A new genetic locus for self-compatibility in the outcrossing grass species perennial ryegrass (Lolium perenne)

Abstract

Background Self-incompatibility (SI) is a physiological mechanism that many flowering plants employ to prevent self-fertilization and maintain heterozygosity. In the grass family this is known to be controlled by a two locus (S-Z) system; however, the SI system is intrinsically leaky. Modifier genes of both the S and Z loci and a further locus, T, are known to override SI leading to self-fertilization and self-seed production. This has implications for the ecological and evolutionary success as well as the commercial breeding of grasses. Here we report a study where the genetic control of self-compatibility (SC) was determined from the results of self-pollinating an F2 population of perennial ryegrass from two independently derived inbred lines produced by single-seed descent. Methods In vitro self-pollinations of 73 fertile plants were analysed. A genetic association analysis was made with a panel of 1863 single-nucleotide polymorphism (SNP) markers, generated through genotype-by-sequencing methodology. Markers were placed on a recombination map of seven linkage groups (LGs) created using Joinmap v.5. The seed set on self- and open-pollinated inflorescences was determined on 143 plants, including the 73 plants analysed for self-pollination response. Key Results Self-pollinations revealed a bimodal distribution of percentage SC with peaks at 50 and 100 %. A single quantitative trait locus (QTL) was identified with peak association for marker 6S14665z17875_11873 that mapped to LG 6. Peak position was associated with maximum marker segregation distortion. The self-compatible plants were equally fecund after self- and open pollination. Conclusions This is the first report in the Poaceae family of an SC locus located on LG 6. This new SC QTL discovery, as well as indicating the complex nature of the pollen–stigma recognition process and its evolutionary significance, provides an additional source of SC for breeding perennial ryegrass.

Identification of candidate genes for self-compatibility in perennial ryegrass (Lolium perenneL.)

“…In our population, male gametes in the F 1 plants carrying the non-SC allele are not transmitted to the F 2 generation, causing a distorted segregation of markers linked to the SC causal gene. This has also been demonstrated recently by Slatter et al (2020), where the QTL underlying the SC locus on LG 6 in perennial ryegrass overlapped with maximum marker segregation distortion. This has relevant implications for future studies aimed at discovering novel SC sources, as the identification of distorted regions can be used as a strategy to map their position in the genome.…”

“…In our population, male gametes in the F 1 plants carrying the non-SC allele are not transmitted to the F 2 generation, causing a distorted segregation of markers linked to the SC causal gene. This has also been demonstrated recently by Slatter et al (2020), where the QTL underlying the SC locus on…”

“…Mutations in loci non-allelic to S and Z can also lead to SC, by interrupting the downstream cascade triggered by the initial self-recognition (Do Canto et al 2016). Such putative mutations have been found in rye ( Secale cereale L.) and perennial ryegrass (Voylokov et al 1993; Egorova et al 2000; Thorogood et al 2005; Arias-Aguirre et al 2013, Do Canto et al 2018; Slatter et al 2020). A detailed molecular understanding of how SC arises in SI grasses is lacking, but several studies have acknowledged that calcium (Ca 2+ ) signaling plays an essential role in the recognition and/or inhibition of self-pollen (Yang et al 2009; Chen et al 2019).…”

Characterization and practical use of self-compatibility in outcrossing grass species

“…Genes underlying these loci likely have a function in the downstream cascade following the initial pollen–stigma recognition mediated by S and Z ( Do Canto et al , 2016 ). The most recent studies on non- S or non- Z sources of SC identified two genetically independent loci on LG 5 ( Arias-Aguirre et al , 2013 ; Do Canto et al , 2018 ; Cropano et al , 2021 ) and LG 6 ( Slatter et al , 2020 ) in two unrelated perennial ryegrass F 2 populations segregating for SC. In both populations, using in vitro self-pollinations ( Fig.…”

Review: evolutionary drivers of agricultural adaptation in Lolium spp.

“…Thus, differences in reproduction success rate may be dependent on the direction of reciprocal crosses and the degree of compatibility between individuals. Additional loci may be involved in the gametophytic self‐incompatibility system in Lolium spp., 12 thus the complexity of the gametophytic self‐incompatibility mating system in Lolium spp. remains unclear.…”