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MBE Advance Access published online on June 16, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl042
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© 2006 The Authors This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Accepted June 9, 2006

Research Article

The Transition to Self-Compatibility in Arabidopsis thaliana and Evolution within S-Haplotypes over 10 Million Years

Jesper S. Bechsgaard 1 * 1, Vincent Castric 2 1, Deborah Charlesworth 3, Xavier Vekemans 2, and Mikkel H. Schierup 1

1 Ecology and Genetics, Institute of Biological Sciences, University of Aarhus, Denmark
2 Laboratoire Génétique et Évolution des Populations Végétales, UMR CNRS 8016. Université Lille 1. France
3 ICAPB, University of Edinburgh, UK

* To whom correspondence should be addressed.
Jesper S. Bechsgaard, E-mail: jesper.bechsgaard{at}biology.au.dk


  Abstract

A recent investigation found evidence that the transition of Arabidopsis thaliana from ancestral self-incompatibility (SI) to full self-compatibility occurred very recently, and suggested that this occurred through a selective fixation of a non-functional allele ({Psi}SCR1) at the SCR gene, which determines pollen specificity in the incompatibility response. The main evidence is the lack of polymorphism at the SCR locus in A. thaliana. However, the nearby SRK gene, which determines stigma specificity in self-incompatible Brassicaceae species, has extremely high sequence diversity, with three very divergent SRK haplotypes, two of them present in multiple strains. Such high diversity is extremely unusual in this species, and it suggests the possibility that multiple different SRK haplotypes may have been preserved from A. thaliana's self-incompatible ancestor. To study the evolution of S-haplotypes in the A. thaliana lineage, we searched the two most closely related Arabidopsis species, A. lyrata and A. halleri, in which most populations have retained SI, and found SRK sequences corresponding to all three A. thaliana haplogroup sequences. Our molecular evolutionary analyses of these three S-haplotypes provide an independent estimate of the timing of the breakdown of SI, and again exclude an ancient transition to selfing in A. thaliana. Comparing sequences of each of the three haplogroups between species, we find that two of the three SRK sequences (haplogroups A and B) are similar throughout their length, suggesting that little or no recombination with other SRK alleles has occurred since these species diverged. The diversity difference between the SCR and SRK loci in A. thaliana, however, suggests crossing-over, either within SRK or between the SCR and SRK loci. If loss of SI involved fixation of the {Psi}SCR1 sequence, the exchange must have occurred during its fixation. Divergence between the species is much lower at the S-locus, compared with reference loci, and we discuss two contributory possibilities. Introgression may have occurred between A. lyrata and A. halleri, and between their ancestral lineage and A. thaliana, at least for some period after their split. In addition, the coalescence times of sequences of individual S-haplogroups are expected to be less than those of alleles at non-S loci.

Keywords: self-incompatibility; mating system; pseudogene; dn/ds ratio; SRK; SCR.

1These two authors contributed equally to this study.


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