Horizontal Gene Transfer and Gene Duplication of β-Fructofuranosidase Confer Lepidopteran Insects Metabolic Benefits.

Horizontal Gene Transfer and Gene Duplication of β-Fructofuranosidase Confer Lepidopteran Insects Metabolic Benefits.
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DOI:
10.1093/molbev/msab080
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发表时间:
2021-06-25
影响因子:
10.7
通讯作者:
Wang H
Wang H
中科院分区:
生物学1区
文献类型:
--
作者:
Dai X;Kiuchi T;Zhou Y;Jia S;Xu Y;Katsuma S;Shimada T;Wang H

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水平基因转移(HGT)是生态适应和新遗传性状进化的重要物质来源。然而,缺乏关于生物体基因组中转移后复制的报道,并且赋予受体的进化优势通常知之甚少。蔗糖酶在昆虫的生理生长发育过程中起着重要作用。在此,我们对通过HGT从细菌转移的昆虫β-呋喃果糖苷酶的进化进行了全面的分析。结果表明,β-呋喃果糖苷酶在鳞翅目昆虫中广泛存在,在鞘翅目和膜翅目昆虫中也有零星存在。β-呋喃果糖苷酶基因经常发生修饰,如基因重复、差异基因丢失和突变率的变化。鳞翅目昆虫β-呋喃果糖苷酶基因(SUC)簇在家蚕(蛾)和黄凤蝶(蝶)的基因表达谱和酶学性质上存在显著差异。我们使用CRISPR/Cas9在B. mori中产生SUC 1突变,以彻底检查SUC的生理功能。BmSUC 1突变体幼虫是可行的,但显示延迟生长和蔗糖酶活性降低,包括敏感性糖模拟生物碱中发现的高浓度的桑树。BmSUC 1是一种重要的蔗糖酶,支持幼虫中肠和丝腺的代谢平衡,表明转β-呋喃果糖苷酶基因增强了鳞翅目昆虫的消化和代谢适应。这些发现不仅突出了β-呋喃果糖苷酶与维持碳水化合物代谢的联系的普遍功能,而且还强调了丝腺中未充分探索的功能。这项研究扩展了我们的知识转移后复制和随后的功能多样化的适应性进化和谱系特异性适应的生物体。
Horizontal gene transfer (HGT) is a potentially critical source of material for ecological adaptation and the evolution of novel genetic traits. However, reports on posttransfer duplication in organism genomes are lacking, and the evolutionary advantages conferred on the recipient are generally poorly understood. Sucrase plays an important role in insect physiological growth and development. Here, we performed a comprehensive analysis of the evolution of insect β-fructofuranosidase transferred from bacteria via HGT. We found that posttransfer duplications of β-fructofuranosidase were widespread in Lepidoptera and sporadic occurrences of β-fructofuranosidase were found in Coleoptera and Hymenoptera. β-fructofuranosidase genes often undergo modifications, such as gene duplication, differential gene loss, and changes in mutation rates. Lepidopteran β-fructofuranosidase gene (SUC) clusters showed marked divergence in gene expression patterns and enzymatic properties in Bombyx mori (moth) and Papilio xuthus (butterfly). We generated SUC1 mutations in B. mori using CRISPR/Cas9 to thoroughly examine the physiological function of SUC. BmSUC1 mutant larvae were viable but displayed delayed growth and reduced sucrase activities that included susceptibility to the sugar mimic alkaloid found in high concentrations in mulberry. BmSUC1 served as a critical sucrase and supported metabolic homeostasis in the larval midgut and silk gland, suggesting that gene transfer of β-fructofuranosidase enhanced the digestive and metabolic adaptation of lepidopteran insects. These findings highlight not only the universal function of β-fructofuranosidase with a link to the maintenance of carbohydrate metabolism but also an underexplored function in the silk gland. This study expands our knowledge of posttransfer duplication and subsequent functional diversification in the adaptive evolution and lineage-specific adaptation of organisms.
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DOI: 10.1093/molbev/msz019
发表时间: 2019-05-01
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