A reference genome and transcriptome of haustorial development in Pedicularis groenlandica reveal diverse trajectories of haustoria-associated gene evolution in parasitic plants.

Abstract

BACKGROUND AND AIMS: Novel traits frequently evolve by co-opting existing genetic pathways through either the direct repurposing of existing genes or neofunctionalization of duplicated genes. Parasitism represents a major innovation in plants, in which a novel organ, the haustorium, evolved to penetrate hosts to extract water and nutrients. Previous studies hypothesized that haustoria-associated genes evolved primarily from root and pollen-associated pathways by neofunctionalization following genome duplications. METHODS: To examine the evolutionary origins of haustoria-associated genes, we generated a chromosome-scale reference genome of the hemiparasite Pedicularis groenlandica (Orobanchaceae) and sampled transcriptomes throughout haustorial development. We identified haustoria-associated genes; quantified the expression of these genes and their paralogues across non-haustorial tissues; and investigated overlap in haustoria-associated genes with publicly available haustorial transcriptomes in four additional parasitic plants. KEY RESULTS: We identified 5635 haustoria-associated genes in P. groenlandica. A greater proportion of these genes were associated with pollen tubes (67 %) than with roots (33 %), evidenced by being either differentially expressed in pollen tubes or nested within pollen tube-associated gene families, or both. Haustoria-associated genes with paralogues that arose after the evolution of parasitism in Orobanchaceae are more likely to be uniquely expressed in haustoria, consistent with neofunctionalization. CONCLUSIONS: Our results support evidence of both pleiotropy and neofunctionalization as mechanisms by which genetic pathways are co-opted for haustorial function. Haustoria-associated genes are highly lineage specific, highlighting a dynamic and ongoing process of independent haustorial co-option of gene functions among parasitic plant lineages.