Rethinking convergence in plant parasitism integrating molecular and population genetic processes

The need for photosynthesis has largely shaped the body plan, physiology, as well as gene repertoire of seed plants. However, shifts to a heterotrophic lifestyle have independently evolved twelve times in more than four thousand parasitic plants. Among these parasites, otherwise rare features have evolved repetitively at both the molecular and phenotypical levels, including reduced vegetative body, carrion mimicking, and abundant alien genetic materials. Here, I propose an integrated conceptual model to describe the general evolutionary trajectory of parasitic plants and provide a mechanistic explanation for their convergent evolution. This model connects our empirical understanding of the plants’ regulatory network with classic theories in molecular and population genetics. It emphasizes the cascading effects driven by the loss of photosynthesis as one major force shaping the genomic landscape of parasitic plants. In this paper, I review recent studies in the anatomy, physiology, and genetics of parasitic plants to support the photosynthesis-centered hypothesis of their convergent evolution. Focusing on non-photosynthetic holoparasites, I elucidate how they inevitably reach an evolutionary terminal status and highlight the utility of an explicitly described, falsifiable model for future studies in parasitic plants.