Plastid genome evolution of the non-photosynthetic liverwort Aneura mirabilis (Malmb.) Wickett & Goffinet (Aneuraceae)

Date of Completion

January 2007

Keywords

Biology, Botany

Degree

Ph.D.

Abstract

Aneura mirabilis is a parasitic liverwort in the Aneuraceae that obtains fixed atmospheric carbon from a host tree, using a fungal symbiont that is simultaneously ectomycorrhizal on the tree. Originally placed in its own genus, Cryptothallus, I determined in chapter one that the parasitic liverwort is nested within a Glade of morphologically indistinguishable photosynthetic liverworts and should be considered to be a distinct species of the genus Aneura. The annotated, complete plastid genome sequence of A. mirabilis, presented in chapter two, revealed the complete functional loss of the chlororespiration (ndh) genes, pseudogenes for major subunits of photosystem I, photosystem II, and the cytochrome b6f complex, and an inversion of psbE and petL. Aside from this inversion, the order of genes is congruent with the order of genes in Marchantia polymorpha, the only other liverwort plastid genome sequence available. The designation of pseudogenes was made using genomic comparisons with the phylogenetically distant liverwort M. polymorpha. In order to correlate functional gene losses with the evolution of a heterotrophic life history, we sampled several populations of A. mirabilis and its photosynthetic sister groups and sequenced plastid regions homologous with the losses detected in the plastid genome sequence. A functional gene loss or the psbE- petL inversion was never detected in a photosynthetic liverwort. All the gene losses and the psbE-petL inversion were detected in every population of the nonphotosynthetic liverwort sampled. The rates of synonymous and non-synonymous substitutions were estimated for eight pseudogenes and six genes to detect whether they are evolving under relaxed purifying selection. Here we present evidence that A. mirabilis has recently acquired an obligately heterotrophic life history, and that large deletions, and structural rearrangements may play an important role in the functional reduction of the plastid genome, rather than a relaxation of a synonymous substitution bias, early in the shift to parasitism. ^

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