Halloween genes in panarthropods and the evolution of the early moulting pathway in Ecdysozoa

Abstract

Moulting is a characteristic feature of Ecdysozoa—the clade of moulting animals that includes the hyperdiverse arthropods and less speciose groups, such as onychophorans, tardigrades and nematodes. Moulting has been best analysed in arthropods, specifically in insects and crustaceans, in which a complex neuroendocrine system acts at the genomic level and initiates the transcription of genes responsible for moulting. The key moulting hormones, ecdysone and 20-hydroxyecdysone, are subsequently synthesized from cholesterol ingested with food. Their biosynthesis is regulated by the Rieske-domain protein Neverland and cytochrome P450 enzymes encoded by the so-called ‘Halloween’ genes. Ecdysone is then released into the haemolymph and modified into 20-hydroxyecdysone, which binds to the nuclear receptor EcR/USP and initiates transcription of the Early genes. As little is known about the moulting pathway of other ecdysozoans, we examined the occurrence of genes involved in ecdysteroid biosynthesis and the early moulting cascade across ecdysozoan subgroups. Genomic and transcriptomic searches revealed no Halloween genes in cycloneuralians, whereas only shadow (CYP315A1) is present in onychophorans and tardigrades, suggesting that the Halloween genes evolved stepwise in panarthropods. These findings imply that the genes which were responsible for the ecdysteroid biosynthesis in the last common ancestor of Ecdysozoa are currently unknown.

Establishment of a marine nematode model for animal functional genomics, environmental adaptation and developmental evolution

“…Systematic detection of such differences and understanding of their roles in vivo remains a significant challenge. elegans and most free-living nematodes (Schumann et al 2018), were found in L. marina (further confirmed by both RNA-Seq data and genomic PCR). Ecdysteroid signaling was widely observed in filarial parasitic nematodes and putative homologs of RXR and EcR were also identified in beetle-associated nematode P. pacificus and its relative species (Parihar et al 2010;Kostrouchova and Kostrouch 2015;Prabh et al 2018).…”

Origin of ecdysis: fossil evidence from 535-million-year-old scalidophoran worms

“…The occurrence of moulting in early scalidophorans suggests that these animals had already acquired a genetic tool-kit and possibly a neuroendocrine system to achieve ecdysis. Although little is known about the molecular control of moulting in scalidophoran worms, a recent molecular study has shed light on key evolutionary aspects of ecdysis [18]. Scalidophorans possess genes that are known to play a key role in the moulting process of other ecdysozoan taxa (e.g.…”

“…The moulting hormone 20E also occurs in non-ecdysozoan animals (e.g. platyhelminthes, annelids and molluscs) and may have been present in the last common ancestor (LCA) of protostomes [18,[74][75][76][77]. This set of recent molecular data suggests that the early evolution of ecdysis includes a suite of molecular innovations possibly starting with the occurrence of Early genes in the LCA of protostomes and continuing throughout the three ecdysozoan clades (acquisition of the EcR/USP complex and Halloween genes; figure 4).…”

“…Thus, ecdysis may have been selected as the most adequate solution to overcome these mechanical constraints, and may have opened up new evolutionary opportunities. Ecdysis implies molecular innovations probably inherited from genetic elements were already present in non-moulting ancestors (figure 4), an [18,19,78]). Numbers at nodes represent possible genetic innovations in the early evolution of ecdysis.…”

“…tanning and biomineralization) of new cuticle, as well as shedding of exuvia [13 -17] and the neuroendocrine process responsible for it [18]. Recently, genomic and transcriptomic studies have shed new light on the molecular pathways involved in ecdysis, which development has paved the way for the formulation of detailed evolutionary scenarios [18,19]. The two critical steps of ecdysis are separation of the old cuticle from the underlying epidermal cells and splitting of the cuticle along predetermined lines of weakness, a process which allows the animal to extricate itself from its old exoskeleton.…”