Fine-Mapping and Comparative Genomic Analysis Reveal the Gene Composition at theSandZSelf-incompatibility Loci in Grasses

Abstract

Self-incompatibility (SI) is a genetic mechanism of hermaphroditic plants to prevent inbreeding after self-pollination. Allogamous Poaceae species exhibit a unique gametophytic SI system controlled by two multi-allelic and independent loci, S and Z. Despite intense research efforts in the last decades, the genes that determine the initial recognition mechanism are yet to be identified. Here, we report the fine-mapping of the Z-locus in perennial ryegrass (Lolium perenne L.) and provide evidence that the pollen and stigma components are determined by two genes encoding DUF247 domain proteins (ZDUF247-I and ZDUF247-II) and the gene sZ, respectively. The pollen and stigma determinants are located side-by-side and were genetically linked in 10,245 individuals of two independent mapping populations segregating for Z. Moreover, they exhibited high allelic diversity as well as tissue-specific gene expression, matching expected characteristics of SI determinants known from other systems. Revisiting the S-locus using the latest high-quality whole-genome assemblies revealed a similar gene composition and structure as found for Z, supporting the hypothesis of a duplicated origin of the two-locus SI system of grasses. Ultimately, comparative genomic analyses across a wide range of self-compatible and self-incompatible Poaceae species revealed that the absence of a functional copy of at least one of the six putative SI determinants is accompanied by a self-compatible phenotype. Our study provides new insights into the origin and evolution of the unique gametophytic SI system in one of the largest and economically most important plant families.

Molecular insights into self-incompatibility systems: From evolution to breeding

“…The downstream reaction upon pollen–stigma interaction in grass appears to involve Ca 2+ signal transduction, protein phosphorylation, and proteolysis pathways ( Yang et al., 2008 ; Klaas et al., 2011 ; Chen et al., 2019b ). Comparative genomic analysis suggested a duplicated origin of the grass SI system owing to the similar gene composition and structure of the S- locus and Z -locus, and the high synteny between these two loci in the Poaceae tribe supported the hypothesis that grasses share the same SI determinants ( Rohner et al., 2023 ). Fine-mapping and comparative studies identified two DUF247 family genes ( SDUF247-I and SDUF247-II ) and an sS gene as the male and female determinants, respectively, at the S -locus ( Manzanares et al., 2016 ).…”

“…The GSI system is controlled by two multiple-allelic loci, S and Z ( Li et al., 1997 ). Each locus contains two male and one female determinant, and SI occurs when the pollen S - and Z - genotypes are identical to the corresponding pistil genotypes ( Rohner et al., 2023 ). The downstream reaction upon pollen–stigma interaction in grass appears to involve Ca 2+ signal transduction, protein phosphorylation, and proteolysis pathways ( Yang et al., 2008 ; Klaas et al., 2011 ; Chen et al., 2019b ).…”

“…Fine-mapping and comparative studies identified two DUF247 family genes ( SDUF247-I and SDUF247-II ) and an sS gene as the male and female determinants, respectively, at the S -locus ( Manzanares et al., 2016 ). Likewise, pollen and stigma components are determined by two DUF247 family genes ( ZDUF247-I and ZDUF247-II ) and the sZ gene at the Z -locus ( Rohner et al., 2023 ). Two linked glycerol kinase-like genes ( LpGK1 and LpGK2 ) were reported as Z -candidates, but further validation experiments remain to be performed ( Studer and Torben, 2014 ).…”

Environmental influence on reproductive traits of buffel grass facultative apomictic genotypes and its implication in plant breeding

“…Self-incompatibility is a genetic mechanism of hermaphroditic plants to prevent inbreeding after selfpollination (Rohner et al, 2023) and has significant effects on population structure, potential diversification, and evolutionary consequences (Yang et al, 2008). This trait is frequently estimated as the seed set of randomly selected OP and SP panicles (Acuña et al, 2007(Acuña et al, , 2009Conde-Lozano et al, 2011;Hignight et al, 1991;Shafer et al, 2000).…”

The diallelic self-incompatibility system in Oleaceae is controlled by a hemizygous genomic region expressing a gibberellin pathway gene

“…The conservation of a single gene is striking, as to our knowledge all SI systems so far elucidated at the molecular level entail the action of at least two separate genes, determining the male and female specificities, respectively (Fujii et al 2016, Rohner et al 2023). These determinants vary greatly in the molecular functions they encode (Broz and Bedinger 2021) and in their level of repetition, with the male determination being, for example, spread across multiple tandemly duplicated paralogs in Solanaceae (Kubo et al 2015).…”