Immune function of the serosa in hemimetabolous insect eggs

Jacobs, Chris G.C.; Hulst, Remy van der; Chen, Yen-Ta; Williamson, Ryan P.; Roth, Siegfried; Zee, Maurijn van der

doi:10.1101/2021.09.27.462031

Cited by 4 publications

(5 citation statements)

References 73 publications

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“…Data accessibility. The data are provided in the electronic supplementary material [79]. The sequencing data discussed in this publication have been deposited in NCBI's Gene Expression Omnibus [33] and are accessible through GEO series accession number GSE100429 (https://www.…”

Section: Discussionmentioning

confidence: 99%

Immune function of the serosa in hemimetabolous insect eggs

Jacobs

Hulst

Chen

et al. 2022

Phil. Trans. R. Soc. B

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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 Tribolium castaneum. It remained elusive, however, whether this immune competence evolved in the Tribolium lineage or is ancestral to all insects. Here, we expand our studies to two hemimetabolous insects, the bug Oncopeltus fasciatus and the swarming grasshopper Locusta migratoria . For Oncopeltus , RNA sequencing reveals an extensive response upon infection, including the massive upregulation of antimicrobial peptides (AMPs). We demonstrate antimicrobial activity of these peptides using in vitro 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 in situ 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’.

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Section: Discussionmentioning

confidence: 99%

Immune function of the serosa in hemimetabolous insect eggs

Jacobs

Hulst

Chen

et al. 2022

Phil. Trans. R. Soc. B

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“…to be adaptive and related to certain environments or behaviours (Briscoe et al 2013;Cheng et al 2017;Rane et al 2019;Chakraborty et al 2021). The Shx genes are expressed in the serosa during development, an extraembryonic tissue implicated in innate immunity and desiccation resistance in insects (Panfilio 2008;Jacobs et al 2013Jacobs et al , 2014Jacobs et al , 2022. It is therefore possible that Shx duplication is an adaptation associated with modifications to the egg, and indeed many of the highly duplicated genes show increased rates of sequence evolution (Figure 4A).…”

Section: Moths Take the Record For The Most Hox Locimentioning

confidence: 99%

Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera

et al. 2022

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Homeobox genes encode transcription factors with essential roles in patterning and cell fate in developing animal embryos. Many homeobox genes, including Hox and NK genes, are arranged in gene clusters, a feature likely related to transcriptional control. Sparse taxon sampling and fragmentary genome assemblies mean that little is known about dynamics of homeobox gene evolution across Lepidoptera, or how changes in homeobox gene number and organization relate to diversity in this large order of insects. Here we analyze an extensive dataset of high-quality genomes to characterize the number and organization of all homeobox genes in 123 species of Lepidoptera from 23 taxonomic families. We find most Lepidoptera have around 100 homeobox loci, including an unusual Hox gene cluster in which the lab gene is repositioned and therogene is next topb. A topologically associating domain spans much of the gene cluster, suggesting deep regulatory conservation of the Hox cluster arrangement in this insect order. Most Lepidoptera have four Shx genes, divergentzen-derived loci, but these loci underwent dramatic duplication in several lineages with some moths having over 165 homeobox loci in the Hox gene cluster; this expansion is associated with local LINE element density. In contrast, the NK gene cluster content is more stable, although there are differences in organization compared to other insects, and major rearrangements within butterflies. Our analysis represents the first description of homeobox gene content across the order Lepidoptera, exemplifying the potential of newly generated genome assemblies for understanding genome and gene family evolution.

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“…[48,51]). Downstream, RNA-seq after RNAi and pathogen-challenge studies have identified factors for serosal tissue maturation and physiology [24,55,56].…”

Section: Deciphering the Genetic Signature Of The Amnionmentioning

confidence: 99%

“…Many purported tissue-scale functions of polyploidy are probably applicable in this outer EE tissue. Serosal tissue integrity as a barrier epithelium of large cells confers cellular protection via detoxification [130] and innate immune responses to infection [55,56]. Furthermore, in many insect species, the serosa secretes a substantial cuticle that provides desiccation resistance [131–133] and mechanical protection [24].…”

Section: Polyploid Genomic Architectures Underpin Extraembryonic Tiss...mentioning

confidence: 99%

The extended analogy of extraembryonic development in insects and amniotes

Panfilio

Lopes

2022

Phil. Trans. R. Soc. B

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It is fascinating that the amnion and serosa/chorion, two extraembryonic (EE) tissues that are characteristic of the amniote vertebrates (mammals, birds and reptiles), have also independently evolved in insects. In this review, we offer the first detailed, macroevolutionary comparison of EE development and tissue biology across these animal groups. Some commonalities represent independent solutions to shared challenges for protecting the embryo (environmental assaults, risk of pathogens) and supporting its development, including clear links between cellular properties (e.g. polyploidy) and physiological function. Further parallels encompass developmental features such as the early segregation of the serosa/chorion compared to later, progressive differentiation of the amnion and formation of the amniotic cavity from serosal–amniotic folds as a widespread morphogenetic mode across species. We also discuss common developmental roles for orthologous transcription factors and BMP signalling in EE tissues of amniotes and insects, and between EE and cardiac tissues, supported by our exploration of new resources for global and tissue-specific gene expression. This highlights the degree to which general developmental principles and protective tissue features can be deduced from each of these animal groups, emphasizing the value of broad comparative studies to reveal subtle developmental strategies and answer questions that are common across species. This article is part of the theme issue ‘Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom’.

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Immune function of the serosa in hemimetabolous insect eggs

Cited by 4 publications

References 73 publications

Immune function of the serosa in hemimetabolous insect eggs

Immune function of the serosa in hemimetabolous insect eggs

Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera

The extended analogy of extraembryonic development in insects and amniotes

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