The Origin and Evolution of RNase T2 Family and Gametophytic Self-incompatibility System in Plants

Abstract

Ribonuclease (RNase) T2 genes are found widely in both eukaryotes and prokaryotes, and genes from this family have been revealed to have various functions in plants. In particular, S-RNase is known to be the female determinant in the S-RNase-based gametophytic self-incompatibility system. However, the origin and evolution of the RNase T2 gene family and gametophytic self-incompatibility system are not well understood. In this study, 785 RNase T2 genes were identified in 81 sequenced plant genomes representing broad-scale diversity, and divided into three subgroups (Class I, II, and III) based on phylogenetic and synteny network analysis. Class I was found to be of ancient origin and to emerge in green algae, Class II was shown to originate with the appearance of angiosperms, while Class III was discovered to be eudicot-specific. Each of three major classes could be further classified into several subclasses of which some subclasses were found to be lineage-specific. Furthermore, duplication, deletion, or inactivation of the S/S-like-locus was revealed to be linked to repeated loss and gain of self-incompatibility in different species from distantly related plant families with gametophytic self-incompatibility. Finally, the origin and evolutionary history of S-locus in Rosaceae species was unraveled with independent loss and gain of S-RNase occurred in different subfamilies of Rosaceae. Our findings provide insights into the origin and evolution of the RNase T2 family and the gametophytic self-incompatibility system in plants.

The Snapdragon Genomes Reveal the Evolutionary Dynamics of the S-Locus Supergene

“…Sequence analyses of the S -genes have been extensively conducted in Solanaceae and Rosaceae ( McClure 2004 ; Williams et al 2014 ; Kubo et al 2015 ; Wu et al 2020 ; Vieira et al 2021 ; Lv et al 2022 ); however, similar studies on Plantaginaceae species are still limited ( Lai et al 2002 ; Qiao et al 2004 ). Prior this work, the first S C -haplotype of cultivar A. majus , which conferred self-compatibility due to loss of S-RNase , has been reported ( Li et al 2019 ).…”

“…Still, the timing of origination of S-RNase is undetermined, which were given to the following two possible explanations: (1) RNase emerged as an S -gene before the diversification of eudicots, and subsequent gene loss (e.g., C. alba scaffold124) or translocation ( P. pubescens Chr03) of S-RNase occurred in many evolutionary entities, and (2) RNase have not come into tight linkage with incipient SLFs to form a functional S -locus which controlled self-incompatibility in the common ancestor of eudicots until the divergence of Plantaginaceae species. By comparing Ks values of ancient SLFs and S-RNase in Rosoideae species, Lv et al concluded that ancestral SLFs originated before the split of grape and Rosaceae ancestor and after the split, the ancestral S-RNase emerged in the Rosaceae common ancestor ( Lv et al 2022 ). Based on these results and principle of parsimony, hypothesis (1) would be the most plausible model to illustrate the origin and evolution of the S -locus supergene.…”

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

“…The increasing number of available plant genomes provides an opportunity to resolve the evolutionary relationships of the RNase T2 gene family and the origin of S -RNase SI on a broad scale. A study based on phylogenetics, syntenic analyses, and identification of whole gene duplication (WGD) events revealed that lineage-specific WGD resulted in expansion of the RNase T2 family ( Lv et al. 2022 ).…”

“…Loss of S -RNase GSI is caused mainly by inactivation, deletion, or duplication of S -loci rather than defects in S -RNase alone, possibly due to additional functions of S -RNase beyond its role in SI ( Zhao et al., 2022 ). Phylogenetic studies have classified T2-RNases into three clades (class I, class II, class III); all functional and predicted S -RNases are members of the class III T2-RNase clade and are found exclusively in eudicots ( Ramanauskas and Igic, 2017 ; Lv et al., 2022 ). Although there is evidence that an ancestral state of tightly linked pollen and pistil components may have existed prior to the eudicots, a genome study of pineapple ( Ananas comosus ) revealed that an RNase T2 family gene was closely linked to several F-box-associated genes ( Chen et al., 2019a ).…”

Comparative stigmatic transcriptomics reveals self and cross pollination responses to heteromorphic incompatibility in Plumbago auriculata Lam.

“…Notably, GSI systems and homomorphic systems have been studied more extensively than heteromorphic systems ( McCubbin, 2008 ). Studies have reported that in Solanaceae, Rosaceae and Plantaginaceae, GSI is based on the SLF ( SFB )/ SRNase system, and in Brassicaceae SSI is based on the SP11 ( SCR )/ SRK system ( Lv et al, 2022 ; Goring et al, 2023 ). Significant advancements have been made in comprehending the molecular foundation of HetSI, particularly in Primula and Fagopyrum ( Banović et al, 2010 ; Li et al, 2023 ).…”