Unusual mitochondrial tRNA rearrangements in stingless bee Tetragonula pagdeni and phylogenetic analysis

Abstract

Tetragonula pagdeni (Hymenoptera: Meliponini) is a widely distributed and economically important stingless bee. The taxonomic status and evolution of this species have not been fully understood. We sequenced the mitogenome of T. pagdeni and analyzed its characteristics including gene rearrangements in present work, which will provide help for better protection and utilization of this germplasm resource. The mitochondrial genome sequence was obtained by establishing library and high-throughput sequencing. Using all protein coding sequences joined, the phylogenetic analysis demonstrated that T. pagdeni has the closest kinship with Lepidotrigona species, and then has a second closest kinship with the Melipona stingless bees. All the stingless bee species (Meliponini) analyzed formed a single clade, and among them the T. pagdeni mitogenome exhibited the highest gene rearrangement score, suggesting this species has an overactive evolutionary history. Especially, an unusual tRNA-Gly translocation was observed in T. pagdeni mitogenome, which broke the super-conserved atp8-atp6-cox3-G block in Hymenoptera mitogenomes. The translocated tRNA-Gly moved to a position next to the D-loop control region, and whether this translocation has a functional effect to the widely distributed T. pagdeni need further exploration. The variations of gene positions in mitogenome could also provide useful information to clarify the phylogenetic relations in Meliponini.

Comparative analyses of mitogenomes in the social bees with insights into evolution of long inverted repeats in the Meliponini

“…Recently, Françoso et al ( 2023 ) also found long IRs in the mitogenomes of Australian species T. hockingsi and T. carbonaria , which have been confirmed from different samples of the two same species in this study. Although mitogenomes of L. terminata and T. pagdeni have long IRs in our assemblies, previous studies failed to identify IRs in L. terminata ( Wang et al, 2020 ), L. flavibasis ( Wang et al 2021 ), and T. pagdeni ( Wang et al, 2022 ). Firstly, it is only possible to detect IRs using de novo assembly.…”

“…Previous studies ( Dowton & Austin, 1999 ; Dowton et al, 2003 , 2009 ; Peters et al, 2017 ; Silvestre & Arias, 2006 ; Wang et al, 2020 , 2021 , 2022 ; Wei et al, 2010 ; Zheng et al, 2018 ) suggest that tRNA rearrangements are prevalent across different taxonomy levels within Hymenoptera, and can provide phylogenetic information. However, all these studies only sampled one or very few species to represent the whole genus or tribe, ignoring the influence of gene rearrangements at lower taxonomic level.…”

“…Major structural variations have been found in insect mitogenomes of some lineages including: (1) duplication of PCGs in the species Microchorista philpotti (Nannochoristidae) ( Beckenbach, 2011 ), or inverted duplication of the nearly whole mitogenome or circular amphimeric mitogenome in two Australian stingless bees of Tetragonula (Hymenoptera) ( Françoso et al, 2023 ); (2) multiple fragmented mitogenomes in order Thysanoptera ( Dickey et al, 2015 ), Psocoptera ( Shi et al, 2016 ), and Phthiraptera ( Sweet et al, 2022 ); (3) gene or gene segment translocations or rearrangements in order Hemiptera ( Li et al, 2012 ), Phthiraptera ( Sweet et al, 2021 ), Psocoptera ( Li et al, 2013 ), and Hymenoptera ( de Paula Freitas et al, 2020 ; Oliveira et al, 2008 ; Xiao et al, 2011 ; Zheng et al, 2018 ), with massive rearrangements in Tetragonula spp. ( Françoso et al, 2023 ; Wang et al 2022 ), Lepidotrigona spp. ( Wang et al, 2020 , 2021 ).…”

“…Among the three tribes, a large number of mitogenomes from Apini and Bombini have been decoded and show the typical type of mitogenome. By contrast, the mitogenomes of Meliponini have been less investigated ( de Paula Freitas et al, 2020 ; Wang et al, 2020 , 2021 , 2022 ). Recent studies showed massive mitogenome variations in gene rearrangements and structural reorganizations in Meliponini.…”

The nuclear and mitochondrial genome assemblies of Tetragonisca angustula (Apidae: Meliponini), a tiny yet remarkable pollinator in the Neotropics

“…We also found that the mitogenome of T. angustula shares the same gene organization with that of F. varia [ 24 ], which distinguishes both from the other sequenced species of stingless bees. Considerable rearrangements have been observed in stingless bees [ 123 , 124 ], albeit with some gene blocks seemingly maintaining their conserved organization—another phenomenon commonly observed in metazoans [ 125 ]. However, only T. angustula and F. varia , as far as the available data show, exhibit the peculiarity of having all mitochondrial genes encoded on the putative plus strand.…”