Genome sequencing provides insights into the evolution of gene families encoding plant cell wall-degrading enzymes in longhorned beetles

With more than 36,000 species, the longhorned beetles (family Cerambycidae) are a mega-diverse lineage of mostly xylophagous insects, all of which are represented by the sole sequenced genome of the Asian longhorned beetle (Anoplophora glabripennis; Lamiinae). Their successful radiation has been linked to their ability to degrade plant cell wall components using a range of so-called plant cell wall-degrading enzymes (PCWDEs). Our previous analysis of larval gut transcriptomes demonstrated that cerambycid beetles horizontally acquired genes encoding PCWDEs from various microbial donors; these genes evolved through multiple duplication events to form gene families. To gain further insights into the evolution of these gene families during the Cerambycidae radiation, we assembled draft genomes for four beetle species belonging to three subfamilies using long-read nanopore sequencing. All of the PCWDE-encoding genes we annotated from the corresponding larval gut transcriptomes were present in these draft genomes, and we identified new ones. We confirmed that the newly discovered horizontally acquired glycoside hydrolase family 7 (GH7), subfamily 26 of GH43 (GH43_26), and GH53 (all of which are absent from the A. glabripennis genome) were indeed encoded by these beetles’ genome. Most of the PCWDE-encoding genes of bacterial origin gained introns after their transfer into the beetle genome. Altogether, we show that draft genome assemblies generated from error-prone nanopore long-reads offer meaningful information to the study of the evolution of gene families in insects. We anticipate that our data will support studies aiming to better understand the biology of the Cerambycidae and other beetles in general.

拥有超过36,000个物种，长角甲虫（科名：Cerambycidae）构成了一个具有高度多样性的谱系，其主要食木昆虫，均以亚洲长角甲虫（Anoplophora glabripennis；Lamiinae）唯一的测序基因组为代表。其成功的辐射分布与其能够利用一系列所谓的植物细胞壁降解酶（PCWDEs）降解植物细胞壁成分的能力密切相关。我们之前对幼虫肠道转录组的分析表明，长角甲虫通过横向获取来自各种微生物供体的编码PCWDEs的基因；这些基因通过多次复制事件演化成基因家族。为了进一步探讨长角甲虫谱系演化过程中这些基因家族的进化，我们利用长读长纳米孔测序技术，对三个亚科中的四个甲虫物种的草图基因组进行了组装。我们从相应的幼虫肠道转录组中注释的所有编码PCWDEs的基因均存在于这些草图基因组中，并发现了新的基因。我们证实，新发现的横向获取的糖苷水解酶家族7（GH7）、GH43的子家族26（GH43_26）以及GH53（均在Anoplophora glabripennis基因组中不存在）确实由这些甲虫的基因组编码。大部分源于细菌的PCWDE编码基因在转移到甲虫基因组后获得了内含子。总的来说，我们表明由错误率较高的纳米孔长读长组装的草图基因组为研究昆虫基因家族的进化提供了有价值的信息。我们期待我们的数据将支持旨在更深入理解长角甲虫以及其他甲虫类生物学的研究。