History of a prolific family: the Hes/Hey-related genes of the annelid Platynereis

Abstract

BackgroundThe Hes superfamily or Hes/Hey-related genes encompass a variety of metazoan-specific bHLH genes, with somewhat fuzzy phylogenetic relationships. Hes superfamily members are involved in a variety of major developmental mechanisms in metazoans, notably in neurogenesis and segmentation processes, in which they often act as direct effector genes of the Notch signaling pathway.ResultsWe have investigated the molecular and functional evolution of the Hes superfamily in metazoans using the lophotrochozoan Platynereis dumerilii as model. Our phylogenetic analyses of more than 200 Metazoan Hes/Hey-related genes revealed the presence of five families, three of them (Hes, Hey and Helt) being pan-metazoan. Those families were likely composed of a unique representative in the last common metazoan ancestor. The evolution of the Hes family was shaped by many independent lineage specific tandem duplication events. The expression patterns of 13 of the 15 Hes/Hey-related genes in Platynereis indicate a broad functional diversification. Nevertheless, a majority of these genes are involved in two crucial developmental processes in annelids: neurogenesis and segmentation, resembling functions highlighted in other animal models.ConclusionsCombining phylogenetic and expression data, our study suggests an unusual evolutionary history for the Hes superfamily. An ancestral multifunctional annelid Hes gene may have undergone multiples rounds of duplication-degeneration-complementation processes in the lineage leading to Platynereis, each gene copies ensuring their maintenance in the genome by subfunctionalisation. Similar but independent waves of duplications are at the origin of the multiplicity of Hes genes in other metazoan lineages.

Phylogenetics of Lophotrochozoan bHLH Genes and the Evolution of Lineage-Specific Gene Duplicates

“…(2012), also fell into Group D and we include it here in table 1. Group E genes encode a hairy/orange domain as well as the bHLH domain and include the Hey and Hes families, with well-defined roles in Notch signaling, as well as the more recently described Clockwork orange gene family which is absent from H. sapiens and other vertebrates (Gyoja and Satoh 2013), and a fourth gene family known as Heylike ( HeyL ) or HELT (Gazave et al. 2014; Gyoja 2014).…”

“…Phylogenetic trees focused on the Group E genes have previously proven insufficiently supported to convincingly determine whether this reflects common ancestry or parallel cluster evolution, though some lineage-specific tandem duplication is supported for some species (Minguillon et al. 2003; Gazave et al. 2014).…”

Annelida

“…Similarly, Notch is also expressed in teloblasts and blast cells, and functional studies revealed that the disruption of the Notch / hairy signaling results in a disruption of segmentation (Song et al 2004 ;Rivera and Weisblat 2009 ). For Platynereis dumerilii , 15 hairy paralogs could be identifi ed, which are expressed in mesodermal tissue, forming segments, and during neurogenesis, where it may be involved in the patterning of the nervous system (Gazave et al 2014 ). However, these authors also found no overlap with the expression of Notch .…”

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

“…Further evidence of a common, and likely homologous, molecular profile comes from expression of the homeodomain gene Arx, the zinc finger Zic, and components of the Notch signaling pathway. These genes are expressed at each chaetae sac territory in the Platynereis larva (62,64), in C. teleta (63,65), and also in the region of the forming chaetae sac territories in T. transversa (Fig. 6 A-L and Fig.…”

“…Brachiopods and annelids share the expression of lab and Post1 in the chaetal sacs (26,43,61). To further analyze these molecular similarities, we identified and studied the expression of the homeodomain-containing transcription factor Arx, the zinc finger Zic, and components of the Notch signaling pathway, all of which are associated with the development of chaetae in annelids (62)(63)(64)(65). Arx was specifically expressed in the developing and mature chaetal sacs (Fig.…”