Sexual and asexual development: two distinct programs producing the same tunicate

Abstract

SUMMARY Colonial tunicates are the only chordate that possess two distinct developmental pathways to produce an adult body: either sexually through embryogenesis or asexually through a stem cell-mediated renewal termed blastogenesis. Using the colonial tunicate Botryllus schlosseri , we combine transcriptomics and microscopy to build an atlas of the molecular and morphological signatures at each developmental stage for both pathways. The general molecular profiles of these processes are largely distinct. However, the relative timing of organogenesis and ordering of tissue-specific gene expression are conserved. By comparing the developmental pathways of B. schlosseri with other chordates, we identify hundreds of putative transcription factors with conserved temporal expression. Our findings demonstrate that convergent morphology need not imply convergent molecular mechanisms but that it showcases the importance that tissue-specific stem cells and transcription factors play in producing the same mature body through different pathways.

Revealing conserved mechanisms of neurodegeneration in a colonial chordate

“…muscle cells in the zooid body wall and heart, and ciliated cells in the oral siphon, branchial sac and gut [23][24][25][26][27][28] . During the weekly cycle of development and degeneration, new brains develop in each growing bud as the brains of older adult zooids degenerate 7,29 .…”

“…Following quality control filters, reads were aligned to the B. schlosseri transcriptome 37 and gene counts determined. A custom algorithm was used to identify genes that had differential expression (DE) between different days of the blastogenic cycle in young colonies 7 .…”

“…Unlike most species where the body is long-lived and maintained by cellular replacements, a B. schlosseri colony regenerates new zooids on a weekly basis and its stem cells persist for its entire life 40 . Putative adult stem cells mediate bud development 31,[41][42][43] and recent transcriptome analyses suggest that these stem cells are tissue specific 7 . For this reason, we investigated the genes included in the mammalian "neural stem cell (NSC) and lineage-specific pathway" 38 and found that 27 putative homologous genes are expressed in B. schlosseri brain (Fig.…”

Stem Cells and Innate Immunity in Aquatic Invertebrates: Bridging Two Seemingly Disparate Disciplines for New Discoveries in Biology

“…In Botryllus schlosseri, a model species for the study of immunobiology (Figure 5A), allorecognition and asexual reproduction, including whole-body regeneration (119,(129)(130)(131), colonies increase their size through periodical cycles of asexual reproduction requiring the involvement of stem cells. Unlike most species, where the body is long-lived and maintained by cellular replacement, B. schlosseri regenerates new colonial units (buds) on a biweekly basis from stem cells that remain for life, replacing the previous generation's zooids and, partly, the circulatory cells (129,(132)(133)(134)(135)(136)(137), Circulating immune cells influence the process as they assure the crosstalk between blastogenic generations at the generation change (takeover) (Figure 5D): cytotoxic MCs increase the transcription of the complement factor 3 (C3) and stimulate phagocytosis, required for the removal of apoptotic cells in tissues of old zooids (138,139). Phagocytes are also required for the completion of the takeover and the formation of new buds as the prevention of phagocytosis blocks the process (140).…”

Distinct gene expression dynamics in developing and regenerating limbs

“…Fold enrichment scores were computed as follows: we took an approach inspired from the one described in Kowarsky et al (2021) where they use an hypergeometric distribution to estimate an enrichment score between gene sets. The enrichment fold was calculated as the ratio of the number of genes that overlapped between two clusters over the size of an overlap that would occur with random sets of genes of the same size.…”