Histochemistry and transcriptomics of mucins and peritrophic membrane (PM) proteins along the midgut of a beetle with incomplete PM and their complementary function

IF 3.2 2区 农林科学 Q2 BIOCHEMISTRY & MOLECULAR BIOLOGY
Samira P. Ibrahim , Renata O. Dias , Clelia Ferreira , Carlos P. Silva , Walter R. Terra
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引用次数: 0

Abstract

The midgut of Zabrotes subfasciatus (Coleoptera) and other insects may have regions lacking a peritrophic membrane (matrix, PM) and covered with a jelly-like material known as peritrophic gel. This work was undertaken to test the hypothesis that the peritrophic gel is a vertebrate-like mucus. By histochemistry we identified mucins along the whole midgut, which contrasts with the known occurrence of PM only at the posterior midgut. We also analyzed the expression of the genes coding for mucus-forming mucins (Mf-mucins), peritrophins, chitin synthases and chitin deacetylases along the midgut and carcass (insect without midgut) by RNA-seq. Mf-mucins were identified as proteins with high O-glycosylation and multiple tandem repeats of Pro/Thr/Ser residues. Peritrophins were separated into PM proteins, cuticular proteins analogous to peritrophins (CPAPs) and ubiquitous-chitin-binding domain-(CBD)-containing proteins (UCBPs). PM proteins have at least 3, CPAP one or 3, and UCBPs have a varied number of CBDs. PM proteins are more expressed at midgut, CPAP at the carcass, and UCBP at both. The results showed that most PM proteins are mainly expressed at the posterior midgut, together with midgut chitin synthase and chitin deacetylase, and in agreement with the presence of PM only at the posterior midgut by visual inspection. The excretion of most midgut chitinase is avoided, suggesting that the shortened PM is functional. Mf-mucins are expressed along the whole midgut, probably forming the extracellular mucus layer observed by histochemistry. Thus, the lack of PM at anterior and middle midgut causes the exposure of a mucus, which may correspond to the previously described peritrophic gel. The putative functional interplay of mucus and PM is discussed. The major role of mucus is proposed to be tissue protection and of PM to enhancing digestive efficiency by allowing enzyme recycling.

Abstract Image

具有不完全PM的甲虫中肠粘蛋白和环营养膜(PM)蛋白的组织化学和转录组学及其互补功能。
Zabrotes subasciatus(鞘翅目)和其他昆虫的中肠可能有缺乏围生膜(基质,PM)的区域,并覆盖着一种称为围生凝胶的果冻状物质。这项工作是为了验证这样一种假设,即营养丰富的凝胶是一种类似脊椎动物的粘液。通过组织化学方法,我们鉴定了整个中肠的粘蛋白,这与已知仅在中肠后部出现PM形成了对比。我们还通过RNA-seq分析了编码粘液形成粘蛋白(Mf粘蛋白)、营养因子、几丁质合成酶和几丁质脱乙酰酶的基因在中肠和胴体(没有中肠的昆虫)上的表达。Mf粘蛋白被鉴定为具有高O-糖基化和Pro/Thr/Ser残基的多个串联重复的蛋白质。将周营养素分为PM蛋白、类似于周营养素的表皮蛋白(CPAP)和普遍存在的含有几丁质结合结构域(CBD)的蛋白(UCBP)。PM蛋白至少有3个,CPAP有1个或3个,UCBP有不同数量的CBD。PM蛋白在中肠表达更多,CPAP在胴体表达更多,UCBP在两者都表达更多。结果表明,大多数PM蛋白主要在中肠后部表达,与中肠几丁质合成酶和几丁质脱乙酰酶一起表达,肉眼观察与PM仅在中肠尾部表达一致。大多数中肠几丁质酶的排泄被避免,这表明缩短的PM是功能性的。Mf粘蛋白沿着整个中肠表达,可能通过组织化学观察形成细胞外粘液层。因此,中肠前部和中部PM的缺乏导致粘液的暴露,这可能对应于先前描述的围生凝胶。讨论了粘液和PM的假定功能相互作用。粘液的主要作用是保护组织,PM通过允许酶循环来提高消化效率。
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来源期刊
CiteScore
7.40
自引率
5.30%
发文量
105
审稿时长
40 days
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.
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