Homology-Based Interactions between Small RNAs and Their Targets Control Dominance Hierarchy of Male Determinant Alleles of Self-Incompatibility in Arabidopsis lyrata

Abstract

Self-incompatibility (SI) is conserved among members of the Brassicaceae plant family. This trait is controlled epigenetically by the dominance hierarchy of the male determinant alleles. We previously demonstrated that a single small RNA (sRNA) gene is sufficient to control the linear dominance hierarchy in Brassica rapa and proposed a model in which a homology-based interaction between sRNAs and target sites controls the complicated dominance hierarchy of male SI determinants. In Arabidopsis halleri, male dominance hierarchy is reported to have arisen from multiple networks of sRNA target gains and losses. Despite these findings, it remains unknown whether the molecular mechanism underlying the dominance hierarchy is conserved among Brassicaceae. Here, we identified sRNAs and their target sites that can explain the linear dominance hierarchy of Arabidopsis lyrata, a species closely related to A. halleri. We tested the model that we established in Brassica to explain the linear dominance hierarchy in A. lyrata. Our results suggest that the dominance hierarchy of A. lyrata is also controlled by a homology-based interaction between sRNAs and their targets.

A haplotype-resolved chromosome-level assembly and annotation of European hazelnut (C. avellanacv. Jefferson) provides insight into mechanisms of eastern filbert blight resistance

“…Indeed, of the eighteen genes identified as PIX7 or MDIS-1 homologs, all were variable in total length (Table 3). Recent studies have shown that in Brassica , the most well characterized SSI system, a small RNA is crucial for inducing methylation of recessive SI allele, in order to induce compatibility (Yasuda et al, 2021). When considering the large number of SI-alleles in Corylus (33 to date), it is possible that unannotated sRNA(s) are acting upon different variants of PIX7 or MIK2 to establish allelic dominance.…”

“…Indeed, of the eighteen genes identified as PIX7 or MDIS-1 homologs, all were variable in total length (Table 3). Recent studies have shown that in Brassica, the most well characterized SSI system, a small RNA is crucial for inducing methylation of recessive SI allele, in order to induce compatibility (Yasuda et al, 2021).…”

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

“…Studies on Brassica and Arabidopsis have revealed that this dominance hierarchy is determined by small RNAs (sRNAs) linked to the S -locus ( Tarutani et al., 2010 ; Durand et al., 2014 ). This role of sRNAs in controlling the dominance hierarchy of male SI determinants appears to be conserved in Brassicaceae ( Yasuda et al., 2021 ). In Brassica , SP11 methylation inducer ( Smi1 ) was found to induce DNA methylation of the recessive class II SP11/SCR promoter to regulate monoallelic gene silencing during dominant–recessive interactions ( Shiba et al., 2006 ; Tarutani et al., 2010 ).…”

“…Two polymorphic sRNAs, AlSmi1 and AlSmi2 , were suggested to control the dominance hierarchy of A . lyrata , and their predicted targets were as follows: class IV > class III > class II > class I ( Yasuda et al., 2021 ). Further analysis of interactions between sRNAs and their target sites in other SI species should provide more information on dominance–recessiveness mechanisms in Brassicaceae ( Fujii and Takayama, 2018 ; Duan et al., 2023 ).…”

Dominance in self-compatibility between subgenomes of allopolyploid Arabidopsis kamchatica shown by transgenic restoration of self-incompatibility

“…The molecular mechanism of male dominance has been revealed by transgenic experiments in diploid species 33 . sRNAs from a dominant S -haplogroup at the S -locus regulate the tissue-specific methylation of the SCR gene of a recessive S -haplogroup, thereby suppressing its expression and function 28 , 30 – 32 . In natural allotetraploid species in Brassicaceae, sequencing and crossing experiments suggested the relevance of dominance in self-compatibility 2 , 11 , 19 .…”