Distinguishing recombination and intragenic gene conversion by linkage disequilibrium patterns. , 2000, Genetical research.

[32]  S. Y. Lee,et al.  The 5' flanking sequences of two S alleles in Lycopersicon peruvianum are highly heterologous but contain short blocks of homologous sequences. , 1995, Plant & cell physiology.

[33]  N. Takahata,et al.  Selection, convergence, and intragenic recombination in HLA diversity , 2004, Genetica.

[34]  M. Worobey,et al.  A novel approach to detecting and measuring recombination: new insights into evolution in viruses, bacteria, and mitochondria. , 2001, Molecular biology and evolution.

[35]  N. Takahata,et al.  Footprints of intragenic recombination at HLA loci , 1998, Immunogenetics.

[36]  N. Risch,et al.  A comparison of linkage disequilibrium measures for fine-scale mapping. , 1995, Genomics.

[37]  T. Kao,et al.  The emerging complexity of self-incompatibility (S-) loci , 1999, Sexual Plant Reproduction.

[38]  H. Hirano,et al.  Characterization of the S-locus region of almond (Prunus dulcis): analysis of a somaclonal mutant and a cosmid contig for an S haplotype. , 2001, Genetics.

[39]  M. Nei,et al.  Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. , 1986, Molecular biology and evolution.

[40]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[41]  J. Braverman,et al.  Linkage disequilibria and the site frequency spectra in the su(s) and su(w(a)) regions of the Drosophila melanogaster X chromosome. , 2000, Genetics.

[42]  C. Strobeck Heterozygosity in pin-thrum plants or with partial sex linkage. , 1972, Genetics.

[43]  B. Charlesworth,et al.  Patterns of genetic variation at a chromosome 4 locus of Drosophila melanogaster and D. simulans. , 2002, Genetics.