Feimin Yuan , Minjing Su , Tiantian Li , Yalin Zhang , Christopher H. Dietrich , Michael D. Webb , Cong Wei
{"title":"Functional and evolutionary implications of protein and metal content of leafhopper brochosomes","authors":"Feimin Yuan , Minjing Su , Tiantian Li , Yalin Zhang , Christopher H. Dietrich , Michael D. Webb , Cong Wei","doi":"10.1016/j.ibmb.2023.103962","DOIUrl":null,"url":null,"abstract":"<div><p><span><span>Brochosomes derived from the specialized glandular segments of the Malpighian tubules<span> (MTs) form superhydrophobic coatings for insects of Membracoidea, and have multiple hypothetical functions. However, the constituents, </span></span>biosynthesis<span> and evolutionary origin of brochosomes remain poorly understood. We investigated general chemical and physical characteristics of the integumental brochosomes (IBs) of the leafhopper </span></span><em>Psammotettix striatus</em><span><span><span><span>, determined the constituents of IBs, identified the unigenes involved in brochosomal </span>protein synthesis<span>, and investigated the potential associations among brochosomal protein synthesis, amino acid composition of food source, and the possible roles of </span></span>endosymbionts<span> in brochosome production. The results show that IBs are mainly composed of glycine- and tyrosine-rich proteins and some metal elements, which contain both essential and non-essential amino acids (EAAs and NEAAs) for insects, including EAAs deficient in the sole food source. All 12 unigenes involved in synthesizing the 12 brochosomal proteins (BPs) with high confidence are exclusively highly expressed in the glandular segment of MTs, confirming that brochosomes are synthesized by this segment. The synthesis of BPs is one of the key synapomorphies of Membracoidea but may be lost secondarily in a few lineages. The synthesis of BPs might be related to the symbiosis of leafhoppers/treehoppers with endosymbionts that provide these insects with EAAs, including those are deficient in the sole diet (i.e., plant sap) and could only be made available by the </span></span>symbionts<span>. We hypothesize that the functional modification of MTs have combined with the application of BPs enabling Membracoidea to colonize and adapt to novel ecological niches, and evolve to the dramatic diversification of this hemipteran group (in particular the family Cicadellidae). This study highlights the importance of evolutionary plasticity and multiple functions of MTs in driving the adaptations and evolution of sap-sucking insects of Hemiptera.</span></span></p></div>","PeriodicalId":330,"journal":{"name":"Insect Biochemistry and Molecular Biology","volume":null,"pages":null},"PeriodicalIF":3.2000,"publicationDate":"2023-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Insect Biochemistry and Molecular Biology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0965174823000565","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Brochosomes derived from the specialized glandular segments of the Malpighian tubules (MTs) form superhydrophobic coatings for insects of Membracoidea, and have multiple hypothetical functions. However, the constituents, biosynthesis and evolutionary origin of brochosomes remain poorly understood. We investigated general chemical and physical characteristics of the integumental brochosomes (IBs) of the leafhopper Psammotettix striatus, determined the constituents of IBs, identified the unigenes involved in brochosomal protein synthesis, and investigated the potential associations among brochosomal protein synthesis, amino acid composition of food source, and the possible roles of endosymbionts in brochosome production. The results show that IBs are mainly composed of glycine- and tyrosine-rich proteins and some metal elements, which contain both essential and non-essential amino acids (EAAs and NEAAs) for insects, including EAAs deficient in the sole food source. All 12 unigenes involved in synthesizing the 12 brochosomal proteins (BPs) with high confidence are exclusively highly expressed in the glandular segment of MTs, confirming that brochosomes are synthesized by this segment. The synthesis of BPs is one of the key synapomorphies of Membracoidea but may be lost secondarily in a few lineages. The synthesis of BPs might be related to the symbiosis of leafhoppers/treehoppers with endosymbionts that provide these insects with EAAs, including those are deficient in the sole diet (i.e., plant sap) and could only be made available by the symbionts. We hypothesize that the functional modification of MTs have combined with the application of BPs enabling Membracoidea to colonize and adapt to novel ecological niches, and evolve to the dramatic diversification of this hemipteran group (in particular the family Cicadellidae). This study highlights the importance of evolutionary plasticity and multiple functions of MTs in driving the adaptations and evolution of sap-sucking insects of Hemiptera.
来自马氏小管(MTs)的特殊腺段的溴小体为膜科昆虫形成了超疏水涂层,并具有多种假设功能。然而,染色体体的组成、生物合成和进化起源仍然知之甚少。研究了叶蝉被绒毛绒小体(IBs)的一般化学和物理特性,确定了IBs的成分,鉴定了参与绒小体蛋白质合成的独特基因,并探讨了绒小体蛋白质合成与食物来源氨基酸组成之间的潜在关联,以及内共生体在绒小体产生中的可能作用。结果表明,IBs主要由富含甘氨酸和酪氨酸的蛋白质和一些金属元素组成,含有昆虫必需和非必需氨基酸(EAAs和NEAAs),包括昆虫唯一食物来源缺乏的EAAs。所有参与合成12个brochosomal protein (bp)的12个unigenes均在MTs的腺段高度表达,证实了brochosomal是由该区段合成的。bp的合成是膜总科的关键突触形态之一,但在少数世系中可能是次要缺失的。BPs的合成可能与叶蝉/树蝉与内共生体的共生有关,这些内共生体为叶蝉/树蝉提供eaa,包括那些缺乏单一饲料(即植物汁液)且只能由共生体提供的eaa。我们假设MTs的功能修饰与bp的应用相结合,使膜纲能够定植和适应新的生态位,并进化到这个半纲类群(特别是蝉科)的急剧多样化。本研究强调了mt的进化可塑性和多种功能在驱动半翅目吸液昆虫适应和进化中的重要性。
期刊介绍:
This international journal publishes original contributions and mini-reviews in the fields of insect biochemistry and insect molecular biology. Main areas of interest are neurochemistry, hormone and pheromone biochemistry, enzymes and metabolism, hormone action and gene regulation, gene characterization and structure, pharmacology, immunology and cell and tissue culture. Papers on the biochemistry and molecular biology of other groups of arthropods are published if of general interest to the readership. Technique papers will be considered for publication if they significantly advance the field of insect biochemistry and molecular biology in the opinion of the Editors and Editorial Board.