Abstract
BackgroundAerobically respiring eukaryotes usually contain four respiratory-chain complexes (complexes I-IV) and an ATP synthase (complex V). In several lineages of aerobic microbial eukaryotes, complex I has been lost, with an alternative, nuclear-encoded NADH dehydrogenase shown in certain cases to bypass complex I and oxidize NADH without proton translocation. The first loss of complex I in any multicellular eukaryote was recently reported in two studies; one sequenced the complete mitogenome of the hemiparasitic aerial mistletoe, Viscum scurruloideum, and the other sequenced the V. album mitogenome. The V. scurruloideum study reported no significant additional loss of mitochondrial genes or genetic function, but the V. album study postulated that mitochondrial genes encoding all ribosomal RNAs and proteins of all respiratory complexes are either absent or pseudogenes, thus raising questions as to whether the mitogenome and oxidative respiration are functional in this plant.ResultsTo determine whether these opposing conclusions about the two Viscum mitogenomes reflect a greater degree of reductive/degenerative evolution in V. album or instead result from interpretative and analytical differences, we reannotated and reanalyzed the V. album mitogenome and compared it with the V. scurruloideum mitogenome. We find that the two genomes share a complete complement of mitochondrial rRNA genes and a typical complement of genes encoding respiratory complexes II-V. Most Viscum mitochondrial protein genes exhibit very high levels of divergence yet are evolving under purifying, albeit relaxed selection. We discover two cases of horizontal gene transfer in V. album and show that the two Viscum mitogenomes differ by 8.6-fold in size (66 kb in V. scurruloideum; 565 kb in V. album).ConclusionsViscum mitogenomes are extraordinary compared to other plant mitogenomes in terms of their wide size range, high rates of synonymous substitutions, degree of relaxed selection, and unprecedented loss of respiratory complex I. However, contrary to the initial conclusions regarding V. album, both Viscum mitogenomes possess conventional sets of rRNA and, excepting complex I, respiratory genes. Both plants should therefore be able to carry out aerobic respiration. Moreover, with respect to size, the V. scurruloideum mitogenome has experienced a greater level of reductive evolution.
Highlights
Respiring eukaryotes usually contain four respiratory-chain complexes and an ATP synthase
Absence of BLAST high-scoring segment pairs (HSPs) was considered evidence for gene loss. This approach is problematic because extensive sequence divergence, as reported in both V. album and V. scurruloideum [2, 5], can obscure the underlying sequence similarity possessed by homologous genes [9]
The V. album genome was compared to mitochondrial gene sequences from 33 complete angiosperm mitogenomes using BLASTN 2.2.28+ [8] with the following parameter settings: word size = 7, reward = 5, penalty = −4, gapopen = 8, and gapextend = 6
Summary
Respiring eukaryotes usually contain four respiratory-chain complexes (complexes I-IV) and an ATP synthase (complex V). In several lineages of aerobic microbial eukaryotes, complex I has been lost, with an alternative, nuclear-encoded NADH dehydrogenase shown in certain cases to bypass complex I and oxidize NADH without proton translocation. Almost all eukaryotes capable of carrying out aerobic respiration contain four multi-subunit electron-transfer complexes (complexes I-IV) that are more-or-less embedded in the inner mitochondrial membrane. Three of these complexes (I, III, and IV) translocate protons across this membrane to generate a proton gradient used by the mitochondrial ATP synthase (complex V) to phosphorylate ADP to ATP. Because functional transfer to the nucleus of all nine missing complex I (nad) genes is prohibitively unlikely [2], we concluded that V. scurruloideum represents the first reported case of loss of complex I in any multicellular eukaryote
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