Horizontally transferred glycoside hydrolase 26 may aid hemipteran insects in plant tissue digestion

IF 3.6 1区 生物学 Q2 BIOCHEMISTRY & MOLECULAR BIOLOGY Molecular Phylogenetics and Evolution Pub Date : 2024-06-18 DOI:10.1016/j.ympev.2024.108134
Hunter K. Walt , Seung-Joon Ahn , Federico G. Hoffmann
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Abstract

Glycoside hydrolases are enzymes that break down complex carbohydrates into simple sugars by catalyzing the hydrolysis of glycosidic bonds. There have been multiple instances of adaptive horizontal gene transfer of genes belonging to various glycoside hydrolase families from microbes to insects, as glycoside hydrolases can metabolize constituents of the carbohydrate-rich plant cell wall. In this study, we characterize the horizontal transfer of a gene from the glycoside hydrolase family 26 (GH26) from bacteria to insects of the order Hemiptera. Our phylogenies trace the horizontal gene transfer to the common ancestor of the superfamilies Pentatomoidea and Lygaeoidea, which include stink bugs and seed bugs. After horizontal transfer, the gene was assimilated into the insect genome as indicated by the gain of an intron, and a eukaryotic signal peptide. Subsequently, the gene has undergone independent losses and expansions in copy number in multiple lineages, suggesting an adaptive role of GH26s in some insects. Finally, we measured tissue-level gene expression of multiple stink bugs and the large milkweed bug using publicly available RNA-seq datasets. We found that the GH26 genes are highly expressed in tissues associated with plant digestion, especially in the principal salivary glands of the stink bugs. Our results are consistent with the hypothesis that this horizontally transferred GH26 was co-opted by the insect to aid in plant tissue digestion and that this HGT event was likely adaptive.

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水平转移的苷水解酶 26 可能有助于半翅目昆虫消化植物组织。
糖苷水解酶是一种通过催化水解糖苷键将复杂碳水化合物分解为单糖的酶。由于糖苷水解酶可以代谢富含碳水化合物的植物细胞壁成分,属于各种糖苷水解酶家族的基因从微生物向昆虫进行了多次适应性水平基因转移。在这项研究中,我们描述了糖苷水解酶家族 26(GH26)的一个基因从细菌向半翅目昆虫水平转移的特征。我们的系统发生学将该基因水平转移追溯到了包括蝽和种子蝽在内的五蠹目和姬蛙目超家族的共同祖先。水平转移后,该基因被同化到昆虫基因组中,表现为获得了一个内含子和一个真核信号肽。随后,该基因在多个品系中经历了独立的拷贝数丢失和扩增,这表明 GH26s 在某些昆虫中具有适应性作用。最后,我们利用公开的 RNA-seq 数据集测量了多种蝽类和大型乳草蝽的组织级基因表达。我们发现,GH26 基因在与植物消化相关的组织中高度表达,尤其是在蝽的主要唾液腺中。我们的研究结果符合这样的假设,即这种横向转移的 GH26 被昆虫共同利用来帮助植物组织消化,而且这种 HGT 事件很可能是适应性的。
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来源期刊
Molecular Phylogenetics and Evolution
Molecular Phylogenetics and Evolution 生物-进化生物学
CiteScore
7.50
自引率
7.30%
发文量
249
审稿时长
7.5 months
期刊介绍: Molecular Phylogenetics and Evolution is dedicated to bringing Darwin''s dream within grasp - to "have fairly true genealogical trees of each great kingdom of Nature." The journal provides a forum for molecular studies that advance our understanding of phylogeny and evolution, further the development of phylogenetically more accurate taxonomic classifications, and ultimately bring a unified classification for all the ramifying lines of life. Phylogeographic studies will be considered for publication if they offer EXCEPTIONAL theoretical or empirical advances.
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