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Distribution and Evolution of Pseudogenes, Gene Losses, and a Gene Rearrangement in the Plastid Genome of the Nonphotosynthetic Liverwort, Aneura mirabilis (Metzgeriales, Jungermanniopsida)

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Abstract

The plastid genome sequence of the parasitic liverwort Aneura mirabilis revealed the loss of five chlororespiration (ndh) genes. Additionally, six ndh genes, subunits of photosystem I, photosystem II, and the cytochrome b6f complex were inferred to be pseudogenes. Pseudogenes of cysA, cyst, ccsA, and ycf3, an inversion of psbE and petL, were also detected. The designation of pseudogenes was made using comparisons with the distantly related liverwort Marchantia polymorpha. We sampled several populations of A. mirabilis and its photosynthetic sister groups to correlate functional gene losses with the evolution of a achlorophylly. The gene losses, pseudogenes, or the psbE-petL inversion were never detected in a photosynthetic Aneura but were detected in every population of A. mirabilis. One population of A. mirabilis revealed a unique deletion of 541 bp in the psbE-petL region; another is characterized by a unique deletion of 471 bp in the trnV(UAC)-ndhC region. The ratio of synonymous-to-nonsynonymous substitution rates (ω) was estimated for eight pseudogenes and six ORFs to detect relaxed purifying selection. A significant increase in ω for the nonphotosynthetic liverwort was detected in six pseudogenes. Relaxation purifying selection, determined by a significant increase in ω, was detected for three intact ORFs: psbA, psbM, and rbcL.

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Acknowledgments

This study was supported by grants from the National Science Foundation (EF-0531557 to B.G. and doctoral dissertation improvement grant DEB-0408043 to N.W.), the National Geographic Society, Sigma Xi, and the University of Connecticut (an R. A. Bamford endowment to Ecology and Evolutionary Biology and a Doctoral Dissertation Fellowship). David Long assisted in obtaining fresh, field-collected material. Herbarium material or DNA was provided by Laura Forrest, Blanka Shaw, Nancy Slack, Alain Vanderpoorten, the New York Botanical Garden, and the Swedish Museum of Natural History. The authors thank Ned Young for assistance with HyPhy and thank Louise Lewis and Kent Holsinger for comments on an early version of the manuscript.

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  1. Department of Ecology and Evolutionary Biology, University of Connecticut, 75 North Eagleville Road, Storrs, CT, 06269-3043, USA

    Norman J. Wickett, Yu Fan, Paul O. Lewis & Bernard Goffinet

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  1. Norman J. Wickett
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Correspondence to Norman J. Wickett.

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Wickett, N.J., Fan, Y., Lewis, P.O. et al. Distribution and Evolution of Pseudogenes, Gene Losses, and a Gene Rearrangement in the Plastid Genome of the Nonphotosynthetic Liverwort, Aneura mirabilis (Metzgeriales, Jungermanniopsida). J Mol Evol 67, 111–122 (2008). https://doi.org/10.1007/s00239-008-9133-1

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