Genome-wide signatures of coevolution in parasitic and autotrophic plants

Abstract

Parasitism has repeatedly evolved in flowering plants, resulting in convergent genomic, metabolic, and morphological adaptations. Evolutionary Rate Covariation (ERC) analysis is a phylogenomic method used to uncover gene pairs whose functional interactions are under shared selection pressures. In this study, we applied the ERCnet pipeline to a paired sample of parasites and autotrophic relatives to investigate patterns of gene coevolution common to trophic mode transitions. Few networks of genes sharing ERC exhibited trophic-mode-driven differences in evolutionary rates, suggesting divergent selection pressures on shared interactions. Gene Ontology (GO) analysis yielded underrepresentation of plastid-related genes in coevolving networks. Meanwhile, two smaller networks highlighted the slow evolution of developmental and fatty acid metabolism genes in parasites. Covarying genes involved in the WUSCHEL/CLAVATA3 (WUS/CLV3) signaling pathway, key to shoot development, evolved slowly in parasites, implicating them in body plan reorganization. Additionally, genes involved in fatty acid metabolism were overrepresented in a slow-evolving parasite cluster, hinting at parasite dependence on conserving this pathway while losing photosynthetic plastid functions. These results indicate conservation of gene coevolution patterns between the two trophic modes, with a few notable exceptions. Expanding ERC analysis of parasitic plants to include more species could provide greater insight into divergent and conserved networks of gene interactions.