Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa)

Abstract

The bilaterian animals are divided into three great branches: the Deuterostomia, Ecdysozoa, and Lophotrochozoa. The evolution of developmental mechanisms is less studied in the Lophotrochozoa than in the other two clades. We have studied the expression of Hox genes during larval development of two lophotrochozoans, the polychaete annelids Nereis virens and Platynereis dumerilii. As reported previously, the Hox cluster of N. virens consists of at least 11 genes (de Rosa R, Grenier JK, Andreeva T, Cook CE, Adoutte A, Akam M, Carroll SB, Balavoine G, Nature, 399:772-776, 1999; Andreeva TF, Cook C, Korchagina NM, Akam M, Dondua AK, Ontogenez 32:225-233, 2001); we have also cloned nine Hox genes of P. dumerilii. Hox genes are mainly expressed in the descendants of the 2d blastomere, which form the integument of segments, ventral neural ganglia, pre-pygidial growth zone, and the pygidial lobe. Patterns of expression are similar for orthologous genes of both nereids. In Nereis, Hox2, and Hox3 are activated before the blastopore closure, while Hox1 and Hox4 are activated just after this. Hox5 and Post2 are first active during the metatrochophore stage, and Hox7, Lox4, and Lox2 at the late nectochaete stage only. During larval stages, Hox genes are expressed in staggered domains in the developing segments and pygidial lobe. The pattern of expression of Hox cluster genes suggests their involvement in the vectorial regionalization of the larval body along the antero-posterior axis. Hox gene expression in nereids conforms to the canonical patterns postulated for the two other evolutionary branches of the Bilateria, the Ecdysozoa and the Deuterostomia, thus supporting the evolutionary conservatism of the function of Hox genes in development.

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

“…In this context, the anterior Hox gene lab is expressed in the chaetae of Chaetopterus sp. (26) and in the ectoderm around chaetal sacs in N. virens (61), and Post1 is expressed in the chaetae of C. teleta, Platynereis dumerilii, and N. virens (43,61). Our results show that, similarly, lab and Post1 are expressed specifically in the chaetal sacs of the brachiopods T. transversa and N. anomala (Figs.…”

“…Although a general trend toward spatial collinearity is present (e.g., the posterior Hox genes are expressed in posterior tissues), the early expression of Hox3 breaks temporal collinearity in T. transversa, whereas it is pb that is first expressed in N. anomala. In both species, Lox5 is also expressed before Scr, as it is also the case in the annelid Nereis virens (61). Ectodermal spatial collinearity is absent in the two brachiopods even when the future location of the larval tissues after metamorphosis is considered (75,76).…”

“…In the other investigated spiralians, there is only either genomic information (e.g., the mollusks L. gigantea and C. gigas) or expression analysis (e.g., the mollusks Gibbula varia and Haliotis asinina) (16,44,49,54). Most of these previous gene expression studies have demonstrated coordinated spatial or temporal expression of Hox genes along the animal's anteroposterior axis (45,46,61) or in organ systems, such the nervous system (49,54). However, the absence of studies revealing a correlation between Hox gene expression and their genomic organization in these animals hinders reconstruction of the putative mechanisms that preserve Hox clusters in Lophotrochozoa, and thus preclude generalizations about possible scenarios of Hox cluster evolution across all animals.…”

“…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).…”

Annelids in evolutionary developmental biology and comparative genomics

“…It has been hypothesised that mechanisms producing the progressive temporal sequence of activation of Hox genes along a cluster (Temporal Colinearity) are responsible for the principle constraint on ordered clusters (reviewed in Ferrier & Holland, 2002;Ferrier & Minguillón, 2003), even if these mechanisms might not be homologous across the animal kingdom (Ferrier, 2007;Monteiro & Ferrier, 2006). This hypothesis has recently been questioned by Hox expression data from the polychaetes Platynereis dumerilii and Nereis virens (Kulakova et al, 2007), in which spatial colinearity seemed to be more apparent than temporal colinearity. The major caveat in interpreting such expression data is whether the organisation of the Hox genes is known.…”