Rethinking convergence in plant parasitism through the lens of molecular and population genetic processes

Abstract

The autotrophic lifestyle of photosynthetic plants has profoundly shaped their body plan, physiology, and gene repertoire. Shifts to parasitism and heterotrophy have evolved at least 12 times in more than 4000 species, and this transition has consequently left major evolutionary footprints among these parasitic lineages. Features that are otherwise rare at the molecular level and beyond have evolved repetitively, including reduced vegetative bodies, carrion‐mimicking during reproduction, and the incorporation of alien genetic material. Here, I propose an integrated conceptual model, referred to as the funnel model, to define the general evolutionary trajectory of parasitic plants and provide a mechanistic explanation for their convergent evolution. This model connects our empirical understanding of gene regulatory networks in flowering plants with classical theories of molecular and population genetics. It emphasizes that the cascading effects brought about by the loss of photosynthesis may be a major force constraining the physiological capacity of parasitic plants and shaping their genomic landscapes. Here I review recent studies on the anatomy, physiology, and genetics of parasitic plants that lend support to this photosynthesis‐centered funnel model. Focusing on nonphotosynthetic holoparasites, I elucidate how they may inevitably reach an evolutionary terminal status (i.e., extinction) and highlight the utility of a general, explicitly described and falsifiable model for future studies of parasitic plants.

Plastid genome evolution in leafless members of the orchid subfamily Orchidoideae, with a focus onDegranvillea dermaptera

“…Leafless, heterotrophic plants provide opportunities to study the genomic consequences of extreme changes in nutritional mode, morphology, physiology, ecology, and evolutionary trajectories (e.g. Bidartondo, 2005; Westwood et al, 2010; Wickett et al, 2014; Těšitel, 2016; Twyford, 2018; Wicke and Naumann, 2018; Yuan et al, 2018; Cai, 2023; Sanchez-Puerta et al, 2023; Timilsena et al, 2023). Plastid genomes have been the focus of intense research over the past few decades, due to their high copy number per cell, relatively small sizes (kilobases for plastomes vs. megabases for nuclear genomes), role in photosynthetic function, and ease with which they can be sequenced via high-throughput technologies (Wicke et al, 2011; Jansen and Ruhlman, 2012; Ruhlman and Jansen, 2014; Twyford and Ness, 2017; Doyle, 2022).…”