Expansion of TALE homeobox genes and the evolution of spiralian development

Abstract

Spiralians, including molluscs, annelids and platyhelminths, share a unique development process that includes the typical geometry of early cleavage and early segregation of cell fate in blastomeres along the animal-vegetal axis. However, the molecular mechanisms underlying this early cell fate segregation are largely unknown. Here, we report spiralian-specific expansion of the three-amino-acid loop extension (TALE) class of homeobox genes. During early development, some of these TALE genes are expressed in staggered domains along the animal-vegetal axis in the limpet Nipponacmea fuscoviridis and the polychaete Spirobranchus kraussii. Inhibition or overexpression of these genes alters the developmental fate of blastomeres, as predicted by the gene expression patterns. These results suggest that the expansion of novel TALE genes plays a critical role in the establishment of a novel cell fate segregation mechanism in spiralians.

A Revised Spiralian Homeobox Gene Classification Incorporating New Polychaete Transcriptomes Reveals a Diverse TALE Class and a Divergent Hox Gene

“…2015) and a selection of other available lophotrochozoan genomes. We expand and modify Paps et al.’s (2015) system of lophotrochozoan homeobox classification, and compare and reconcile it with Morino et al.’s (2017) overlapping classification. We describe a surprising diversity of novel and difficult to classify homeobox genes in the transcriptomes of operculum regeneration, including members of a Spiralia-specific TALE-class gene radiation, a novel homeobox gene family restricted to lophotrochozoans, and an extremely divergent Hox gene.…”

“…To these were added sequences from Paps et al.’s (2015) recent classification of spiralian TALE families, SPILE (Spiralian TALE) sequences from the NCBI database (Morino et al. 2017), and canonical TALE class family sequences.…”

“… Note .—In the Origin column, “N” denotes that the sequence is newly discovered by this analysis, “P” that the sequence was included in Paps et al.’s (2015) analysis, and “M” that the sequences were described by Morino et al. (2017).…”

“…To fulfil the purpose of identifying the difficult-to-classify genes in the S. lamarcki regenerative transcriptomes, we elected to sample only then-available lophotrochozoan (sensu stricto) genomes, excluding the TALE and PRD sequences from Platyhelminthes and Rotifera included in earlier analyses (Paps et al . 2015; Morino et al. 2017).…”

“…However, a reconciliation of the Paps et al. (2015) and Morino et al. (2017) data sets and nomenclatures has not yet been attempted.…”