Laboratorio de Neurobiología de Insectos (LNI), Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, CENEXA, CONICET, La Plata, Buenos Aires, Argentina.
Laboratorio de Insectos Sociales, Instituto de Fisiología, Biología Molecular y Neurociencias, Universidad de Buenos Aires - CONICET, Ciudad Autónoma de Buenos Aires, Argentina.
BMC Genomics. 2022 Nov 17;23(1):757. doi: 10.1186/s12864-022-08974-y.
Hemiptera is one of the most speciose orders of insects, and the most speciose considering Hemimetabola. Through their evolutive history, hemipterans with different feeding habits have adapted to deal with different chemical challenges. Three major gene families are involved in xenobiotic detoxification in insects: the cytochromes P450 (CYPs), carboxyl/cholinesterases (CCEs), and glutathione transferases (GSTs). Here we perform a comparative analysis on the complement of these gene superfamilies across five hemipteran species; four heteropterans (the pentatomid plant feeders Nezara viridula and Halyomorpha halys; the hematophagous Cimex lectularius, Cimicidae, and Rhodnius prolixus, Reduviidae), and one Auchenorrhyncha plant feeder (Nilaparvata lugens).
Our results point to an expansion of several enzyme families associated with xenobiotic detoxification in heteropterans with respect to other species and the existence of a dynamic evolution pattern including CYP3 clan, hormone and pheromone processing class in the CCE superfamily, and sigma class in GST superfamily. Other detoxification-related families are reduced in the hemipteran species analyzed here: reduction or even absence of epsilon class and reduced delta class in GST superfamily; absence of mitochondrial CYP12 family; absence of CYP9 family in CYP3 clan; and reduction or even absence of some dietary/detoxification groups of CCEs. Interestingly, the most polyphagous species analyzed here (H. halys) is also the one that presents the largest repertoire of detoxification enzymes. Gene cluster analysis suggests that this could be due to gene duplication events.
The evolutionary analysis performed here reveals characteristics that are both common and particular for heteropterans. The composition and organization of detoxification-related gene families could shed light on evolutionary forces that shaped their divergence. These families are important for both the detoxification of diet products and for conferring tolerance or resistance to synthetic insecticides. Furthermore, we present the first comprehensive analysis of detoxification gene superfamilies in N. viridula, an understudied species in spite of its economic relevance as a crop pest. The information obtained is of interest for basic insect science as well as for the control of harmful species and the management of insecticide resistance.
半翅目是昆虫中物种最丰富的目之一，也是考虑到不全变态的最丰富的目。通过它们的进化历史，具有不同取食习性的半翅目昆虫已经适应了不同的化学挑战。在昆虫中，有三个主要的基因家族参与了外来化合物的解毒作用：细胞色素 P450（CYPs）、羧酸酯酶/胆碱酯酶（CCEs）和谷胱甘肽转移酶（GSTs）。在这里，我们对五个半翅目物种中的这些基因超家族进行了比较分析；四个半翅目（半翅目植物食者绿盲蝽和红猎蝽；吸血的 Cimex lectularius、Cimicidae 和 Rhodnius prolixus、Reduviidae），以及一个 Auchenorrhyncha 植物食者（褐飞虱）。
我们的结果表明，与其他物种相比，异翅目昆虫中与外来化合物解毒相关的几种酶家族发生了扩张，并且存在一种动态进化模式，包括 CCE 超家族中的 CYP3 族、激素和信息素处理类以及 GST 超家族中的 sigma 类。在我们分析的半翅目物种中，其他与解毒相关的家族减少了：GST 超家族中的 epsilon 类和 delta 类减少或甚至缺失；线粒体 CYP12 家族缺失；CYP3 族中的 CYP9 家族缺失；CCE 的一些饮食/解毒组缺失或甚至缺失。有趣的是，这里分析的最杂食性物种（红猎蝽）也是解毒酶种类最多的物种。基因簇分析表明，这可能是由于基因重复事件。
这里进行的进化分析揭示了异翅目既共同又独特的特征。解毒相关基因家族的组成和组织可能揭示了塑造它们分化的进化力量。这些家族对于饮食产物的解毒以及赋予对合成杀虫剂的耐受性或抗性都很重要。此外，我们首次对面盲蝽属 N. viridula 的解毒基因超家族进行了全面分析，尽管它是一种经济上重要的作物害虫，但对它的研究却很少。获得的信息不仅对基础昆虫学有意义，而且对有害物种的控制和杀虫剂抗性的管理也有意义。
