Expression of a Musashi‐like gene in sexual and asexual development of the colonial chordate Botryllus schlosseri and phylogenetic analysis of the protein group

Abstract

Tunicates are the unique chordates to possess species reproducing sexually and asexually. Among them, the colonial ascidian Botryllus schlosseri is a reference model for the study of similarities and differences in these two developmental pathways. We here illustrate the characterization and expression pattern during both pathways of a transcript for a gene orthologous to Dazap1. Dazap1 genes encode for RNA-binding proteins and fall into the Musashi-like (Msi-like) group. Our phylogenetic analysis shows that these are related to other RNA-binding proteins (Tardbp and several heterogeneous nuclear ribonucleoproteins types) that share the same modular domain structure of conserved tandem RNA Recognition Motifs (RRMs). We also classify the whole group as derived from a single ancient duplication of the RRM. Our results also show that Dazap1 is expressed with discrete spatiotemporal pattern during embryogenesis and blastogenesis of B. schlosseri. It is never expressed in wholly differentiated tissues, but it is located in all bud tissues and in different spatiotemporally defined territories of embryos and larva. These expression patterns could indicate different roles in the two processes, but an intriguing relationship appears if aspects of cell division dynamics are taken into account, suggesting that it is related to the proliferative phases in all tissues, and raising a similarity with known Dazap1 orthologs in other metazoans.

Asymmetric Distribution of pl10 and bruno2, New Members of a Conserved Core of Early Germline Determinants in Cephalochordates

“…Although the evolutionary history of RRM domain containing proteins is complex, orthologs of musashi-related genes have been identified from sponge to human (Gasparini et al, 2011;Okamoto et al, 2012), including lancelets (Gasparini et al, 2011, this study). One of the principal findings of this study is that cephalochordates appear to have lost the ortholog of DAZAP, as we were unable to identify the gene in either the genomes of B. floridae or B. belcheri.…”

“…As we were interested specifically in stem cell-related Musashi, and relationships among Musashi-related protein families are complex (Gasparini et al, 2011) we generated phylogenies utilizing the available full length B. floridae and B. belcheri sequences, and included putative Saccoglossus kowalevski orthologs. We clearly identified sequences belonging to the TARDBP43 and hnrpA3/hnrpD clades (Figure 2).…”

The involvement of three signal transduction pathways in botryllid ascidian astogeny, as revealed by expression patterns of representative genes

“…Both astogeny and ontogeny form similar bodily structures (Manni and Burighel, 2006), including axial polarity and colonial patterning, all adhering to the rules of stem cell proliferation and differentiation. Therefore, it is assumed that basic evolutionary traits, like STPs, could be shared between embryogenesis and astogeny (such as blastogenesis; Gasparini et al, 2011), as well as with major regeneration routes (Rinkevich et al, 2008), taking also into account that modulation of Wnt/b-catenin, MAPK/Erk and TGF-b pathways enhances somatic cell reprogramming in ways that are still poorly understood (Sanges and Cosma, 2010). Colonial ascidians, with their recurring blastogenic cycles and their close relationship with the vertebrates, are thus excellent models for studying these relationships.…”

“…However, while studies (e.g., Berrill, 1941a,b;Izzard, 1973;Sabbadin et al, 1975;Lauzon et al, 2002) have already described major routes in the botryllid ascidian astogeny, knowledge regarding the molecular programs in colonial ascidians is limited. Tiozzo et al, (2005) studied the expression of pitx (pituitary homeobox gene) and Gasparini et al, (2011) studied the outcomes for the expression of a Musashi-like gene in blastogenesis and embryogenesis. pmERK (MAPK pathway) and pmb-CTN (b-catenin orthologue) were shown to be strongly induced in Polyandrocarpa misakiensis trans-differentiating buds (Kawamura et al, 2013) following RA treatment.…”

“…Therefore, when we look at the yet unknown cellular and molecular pathways, patterns, and rules which impose astogeny in colonial organisms, it is clear that elucidating the operation of astogeny associated developmental gene families is of fundamental interest, because the same gene families may have shaped ontogeny (e.g., Gasparini et al, 2011). One of the preferred investigatory approaches utilizes Signal Transduction Pathways (STPs).…”