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 (GSI) system. However, the origin and evolution of the RNase T2 gene family and GSI 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 the 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 GSI. 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 GSI system in plants.

Keywords: S-locus; RNase T2 family; evolution; gametophytic self-incompatibility; phylogeny.

Fig. 1.

Phylogeny, genome information, and RNase T2 genes of 81 plant species. The taxonomic information and genome features of each species are presented. The total number of RNase T2 genes and the number in each class are shown for each species. C.N., haploid chromosome number (n); P.L., ploidy level; G.S., 1C genome size in megabase pairs (Mb). Information about genome size was obtained from the Plant DNA C-values Database (https://cvalues.science.kew.org/search).

Fig. 2.

Phylogeny of RNases T2 family genes in 81 plants. The phylogenetic tree was constructed using IQ-TREE with the maximum-likelihood method and visualized using iTOL v6.3. The bootstrap was set to 1,000 replicates. Tip labels have been omitted for clarity. The RNase T2 genes were divided into three major classes (Class I, II, and III). S-RNase genes within Class III are indicated in five families with GSI, including the Rubiaceae, Plantaginaceae, Solanaceae, Rutaceae, and two genera of Rosaceae (Amygdaleae and Maleae). Support values of each branch are contained in supplementary figure S2, Supplementary Material online.

Fig. 3.

Synteny network of RNases T2 family genes and syntenic relationships within and between three classes of genes. (A) The synteny network of RNase T2 family genes. Communities were rendered based on the clique percolation method at k = 3. The size of each node indicates the number of connected edges (node degree). The communities are denoted by the three classes (Class I, II, and III) involved. (B) Syntenic relationships among the RNase T2 genes within the phylogenetic tree. Each connecting line located inside the inverted circular gene tree indicates a syntenic relationship between two RNase T2 genes. Lineage information was contained in the branch.

Fig. 4.

The number and percentage of RNase T2 gene pairs derived from different modes of gene duplication in 81 plant species. (A) Taxonomy tree of 81 plant species. (B) Number of duplicated gene pairs. Five modes of duplicated RNase T2 gene pairs were identified, and the different colored bars represent the different modes of gene duplication. WGD, whole-genome duplication; TD, tandem duplication; PD, proximal duplication; TRD, transposed duplication; DSD, dispersed duplication. (C) Percentage of duplicated gene pairs.

Fig. 5.

The S-/S-like loci annotated in species from five plant families with GSI and the evolutionary routes for the loss and regain of SI. (A) The evolutionary routes proposed to illustrate the loss and regain of SI. The loss of SI may be caused by duplication (I), deletion (b), reactivation (c), or mutation (d), while the regain of SI may be due to inactivation (a) or deletion of the S-like-locus (e). The solid-color rectangles and ovals represent SLF/S-like SLF and S-/S-like-RNase genes involved in GSI. (B) Annotated S-/S-like loci composed of S-/S-like-RNases and F-box/FBA genes in 22 angiosperm species from five plant families with GSI systems. The species with SC are highlighted with a gray background. Two and three stars indicate WGD and whole-genome triplication, respectively. The “Routes” (numbers and letters) correspond to the evolutionary processes depicted in (A). This figure was inspired by a previous study (Zhao et al. 2021b).

Fig. 6.

The origin and evolutionary history of the S-locus in Rosaceae. (A) Microsynteny relationships of the S-locus region in strawberry and homologous segments in Amygdaleae and Maleae species. The arrows indicate S-RNases. (B) Microsyntenic relationships between the S-locus region in strawberry and homologous segments in other species from Amygdaleae, Maleae, and Vitaceae. (C) Microsyntenic relationships between the S-locus region in pear and syntenic regions in other species of Rosaceae. (D) Microsyntenic relationships between the extended segment on peach Chr 3 and syntenic regions in pear and apple. (E) The evolutionary model proposed to illustrate the origin and diversified evolution of the S-locus in Rosaceae. (F) Boxplot of K_S distributions between S-locus genes (S-RNases and SLFs) and its closest paralog calculated in Rosaceae species.