Positive Correlation of the Gene Rearrangements and Evolutionary Rates in the Mitochondrial Genomes of Thrips (Insecta: Thysanoptera)

Abstract

Extensive gene rearrangement is characteristic in the mitogenomes of thrips (Thysanoptera), but the historical process giving rise to the contemporary gene rearrangement pattern remains unclear. To better understand the evolutionary processes of gene rearrangement in the mitogenomes of thrips, we sequenced the mitogenome of the banded thrip species Aeolothrips xinjiangensis. First, we found a novel mitochondrial gene order in this species. This mitogenome is 16,947 bp in length and encodes the typical 37 coding genes (13 protein-coding genes, 22 tRNA genes, and two rRNA genes) of insects. The gene arrangement was dramatically different from the putative ancestral mitogenome, with 26 genes being translocated, eight of which were inverted. Moreover, we found a novel, conserved gene block, trnC-trnY, which has not been previously reported in the mitogenomes of thrips. With this newly assembled mitogenome, we compared mitogenome sequences across Thysanoptera to assess the evolutionary processes giving rise to the current gene rearrangement pattern in thrips. Seven identical gene blocks were shared by two sequenced banded thrip mitogenomes, while the reversal of ND2 combined with TDRL events resulted in the different gene orders of these two species. In phylogenetic analysis, the monophyly of the suborders and families of Thysanoptera was well supported. Across the gene orders of 14 thrips, only two conserved gene blocks, ATP8-ATP6 and ND4-ND4L, could be found. Correlation analysis showed that the degree of gene rearrangement was positively correlated with the non-synonymous substitution rate in thrips. Our study suggests that the mitogenomes of thrips remain stable over long evolutionary timescales after massive rearrangement during early diversification.

The extraordinary rearrangement of mitochondrial genome of the wheat pest, Aptinothrips stylifer and the mitochondrial phylogeny of Thripidae (Thysanoptera)

“…As DNA markers, mitochondrial genomes (mitogenomes) have been instrumental in analyzing tribal and generic relationships in various insects (Chen et al, 2019(Chen et al, , 2021Wu et al, 2022;Zhou et al, 2020). In Thysanoptera, mitogenomic data have been beneficial in uncovering phylogenetic and evolutionary relationships among genera and species of thrips (Chakraborty et al, 2018;Kumar et al, 2019;Liu et al, 2022), revealing unique and complex rearrangements in the mitogenome structure. The first sequenced thrips mitogenome, Thrips imaginis, exhibited obvious structural rearrangement (Shao & Barker, 2003), with subsequent thrips species also showing rearrangements compared with the proposal ancestral genome (Chakraborty et al, 2018;Dang et al, 2021;Kumar et al, 2019;Liu et al, 2017Liu et al, , 2022Yan et al, 2014).…”

“…In Thysanoptera, mitogenomic data have been beneficial in uncovering phylogenetic and evolutionary relationships among genera and species of thrips (Chakraborty et al, 2018;Kumar et al, 2019;Liu et al, 2022), revealing unique and complex rearrangements in the mitogenome structure. The first sequenced thrips mitogenome, Thrips imaginis, exhibited obvious structural rearrangement (Shao & Barker, 2003), with subsequent thrips species also showing rearrangements compared with the proposal ancestral genome (Chakraborty et al, 2018;Dang et al, 2021;Kumar et al, 2019;Liu et al, 2017Liu et al, , 2022Yan et al, 2014). At present, GenBank contains only 28 mitogenomic sequences pertaining to thrips, 19 of which belong to the family Thripidae.…”

Multiple independent origins of duplicated mitochondrial control regions indicate an apomorphy in the Thysanoptera (Insecta)

“…Phylogenetic relationships of thrip species were inferred using the concatenated alignment of 13 PCGs with Bayesian inference (BI) and maximum likelihood (ML) methods, with Alloeorhynchus bakeri from Heteroptera as the outgroup, which was also used in other mitogenome-based phylogenetic analyses of Thysanoptera (Liu et al, 2022;Pakrashi et al, 2022Pakrashi et al, , 2023Tyagi et al, 2020). The codon-based multiple alignment with ClustalW was used to align each of the 13 mitochondrial genes individually in MEGA 5 (Tamura et al, 2011).…”

“…The frequent duplicated CRs, high rate of gene rearrangement, and duplication events make them an excellent model for researching the evolution of insect mitogenomes (Shao & Barker, 2003). Duplicate CRs were first found in the genus Thrips from the family Thripidae (Shao & Barker, 2003); then it was further identified in many other genera, for example, Frankliniella (Pakrashi et al, 2022;Yan et al, 2012Yan et al, , 2014, Scirtothrips (Dickey et al, 2015), Neohydatothrips (Kumar et al, 2019), Franklinothrips (Tyagi et al, 2020), Mycterothrips (Pakrashi et al, 2022), Phibalothrips (Pakrashi et al, 2022), and Aeolothrips (Liu et al, 2022). The sequence similarity between CR copies varies widely from >90% in Frankliniella spp.…”

“…However, recently, some authors proposed that the presence of multiple CRs and gene rearrangement is not causal (Tyagi et al, 2020). The thrip phylogeny is intensively studied, and classification systems based on mitogenomes were proposed (Liu et al, 2022;Pakrashi et al, 2022Pakrashi et al, , 2023Tyagi et al, 2020).…”