SLocus Genes and the Evolution of Self-Fertility inArabidopsis thaliana

Abstract

Loss of self-incompatibility (SI) in Arabidopsis thaliana was accompanied by inactivation of genes required for SI, including S-LOCUS RECEPTOR KINASE (SRK) and S-LOCUS CYSTEINE-RICH PROTEIN (SCR), coadapted genes that constitute the SI specificity-determining S haplotype. Arabidopsis accessions are polymorphic for CSRK and CSCR, but it is unknown if the species harbors structurally different S haplotypes, either representing relics of ancestral functional and structurally heteromorphic S haplotypes or resulting from decay concomitant with or subsequent to the switch to self-fertility. We cloned and sequenced the S haplotype from C24, in which self-fertility is due solely to S locus inactivation, and show that this haplotype was produced by interhaplotypic recombination. The highly divergent organization and sequence of the C24 and Columbia-0 (Col-0) S haplotypes demonstrate that the A. thaliana S locus underwent extensive structural remodeling in conjunction with a relaxation of selective pressures that once preserved the integrity and linkage of coadapted SRK and SCR alleles. Additional evidence for this process was obtained by assaying 70 accessions for the presence of C24-or Col-0-specific sequences. Furthermore, analysis of SRK and SCR polymorphisms in these accessions argues against the occurrence of a selective sweep of a particular allele of SCR, as previously proposed.

Molecular Characterization and Evolution of Self-Incompatibility Genes inArabidopsis thaliana:The Case of theScHaplotype

“…Previous studies had shown that in some accessions, such as C24, the SRK and SCR sequences are highly decayed or deleted, and only partial remnants of these sequences have been retained . In other accessions, SRK sequences are relatively well preserved while SCR sequences are very much degraded or entirely absent (Nasrallah et al 2004;Sherman-Broyles et al 2007). For example, in SA-containing accessions, SCRA sequences are nonfunctional and may be repeated, truncated, or rearranged (Nasrallah et al 2004;Sherman-Broyles et al 2007;Boggs et al 2009a), while the SRKA gene has remained much more intact, being transcribed but encoding a truncated open reading frame due to splice site usage as in the Col-0 accession (Kusaba et al 2001;Shimizu et al 2004;Tang et al 2007), or even remaining functional as in the Wei-0 accession (Tsuchimatsu et al 2010).…”

“…The structure of the Lz-0 SC haplotype was compared to that of the previously characterized C24 SA-SC recombinant haplotype ( Figure 1B; Sherman-Broyles et al 2007), the Col-0 SA haplotype ( Figure 1C; Kusaba et al 2001), and the Cvi-0 SB haplotype ( Figure 1D; Tang et al 2007). Among these S haplotypes, the Lz-0 S haplotype has the longest PUB8-ARK3 region (.44 kb).…”

“…By contrast, for the SC haplotype, only SRK sequences, some of them encoding full-length open reading frames, are available, and neither SCRC sequences nor the corresponding A. lyrata SCR36 sequences have been isolated to date. Thus, although there is clear evidence that the SC haplotype is nonfunctional, at least in some accessions (Boggs et al 2009a), it is not known what mutations were associated with inactivation of this locus in the 11 A. thaliana accessions known to harbor the SC haplotype (Shimizu et al 2004;Sherman-Broyles et al 2007), how these mutations compare with those that inactivated the SA and SB haplotypes, and if SA-SC recombinant haplotypes have retained SCRC sequences. Thus, our view of the events that remodeled the A. thaliana S locus is incomplete.…”

“…The SRK and SCR proteins are highly polymorphic and co-evolving proteins (Sato et al 2002) and their haplotype-specific interaction is responsible for the specific recognition and inhibition by the stigma epidermis of self-related pollen (i.e., pollen derived from the same flower, other flowers on the same plant, or plants expressing the same S haplotype) (reviewed in Rea and Nasrallah 2008). Consequently, an understanding of the genetic events associated with the switch to self-fertility in the A. thaliana lineage was sought through analysis of SRK and SCR sequences harbored by various A. thaliana geographical accessions (Kusaba et al 2001;Shimizu et al 2004Shimizu et al , 2008Sherman-Broyles et al 2007;Tang et al 2007; Boggs et al 2009a,b;Tsuchimatsu et al 2010) and comparisons to orthologous sequences from A. thaliana's close self-incompatible relatives A. lyrata and A. halleri (Bechsgaard et al 2006). These comparisons have suggested that A. thaliana has retained only three of the many S haplotypes that must have Liu et al 2007;Boggs et al 2009b).…”

Molecular and Genetic Analyses of Four Nonfunctional S Haplotype Variants Derived from a Common Ancestral S Haplotype Identified in Sour Cherry (Prunus cerasus L.)

“…S locus (Sherman-Broyles et al 2007), suggesting that this element might have a widespread role in the evolution of self-compatibility.…”