Department of Biology, Lund University, Sölvegatan 37, 223 62, Lund, Sweden.
Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.
BMC Genomics. 2024 Aug 6;25(1):764. doi: 10.1186/s12864-024-10678-4.
BACKGROUND: Chemoreception is crucial for insect fitness, underlying for instance food-, host-, and mate finding. Chemicals in the environment are detected by receptors from three divergent gene families: odorant receptors (ORs), gustatory receptors (GRs), and ionotropic receptors (IRs). However, how the chemoreceptor gene families evolve in parallel with ecological specializations remains poorly understood, especially in the order Coleoptera. Hence, we sequenced the genome and annotated the chemoreceptor genes of the specialised ambrosia beetle Trypodendron lineatum (Coleoptera, Curculionidae, Scolytinae) and compared its chemoreceptor gene repertoires with those of other scolytines with different ecological adaptations, as well as a polyphagous cerambycid species. RESULTS: We identified 67 ORs, 38 GRs, and 44 IRs in T. lineatum ('Tlin'). Across gene families, T. lineatum has fewer chemoreceptors compared to related scolytines, the coffee berry borer Hypothenemus hampei and the mountain pine beetle Dendroctonus ponderosae, and clearly fewer receptors than the polyphagous cerambycid Anoplophora glabripennis. The comparatively low number of chemoreceptors is largely explained by the scarcity of large receptor lineage radiations, especially among the bitter taste GRs and the 'divergent' IRs, and the absence of alternatively spliced GR genes. Only one non-fructose sugar receptor was found, suggesting several sugar receptors have been lost. Also, we found no orthologue in the 'GR215 clade', which is widely conserved across Coleoptera. Two TlinORs are orthologous to ORs that are functionally conserved across curculionids, responding to 2-phenylethanol (2-PE) and green leaf volatiles (GLVs), respectively. CONCLUSIONS: Trypodendron lineatum reproduces inside the xylem of decaying conifers where it feeds on its obligate fungal mutualist Phialophoropsis ferruginea. Like previous studies, our results suggest that stenophagy correlates with small chemoreceptor numbers in wood-boring beetles; indeed, the few GRs may be due to its restricted fungal diet. The presence of TlinORs orthologous to those detecting 2-PE and GLVs in other species suggests these compounds are important for T. lineatum. Future functional studies should test this prediction, and chemoreceptor annotations should be conducted on additional ambrosia beetle species to investigate whether few chemoreceptors is a general trait in this specialized group of beetles.
背景:化感作用对昆虫的适应性至关重要,例如对食物、宿主和配偶的寻找。环境中的化学物质是由三个不同基因家族的受体检测到的:气味受体 (ORs)、味觉受体 (GRs) 和离子型受体 (IRs)。然而,化感受体基因家族如何与生态特化平行进化,特别是在鞘翅目昆虫中,仍知之甚少。因此,我们对专门的粉蠹虫 Trypodendron lineatum(鞘翅目,象甲科,小蠹亚科)的基因组进行了测序,并注释了其化感受体基因,并将其化感受体基因谱与其他具有不同生态适应能力的小蠹以及一种多食性的天牛属物种进行了比较。
结果:我们在 T. lineatum(“Tlin”)中鉴定出了 67 个 ORs、38 个 GRs 和 44 个 IRs。在基因家族中,与相关的小蠹、咖啡浆果象甲 Hypothenemus hampei 和松材线虫 Dendroctonus ponderosae 相比,T. lineatum 的化感受体数量较少,与多食性的天牛属物种 Anoplophora glabripennis 相比则明显较少。相对较少的化感受体数量在很大程度上是由于大受体谱系辐射的稀缺,特别是在苦味 GRs 和“分歧”IRs 中,以及缺乏选择性剪接的 GR 基因。只发现了一个非果糖糖受体,表明几个糖受体已经丢失。此外,我们在“GR215 分支”中没有发现直系同源物,该分支在鞘翅目昆虫中广泛保守。两个 TlinOR 与功能上在 curculionids 中保守的 OR 同源,分别对 2-苯乙醇 (2-PE) 和绿叶挥发物 (GLVs) 做出反应。
结论:Trypodendron lineatum 在腐朽的针叶树的木质部中繁殖,在那里它以其专性真菌共生菌 Phialophoropsis ferruginea 为食。与之前的研究一样,我们的结果表明,食性狭窄与蛀木甲虫中较少的化感受体数量相关;实际上,较少的 GR 可能是由于其有限的真菌饮食。与其他物种中检测到 2-PE 和 GLVs 的 TlinOR 同源的存在表明,这些化合物对 T. lineatum 很重要。未来的功能研究应该检验这一预测,并且应该对其他粉蠹属物种进行化感受体注释,以研究在这个专门的甲虫群体中,少数化感受体是否是一个普遍特征。
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