The mitochondrial genomes of the early land plants Treubia lacunosa and Anomodon rugelii: dynamic and conservative evolution.

Yang Liu,Bin Wang,Yin-Long Qiu,Libo Li,Jia-Yu Xue,Debashish Bhattacharya

doi:10.1371/journal.pone.0025836

Yang Liu, Bin Wang + Show 4 more

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https://doi.org/10.1371/journal.pone.0025836

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Abstract

Early land plant mitochondrial genomes captured important changes of mitochondrial genome evolution when plants colonized land. The chondromes of seed plants show several derived characteristics, e.g., large genome size variation, rapid intra-genomic rearrangement, abundant introns, and highly variable levels of RNA editing. On the other hand, the chondromes of charophytic algae are still largely ancestral in these aspects, resembling those of early eukaryotes. When the transition happened has been a long-standing question in studies of mitochondrial genome evolution. Here we report complete mitochondrial genome sequences from an early-diverging liverwort, Treubia lacunosa, and a late-evolving moss, Anomodon rugelii. The two genomes, 151,983 and 104,239 base pairs in size respectively, contain standard sets of protein coding genes for respiration and protein synthesis, as well as nearly full sets of rRNA and tRNA genes found in the chondromes of the liverworts Marchantia polymorpha and Pleurozia purpurea and the moss Physcomitrella patens. The gene orders of these two chondromes are identical to those of the other liverworts and moss. Their intron contents, with all cis-spliced group I or group II introns, are also similar to those in the previously sequenced liverwort and moss chondromes. These five chondromes plus the two from the hornworts Phaeoceros laevis and Megaceros aenigmaticus for the first time allowed comprehensive comparative analyses of structure and organization of mitochondrial genomes both within and across the three major lineages of bryophytes. These analyses led to the conclusion that the mitochondrial genome experienced dynamic evolution in genome size, gene content, intron acquisition, gene order, and RNA editing during the origins of land plants and their major clades. However, evolution of this organellar genome has remained rather conservative since the origin and initial radiation of early land plants, except within vascular plants.

Highlights

Among major lineages of eukaryotes, land plants have mitochondrial genomes that exhibit several derived features setting them apart from chondromes of other eukaryotes: large and highly variable genome sizes, frequent intra-genomic rearrangements, rich and varied intron contents, highly variable RNA editing levels, and incorporation of foreign DNAs [1,2,3,4,5,6]
Over the last twenty years, chondromes from representatives of all major lineages of early land plants and some charophytic algae have been sequenced. These include four charophytes (Mesostigma viride [8], Chlorokybus atmophyticus [9], Chaetosphaeridium globosum [10], and Chara vulgaris [11]), two liverworts (Marchantia polymorpha [12] and Pleurozia purpurea [13]), one moss (Physcomitrella patens [14]), two hornworts (Megaceros aenigmaticus [15] and Phaeoceros laevis [17]), and two lycophytes (Isoetes engelmanii [18] and Selaginella moellendorffii [19])
General Features of the Treubia and Anomodon Mitochondrial Genomes. Both Treubia and Anomodon chondromes are assembled as single circular molecules (Figs. 1 and 2, deposited in GenBank under accessions JF973315 and JF973314)

Summary

Introduction

Among major lineages of eukaryotes, land plants (embryophytes) have mitochondrial genomes that exhibit several derived features setting them apart from chondromes of other eukaryotes: large and highly variable genome sizes, frequent intra-genomic rearrangements, rich and varied intron contents, highly variable RNA editing levels, and incorporation of foreign DNAs [1,2,3,4,5,6]. To determine the mode of mitochondrial genome evolution across the entire diversity of bryophytes, we sequenced chondromes of the moss Anomodon rugelii and the liverwort Treubia lacunosa. Comparison of the seven bryophyte chondromes with the Chara chondrome shows that the genome size increased roughly by three times during the origin of land plants and has been relatively stable afterwards, especially within liverworts, mosses, and hornworts (Table 1).

Results

Conclusion