Abstract
Self-incompatibility (SI) is a mechanism that many flowering plants employ to prevent fertilisation by self- and self-like pollen ensuring heterozygosity and hybrid vigour. Although a number of single locus mechanisms have been characterised in detail, no multi-locus systems have been fully elucidated. Historically, examples of the genetic analysis of multi-locus SI, to make analysis tractable, are either made on the progeny of bi-parental crosses, where the number of alleles at each locus is restricted, or on crosses prepared in such a way that only one of the SI loci segregates. Perennial ryegrass (Lolium perenne L.) possesses a well-documented two locus (S and Z) gametophytic incompatibility system. A more universal, realistic proof of principle study was conducted in a perennial ryegrass population in which allelic and non-allelic diversity was not artificially restricted. A complex pattern of pollinations from a diallel cross was revealed which could not possibly be interpreted easily per se, even with an already established genetic model. Instead, pollination scores were distilled into principal component scores described as Compatibility Components (CC1-CC3). These were then subjected to a conventional genome-wide association analysis. CC1 associated with markers on linkage groups (LGs) 1, 2, 3, and 6, CC2 exclusively with markers in a genomic region on LG 2, and CC3 with markers on LG 1. BLAST alignment with the Brachypodium physical map revealed highly significantly associated markers with peak associations with genes adjacent and four genes away from the chromosomal locations of candidate SI genes, S- and Z-DUF247, respectively. Further significant associations were found in a Brachypodium distachyon chromosome 3 region, having shared synteny with Lolium LG 1, suggesting further SI loci linked to S or extensive micro-re-arrangement of the genome between B. distachyon and L. perenne. Significant associations with gene sequences aligning with marker sequences on Lolium LGs 3 and 6 were also identified. We therefore demonstrate the power of a novel association genetics approach to identify the genes controlling multi-locus gametophytic SI systems and to identify novel loci potentially involved in already established SI systems.
Highlights
Many flowering plants possess self-incompatibility (SI) mechanisms that prevent inbreeding by blocking fertilisation of ovules by self or self-like pollen
We examined the simplest known example of a multi-locus SI system, the grass system, which is known to be controlled gametophytically by at least two unlinked complementary loci
A novel approach was used where a complex pattern of pollination scores was distilled from a diallel cross of a perennial ryegrass population into principal components for which we coined the phrase “Compatibility Components”
Summary
Many flowering plants possess self-incompatibility (SI) mechanisms that prevent inbreeding by blocking fertilisation of ovules by self or self-like pollen. These mechanisms have evolved independently several times and a number of different plant family-specific systems have been described (FranklinTong, 2008). Even though the mode of action of SI in grasses was reported 60 years ago (Hayman, 1956; Lundqvist, 1956) and confirmed in perennial ryegrass (Lolium perenne L.) (Cornish et al, 1979), the identity of the genes has remained elusive despite efforts to map and clone them (Voylokov et al, 1998; Thorogood et al, 2002; Bian et al, 2004; Hackauf and Wehling, 2005; Kakeda et al, 2008; Shinozuka et al, 2010). Thorogood et al (2002) described a locus on LG 3 that acted epistatically where pollen-specific S allele—LG 3 marker allele combinations from a cross between two unrelated plants were not transmitted to their progeny
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