Evolutionary dynamics of plant cell wall-degrading enzymes in weevils: A comparative study across Curculionoidea

Weevils of the superfamily Curculionoidea arguably represent the most diverse group of herbivorous beetles. Most of the 62,000 described species feed on live plants, some on rotten wood, and others on wood-decaying fungi. They include economically important pests like bark beetles (Scolytinae), grain weevils (Sitophilus spp.), and the boll weevil (Anthonomus grandis). Previous research suggests that enzymes breaking down plant cell wall polysaccharides may have influenced weevil diversification. However, our understanding of the distribution of plant cell wall-degrading enzymes (PCWDEs) and their evolution in Curculionoidea is limited to a few species, primarily within Curculionidae. Herein, using transcriptome and genome data, we analyzed PCWDE-encoding genes in 45 weevil species representative of the majority of families within Curculionoidea. Our investigation revealed the presence of 13 families of PCWDEs, including the description of putative endo-α-1,5-L-arabinanases from subfamily 6 of glycoside hydrolase family 43 (GH43_6) in animals for the first time. Different weevil species possessed varying numbers of PCWDE families, ranging from one to nine. Notably, species associated with wood-decaying fungi, including ambrosia beetles (Scolytinae), exhibited a reduced set of PCWDEs compared to closely related species that primarily feed on plants. Our study provides valuable insights into the distribution and diversity of PCWDEs within Curculionoidea, reinforcing the role played by horizontal gene transfer, gene duplication and gene loss in the evolution of these enzyme families.

曲翅甲总科中的象甲虫群，或许可称之为最繁茂的植食性甲虫类群。在已描述的62,000种象甲虫中，大多数以活植物为食，部分以腐烂木材为食，还有的以木腐真菌为食。它们包括对经济造成重大损失的害虫，如 bark beetles (Scolytinae)、grain weevils (Sitophilus spp.) 以及棉铃象虫 (Anthonomus grandis)。先前的研究表明，分解植物细胞壁多糖的酶可能影响了象甲虫的多样性。然而，我们对植物细胞壁降解酶（PCWDEs）的分布及其在曲翅甲总科中的进化的理解，仅限于少数物种，主要集中于 Curculionidae 科。在本研究中，我们利用转录组和基因组数据，分析了代表曲翅甲总科大多数科类的45种象甲虫中的PCWDE编码基因。我们的研究揭示了13个PCWDE家族的存在，其中包括首次在动物中描述了来自糖苷水解酶家族43（GH43_6）第6亚科的假定的内切-α-1,5-L-阿拉伯糖苷酶。不同的象甲虫物种拥有不同数量的PCWDE家族，数量从一至九不等。值得注意的是，与木腐真菌相关的物种，包括 ambrosia beetles (Scolytinae)，相较于主要以植物为食的近缘物种，其PCWDEs的集合更为减少。本研究为曲翅甲总科中PCWDEs的分布和多样性提供了宝贵的见解，进一步强化了水平基因转移、基因复制和基因丢失在酶家族进化中所扮演的角色。