Institute of Biology, Leiden University, Sylviusweg 72, Leiden 2333 BE, The Netherlands.
Max Planck Institute for Chemical Ecology, Hans Knöll Straße 8, Jena 07745, Germany.
Philos Trans R Soc Lond B Biol Sci. 2022 Dec 5;377(1865):20210266. doi: 10.1098/rstb.2021.0266. Epub 2022 Oct 17.
Insects comprise more than a million species and many authors have attempted to explain this success by evolutionary innovations. A much overlooked evolutionary novelty of insects is the serosa, an extraembryonic epithelium around the yolk and embryo. We have shown previously that this epithelium provides innate immune protection to eggs of the beetle It remained elusive, however, whether this immune competence evolved in the lineage or is ancestral to all insects. Here, we expand our studies to two hemimetabolous insects, the bug and the swarming grasshopper . For , RNA sequencing reveals an extensive response upon infection, including the massive upregulation of antimicrobial peptides (AMPs). We demonstrate antimicrobial activity of these peptides using bacterial growth assays and describe two novel AMP families called Serosins and Ovicins. For both insects, quantitative polymerase chain reaction shows immune competence of the eggs when the serosa is present, and hybridizations demonstrate that immune gene expression is localized in the serosa. This first evidence from hemimetabolous insect eggs suggests that immune competence is an ancestral property of the serosa. The evolutionary origin of the serosa with its immune function might have facilitated the spectacular radiation of the insects. This article is part of the theme issue 'Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom'.
昆虫包含超过一百万种物种,许多作者试图通过进化创新来解释这种成功。昆虫的一个被忽视的进化新奇之处是浆膜,即围绕蛋黄和胚胎的外胚层上皮。我们之前已经表明,这种上皮为甲虫的卵提供了先天免疫保护。然而,这种免疫能力是在鞘翅目谱系中进化而来的,还是所有昆虫的祖先,仍然难以捉摸。在这里,我们将研究扩展到两种半变态昆虫,即臭虫和 swarm 草蜢。对于臭虫,RNA 测序显示感染后会产生广泛的反应,包括抗菌肽 (AMP) 的大量上调。我们使用细菌生长测定法证明了这些肽的抗菌活性,并描述了两种新的 AMP 家族,称为 Serosins 和 Ovicins。对于这两种昆虫,定量聚合酶链反应显示当浆膜存在时卵具有免疫能力,并且杂交显示免疫基因表达定位于浆膜中。这是半变态昆虫卵中首次出现的免疫能力的证据,表明免疫能力是浆膜的一个祖征。具有免疫功能的浆膜的进化起源可能促进了昆虫的惊人辐射。本文是主题问题“胚外组织:探索动物王国的概念、定义和功能”的一部分。