Evolution of theS-Locus Region in Arabidopsis Relatives    

Abstract

The S locus, a single polymorphic locus, is responsible for self-incompatibility (SI) in the Brassicaceae family and many related plant families. Despite its importance, our knowledge of S-locus evolution is largely restricted to the causal genes encoding the S-locus receptor kinase (SRK) receptor and S-locus cysteine-rich protein (SCR) ligand of the SI system. Here, we present highquality sequences of the genomic region of six S-locus haplotypes: Arabidopsis (Arabidopsis thaliana; one haplotype), Arabidopsis lyrata (four haplotypes), and Capsella rubella (one haplotype). We compared these with reference S-locus haplotypes of the selfcompatible Arabidopsis and its SI congener A. lyrata. We subsequently reconstructed the likely genomic organization of the S locus in the most recent common ancestor of Arabidopsis and Capsella. As previously reported, the two SI-determining genes, SCR and SRK, showed a pattern of coevolution. In addition, consistent with previous studies, we found that duplication, gene conversion, and positive selection have been important factors in the evolution of these two genes and appear to contribute to the generation of new recognition specificities. Intriguingly, the inactive pseudo-S-locus haplotype in the self-compatible species C. rubella is likely to be an old S-locus haplotype that only very recently became fixed when C. rubella split off from its SI ancestor, Capsella grandiflora.

The ARC1 E3 Ligase Promotes Two Different Self-Pollen Avoidance Traits inArabidopsis

“…A. thaliana is an excellent model system for investigating factors required for restoring self-incompatibility as most ecotypes carry pseudogenes for both SCR and SRK (Kusaba et al, 2001;Bechsgaard et al, 2006;Tang et al, 2007;Shimizu et al, 2008;Boggs et al, 2009a;Tsuchimatsu et al, 2010;Guo et al, 2011), and ARC1 has been deleted (Kitashiba et al, 2011;Indriolo et al, 2012). Previous studies on the restoration of self-incompatibility in A. thaliana with functional SCR and SRK produced varying results with some ecotypes remaining fully selfcompatible, while other ecotypes displayed varying degrees of the self-incompatibility phenotype, but the self-pollen rejection response was incomplete and still produced some seeds (Nasrallah et al, 2004;Boggs et al, 2009a;Tsuchimatsu et al, 2010).…”

“…thaliana is a self-compatible species, and while some A. thaliana ecotypes still carry an intact SCR or SRK gene, the majority have been shown to carry nonfunctional SCR and SRK genes; this loss was hypothesized to be a key part of the transition to selfing from self-incompatibility (Kusaba et al, 2001;Bechsgaard et al, 2006;Tang et al, 2007;Shimizu et al, 2008;Boggs et al, 2009a;Tsuchimatsu et al, 2010;Guo et al, 2011). Previous work into the reconstruction of the self-incompatibility signaling pathway in A. thaliana with functional SCR and SRK genes has shown mixed results with considerable variability in the strength and stability of the self-incompatibility responses (Nasrallah et al, 2004;Boggs et al, 2009aBoggs et al, , 2009bTsuchimatsu et al, 2010).…”

Signaling Events in Pollen Acceptance or Rejection in the Arabidopsis Species

“…thaliana is a self-compatible species that has lost its self-incompatibility system by the pseudogenization of the SCR/SP11 and SRK genes (Kusaba et al 2001 ;Bechsgaard et al 2006 ;Tang et al 2007 ;Shimizu et al 2008 ;Guo et al 2011 ). As A. thaliana is easily transformed, a number of studies have reintroduced the SCR/ SP11 or SRK genes from other Brassicaceae species in an attempt to reintroduce the self-incompatibility trait (Bi et al 2000 ;Nasrallah et al 2002 ).…”

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

“…For example, genes controlling sporophytically controlled self-incompatibility (SI) in plants have been found to be missing from resequencing assemblies because they are too divergent from the reference genome and so trawling in the unassembled reads is necessary to characterize these highly polymorphic genes (Mable et al, 2017). Both male and female components are members of large gene families that show extensive trans-specific polymorphism, with highly similar alleles shared across species and even genera but high divergence between functional specificities (Schierup et al, 1998;Paetsch et al, 2006;Castric and Vekemans, 2007;Busch et al, 2008;Guo et al, 2011;Tedder et al, 2011;Leducq et al, 2014). The gene controlling female specificity (S-receptor kinase, SRK) is part of a large family of receptor kinases, which evolved through a complex history of gene duplication and loss, followed by gene fission and fusion (Xing et al, 2013).…”

“…The gene controlling female specificity (S-receptor kinase, SRK) is part of a large family of receptor kinases, which evolved through a complex history of gene duplication and loss, followed by gene fission and fusion (Xing et al, 2013). Gene conversion between SRK and other members of the gene family is also thought to have contributed to expansion of functional allelic diversity (Prigoda et al, 2005;Guo et al, 2011). This creates additional challenges with interpreting which variants are parts of the functional locus regulating the SI response and which are functionally unlinked but show high sequence similarity.…”