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Plastid genome evolution in partially and fully mycoheterotrophic eudicots Darby, Hayley


Plastid-genome evolution following photosynthesis loss is characterized by substantial change, contrasting with strong conservation in most photosynthetic land plants. Common features of reduced plastid genomes across diverse heterotrophic lineages point to a predictable trajectory of genome degradation, but this has been only partly tested. Here I document the molecular evolution of plastid genomes belonging to several mycoheterotroph lineages in Ericaceae, Gentianaceae and Polygalaceae, which include several independent origins of mycoheterotrophy in eudicot angiosperms that span different time scales since photosynthesis loss. I used next-generation and Sanger sequencing techniques to assemble complete plastomes or gene sets for comparative analyses of gene content and genome structure, and phylogenomic inference. I also sequenced several partially mycoheterotrophic and fully autotrophic relatives. Patterns of gene loss in mycoheterotroph plastomes are generally consistent with a previously hypothesized trajectory of change, starting with the loss of plastid NAD(P)H dehydrogenase before full loss of photosynthesis, and ending (here) with substantial reduction in genes involved in the translation apparatus and other nonphotosynthetic functions. Several retentions (delayed losses) of subunit genes for plastid-encoded polymerase, plastid ATP synthase and Rubisco are also consistent with hypothesized secondary (nonphotosynthetic) functions for these complexes. Two within-genus comparisons (for Epirixanthes in Polygalaceae and Voyria in Gentianaceae) demonstrate substantially different levels of genome degradation, consistent with heterogeneity in rates of genome change after a given origin of full mycoheterotrophy. Mycoheterotrophs in two families (Ericaceae, Polygalaceae) have extensive genome rearrangement compared to most land plants, contrasting with near colinearity in mycoheterotrophic members of Gentianaceae (despite sometimes extensive genome reduction in the latter). However, these contrasting patterns are apparently not associated with transitions to mycoheterotrophy, as photosynthetic relatives in Ericaceae and Polygalaceae are also substantially rearranged—or with inverted repeat loss (evident in Epirixanthes pallida, Polygalaceae), as autotrophic Polygala retains its inverted repeats. Phylogenomic inferences of core eudicot phylogeny made using the retained genes are generally well supported and robust to a variety of phylogenetic approaches, and are also congruent with recent phylogenetic studies in each mycoheterotrophic family.

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