An axial Hox code controls tissue segmentation and body patterning in Nematostella vectensis

Abstract

Hox genes encode conserved developmental transcription factors that govern anterior-posterior (A-P) pattering in diverse bilaterian animals, which display bilateral symmetry. Although Hox genes are also present within Cnidaria, these simple animals lack a definitive A-P axis, leaving it unclear how and when a functionally integrated Hox code arose during evolution. We used short hairpin RNA (shRNA)–mediated knockdown and CRISPR-Cas9 mutagenesis to demonstrate that a Hox-Gbx network controls radial segmentation of the larval endoderm during development of the sea anemone Nematostella vectensis. Loss of Hox-Gbx activity also elicits marked defects in tentacle patterning along the directive (orthogonal) axis of primary polyps. On the basis of our results, we propose that an axial Hox code may have controlled body patterning and tissue segmentation before the evolution of the bilaterian A-P axis.

Hedgehog signaling is required for endomesodermal patterning and germ cell development inNematostella vectensis

“…While the mechanism of primary mesentery 170 specification is unknown, this process likely lies downstream of Hox-dependent endomesodermal 171 segmentation in developing larvae. Interestingly, segmentation of the presumptive primary 172 mesenteries is disrupted in both Anthox6a mutants and Gbx shRNA-KD polyps(He et al, 2018). 173In both loss of function conditions, we observed aberrant attachment of the septal filaments and 174 the associated induction of PGC clusters in non-primary septa (Fig.…”

“…Generation of mutant lines by CRISPR/Cas9 mutagenesis 404 hh1 and ptc mutant lines were generated using established methods (He et al, 2018). In brief, 405…”

“…2C, Fig. 3B-B';He et al, 2018). The direction of this initial 110 migration was away from the high BMP activity domain along the directive axis(Genikhovich et 111 al., 2015), suggesting the potential existence of attractive/repulsive signals for migratory PGCs.…”

“…Among 50 cnidarians, the sea anemone Nematostella vectensis maintains distinct adult gonad tissue and 51 features PGC specification dynamics hypothesized to partially reflect ancient epigenesis based 52 on expression patterns of conserved germline genes (Extavour et al, 2005). Additionally, a well-53 annotated genome (Putnam et al, 2007), defined developmental stages (Fritzenwanker et al, 54 2007) and diverse genetic tools (Ikmi et al, 2014;Renfer and Technau, 2017;He et al, 2018;55 Karabulut et al, 2019) make Nematostella a genetically tractable model to elucidate 56 developmental mechanisms controlling PGC specification. 57…”

Hox gene expression during the development of the phoronidPhoronopsis harmeri

“…Although expression of Hox genes has been described during embryonic and larval development of many animals representing diverse evolutionary lineages (4,, there are still some clades for which information about Hox expression during development is lacking. Among them are phoronids, marine, sessile worms, which feed using a specialized filter apparatus, the so-called lophophore (lp in Fig.…”