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Mitochondrial genome evolution and tRNA truncation in Acariformes mites: new evidence from eriophyoid mites.

ABSTRACT: The subclass Acari (mites and ticks) comprises two super-orders: Acariformes and Parasitiformes. Most species of the Parasitiformes known retained the ancestral pattern of mitochondrial (mt) gene arrangement of arthropods, and their mt tRNAs have the typical cloverleaf structure. All of the species of the Acariformes known, however, have rearranged mt genomes and truncated mt tRNAs. We sequenced the mt genomes of two species of Eriophyoidea: Phyllocoptes taishanensis and Epitrimerus sabinae. The mt genomes of P. taishanensis and E. sabinae are 13,475?bp and 13,531?bp, respectively, are circular and contain the 37 genes typical of animals; most mt tRNAs are highly truncated in both mites. On the other hand, these two eriophyoid mites have the least rearranged mt genomes seen in the Acariformes. Comparison between eriophyoid mites and other Aacariformes mites showed that: 1) the most recent common ancestor of Acariformes mites retained the ancestral pattern of mt gene arrangement of arthropods with slight modifications; 2) truncation of tRNAs for cysteine, phenylalanine and histidine occurred once in the most recent common ancestor of Acariformes mites whereas truncation of other tRNAs occurred multiple times; and 3) the placement of eriophyoid mites in the order Trombidiformes needs to be reviewed.

SUBMITTER: Xue XF

PROVIDER: S-EPMC4702108 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Mitochondrial genome evolution and tRNA truncation in Acariformes mites: new evidence from eriophyoid mites.

Xue Xiao-Feng XF Guo Jing-Feng JF Dong Yan Y Hong Xiao-Yue XY Shao Renfu R

Scientific reports 20160106

The subclass Acari (mites and ticks) comprises two super-orders: Acariformes and Parasitiformes. Most species of the Parasitiformes known retained the ancestral pattern of mitochondrial (mt) gene arrangement of arthropods, and their mt tRNAs have the typical cloverleaf structure. All of the species of the Acariformes known, however, have rearranged mt genomes and truncated mt tRNAs. We sequenced the mt genomes of two species of Eriophyoidea: Phyllocoptes taishanensis and Epitrimerus sabinae. The ...[more]

PMID: 26732998

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Project description:BackgroundThe mitochondrial (mt) genomes of Sarcoptiformes mites typically contain 37 genes. Although the loss of genes is rare in Sarcoptiformes mite mitogenomes, two of the six previously reported oribatid mites (Acariforms: Sarcoptiformes) are reported to have lost parts of their tRNA genes. To confirm whether the tRNA genes were indeed lost and whether the loss is universal, we re-annotated the available oribatid mite sequences and sequenced the mitogenome of Oribatula sakamorii.MethodsThe mitogenome of O. sakamorii was sequenced using an Illumina HiSeq sequencer. The mt tRNA gene was annotated using multi-software combined with a manual annotation approach. Phylogenetic analyses were performed using the maximum likelihood and Bayesian inference methods with concatenated nucleotide and amino acid sequences.ResultsThe mitogenomes of O. sakamorii contained 37 genes, including 22 tRNA genes. We identified all mt tRNA genes that were reported as "lost" in Steganacarus magnus and Paraleius leontonychus and revealed certain atypical tRNA annotation errors in oribatid mite sequences. Oribatid mite mitogenomes are characterized by low rates of genetic rearrangement, with six or seven gene blocks conserved between the mitogenome of all species and that of ancestral arthropods. Considering the relative order of the major genes (protein-coding genes and rRNAs), only one or two genes were rearranged with respect to their positions in the ancestral genome. We explored the phylogenetic relationships among the available oribatid mites, and the results confirmed the systematic position of Hermannia in the Crotonioidea superfamily. This was also supported by the synapomorphic gene-derived boundaries.ConclusionsThe tRNA "lost" phenomenon is not universal in oribatid mites. Rather, highly atypical secondary structure of the inferred mt tRNA genes made them unidentifiable using a single type of tRNA search program. The use of multi-software combined with a manual annotation approach can improve the accuracy of tRNA gene annotation. In addition, we identified the precise systematic position of Hermannia and validated that Astigmata is nested in Oribatida.

Project description:Phytoparasitic mites of the superfamily Eriophyoidea Nalepa live and feed on mature leaf surfaces, between leaf bud scales, and (though less commonly) on flowers or fruits. In this study, we focused on the seasonal associations of two eriophyoid species, Shevtchenkella serrata (Nalepa 1892) with the Norway maple tree (Acer platanoides L.), and Brevulacus reticulatus Manson 1984 with the common oak (Quercus robur L.). These species have complex life cycles with two morphologically different, seasonal female forms, the protogyne and deutogyne. In B. reticulatus, both forms retain all the major generic characteristics but in S. serrata only the protogynes conform to the diagnosis of Shevtchenkella, whereas the deutogynes have the typical traits of Anthocoptes. We confirmed the conspecificity of the protogynes and deutogynes of both eriophyoid species by sequencing a barcode fragment of the Cox1 gene from which we obtained four pairwise identical sequences: ON920305/ON920306 (S. serrata) and ON920307/ON920308 (B. reticulatus). In addition, taxonomical studies on Shevtchenkella and Brevulacus resulted in new synonymies and combinations: (1) Oxypleurites obtusus Roivainen 1947 is considered a deutogyne of S. serrata and treated as a junior synonym of S. serrata; (2) two rhyncaphytoptine species from North America are transferred from the genus Rhyncaphytoptus to Brevulacus: B. albus (Keifer 1959) comb. nov. and B. atlanticus (Keifer 1959) comb. nov.; and (3) one species, B. salicinus Soika et al. 2017, is excluded from Brevulacus and transferred to Rhyncaphytoptus: Rhyncaphytoptus salicinus (Soika et al. 2017) comb. nov. Apart from distinct morphological deuterogyny in S. serrata and B. reticulatus, we observed the persistent association of S. serrata with the generative organs of the maple tree, A. platanoides, leading to transmission to the next host generation via the seed-containing winged fruits (samaras) and subsequent colonization of seedlings. In B. reticulatus, similar synchronization with host-plant dispersal was not detected; however, in mid-summer, temporary colonization of immature acorns and feeding was observed. Additional studies conducted in various ecosystems and including different ecological groups of plants, especially anemochorous plants, are needed to estimate the frequency of the association of eriophyoids with plant generative organs, seeds and seedlings to better understand what role in mite ecology such associations may play.

Dataset Information

Mitochondrial genome evolution and tRNA truncation in Acariformes mites: new evidence from eriophyoid mites.

Publications

Mitochondrial genome evolution and tRNA truncation in Acariformes mites: new evidence from eriophyoid mites.

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