Bocheng Guo

S-RNases are essential in the gametophytic self-incompatibility (GSI) system of many flowering plants, where they act as stylar-S determinants. Despite their prominence, the syntenic genomic origin and evolutionary trajectory of S-RNase genes in eudicots have remained largely unclear. Here, we performed large-scale phylogenetic and microsynteny network analyses of T2 RNase genes across 130 angiosperm genomes, encompassing 35 orders and 56 families. S-like RNase genes in Cucurbitaceae species phylogenetically grouped with functionally characterized S-RNases in various species. Additionally, Cucurbitaceae S-like RNase genes showed conserved synteny with Class I T2 RNase genes. From this, we inferred that the well-characterized S-RNase genes (belonging to Class III-A genes) and Class I T2 RNase genes (located on duplicated genomic blocks) likely derived from the gamma triplication event shared by core eudicots. Additionally, we identified frequent lineage-specific gene transpositions of S-RNases and S-like RNases across diverse angiosperm lineages, including Rosaceae, Solanaceae, and Rutaceae families, accompanied by a significant increase in transposable element activity near these genes. Our findings delineate the genomic origin and evolutionary path of eudicot S-RNase genes, enhancing our understanding of the evolution of the S-RNase-based GSI system.

Nucleotide-binding leucine-rich repeat receptor (NLR) genes encode a pivotal class of plant immune receptors. However, their rampant duplication and loss have made inferring their genomic evolutionary trajectory difficult, exemplified by the loss of TNL family genes in monocots. In this study, we introduce a novel classification system for angiosperm NLR genes, grounded in network analysis of microsynteny information. This refined classification categorizes these genes into five classes: CNL_A, CNL_B, CNL_C, TNL, and RNL. Compared to the previous classification, we further subdivided CNLs into three subclasses. The credibility of this classification is supported by phylogenetic analysis and examination of protein domain structures. Importantly, this classification enabled a model to explain the extinction of TNL genes in monocots. Compelling microsynteny evidence underscores this revelation, indicating a clear synteny correspondence between the non-TNLs in monocots and the extinct TNL subclass. Our study provides crucial insights into the genomic origin and divergence of plant NLR subfamilies, unveiling the malleability-driven journey that has shaped the functionality and diversity of plant NLR genes.

S-RNases are essential in the gametophytic self-incompatibility (GSI) system of many flowering plants, where they act as stylar-S determinants. Despite their significance, the syntenic genomic origin and evolutionary trajectory of S-RNase genes in eudicots have remained largely unclear. Here, we performed large-scale phylogenetic and microsynteny network analyses of RNase T2 genes across 130 angiosperm genomes, encompassing 35 orders and 56 families. Based on the connections observed in the synteny network, particularly the persisting synteny block in none-SI Cucurbitaceae species, we infer that well-characterized S-RNase genes (Class III-A RNase genes) were duplicated and evolved from Class I S-like RNase genes, possibly as a result of the gamma triplication event shared by core eudicots. Additionally, we identified frequent lineage-specific gene transpositions of S-RNase genes across diverse angiosperm lineages, including Rosaceae, Solanaceae, and Rutaceae families, accompanied by a significant increase in transposable element (TE) activity near these genes. Our findings delineate the precise genomic origin and evolutionary path of eudicot S-RNase genes, enhancing our understanding of the evolution of the S-RNase-based GSI system.

Transposable elements (TEs) exert significant influence on plant genomic structure and gene expression. Here, we explored TE-related aspects across 14 Rosaceae genomes, investigating genomic distribution, transposition activity, expression patterns, and nearby differentially expressed genes (DEGs). Analyses unveiled distinct long terminal repeat retrotransposon (LTR–RT) evolutionary patterns, reflecting varied genome size changes among nine species over the past million years. In the past 2.5 million years, Rubus idaeus showed a transposition rate twice as fast as Fragaria vesca, while Pyrus bretschneideri displayed significantly faster transposition compared with Crataegus pinnatifida. Genes adjacent to recent TE insertions were linked to adversity resistance, while those near previous insertions were functionally enriched in morphogenesis, enzyme activity, and metabolic processes. Expression analysis revealed diverse responses of LTR–RTs to internal or external conditions. Furthermore, we identified 3695 pairs of syntenic DEGs proximal to TEs in Malus domestica cv. ‘Gala’ and M. domestica (GDDH13), suggesting TE insertions may contribute to varietal trait differences in these apple varieties. Our study across representative Rosaceae species underscores the pivotal role of TEs in plant genome evolution within this diverse family. It elucidates how these elements regulate syntenic DEGs on a genome-wide scale, offering insights into Rosaceae-specific genomic evolution.