Lineage-specific, fast-evolving GATA-like gene regulates zygotic gene activation to promote endoderm specification and pattern formation in the Theridiidae spider

Abstract

Background The process of early development varies across the species-rich phylum Arthropoda. Owing to the limited research strategies for dissecting lineage-specific processes of development in arthropods, little is known about the variations in early arthropod development at molecular resolution. The Theridiidae spider, Parasteatoda tepidariorum, has its genome sequenced and could potentially contribute to dissecting early embryonic processes. Results We present genome-wide identification of candidate genes that exhibit locally restricted expression in germ disc forming stage embryos of P. tepidariorum, based on comparative transcriptomes of isolated cells from different regions of the embryo. A subsequent pilot screen by parental RNA interference identifies three genes required for body axis formation. One of them is a GATA-like gene that has been fast evolving after duplication and divergence from a canonical GATA family gene. This gene is designated fuchi nashi (fuchi) after its knockdown phenotypes, where the cell movement toward the formation of a germ disc was reversed. fuchi expression occurs in cells outside a forming germ disc and persists in the endoderm. Transcriptome and chromatin accessibility analyses of fuchi pRNAi embryos suggest that early fuchi activity regulates chromatin state and zygotic gene activation to promote endoderm specification and pattern formation. We also show that there are many uncharacterized genes regulated by fuchi. Conclusions Our genome-based research using an arthropod phylogenetically distant from Drosophila identifies a lineage-specific, fast-evolving gene with key developmental roles in one of the earliest, genome-wide regulatory events, and allows for molecular exploration of the developmental variations in early arthropod embryos.

Role of maternal spiralian‐specific homeobox gene SPILE‐E in the specification of blastomeres along the animal–vegetal axis during the early cleavage stages of mollusks

“…Increasing animal genomic information and annotations have revealed the existence of lineage-specific, fast-evolving transcription factors (Holland et al, 2017). Recent studies have reported several lineage-specific transcription factors that show zygotic expression during early development (Dylus et al, 2016;Ferguson et al, 2014;Iwasaki-Yokozawa et al, 2022;Lewin et al, 2021Lewin et al, , 2022Maeso et al, 2016;Yamazaki et al, 2020). In spiralians, many lineage-specific transcription factors are also known to exhibit peak expression during the early cleavage stages (Paps et al, 2015).…”

“…Although the developmental toolkit genes were once thought to be largely conserved among animals, recent genomic studies and curated annotations have revealed that lineage-specific and fast-evolving transcription factors are expressed during animal development (Holland et al, 2017), including in mammals (Lewin et al, 2021(Lewin et al, , 2022Maeso et al, 2016), echinoderms (Dylus et al, 2016;Yamazaki et al, 2020), lepidopterans (Chai et al, 2008;Ferguson et al, 2014;Mulhair et al, 2023), spiders (Iwasaki-Yokozawa et al, 2022), and spiralians (Morino, 2022;Morino et al, 2017;Paps et al, 2015;Phuangphong et al, 2021). In the examples above, most transcription factors are expressed zygotically and function early in animal development.…”

Single-cell RNA sequencing of mid-to-late stage spider embryos: new insights into spider development

“…In order to investigate genes (and thus gene regulatory networks) beyond the classic candidate gene approach, genomics and embryonic and tissue-specific transcriptomics have been applied in the recent past, leading to the investigation of complete gene families, orphan genes, fast evolving genes and tissue-specific genes (e.g. [ 20 , 77 , 89 , 142 , 155 ]. A relatively recent new technical innovation now allows investigation of the transcriptome of every cell of a given organism or a developmental stage of a given organism separately.…”

Publisher Correction: Lineage-specific, fast-evolving GATA-like gene regulates zygotic gene activation to promote endoderm specification and pattern formation in the Theridiidae spider

“…The original article [ 1 ] erroneously presented the supplementary materials in accordance with their respective citations; the supplementary files are now correctly presented and cited.…”