Discovery of methylfarnesoate as the annelid brain hormone reveals an ancient role of sesquiterpenoids in reproduction

Abstract

Animals require molecular signals to determine when to divert resources from somatic functions to reproduction. This decision is vital in animals that reproduce in an all-or-nothing mode, such as bristle worms: females committed to reproduction spend roughly half their body mass for yolk and egg production; following mass spawning, the parents die. An enigmatic brain hormone activity suppresses reproduction. We now identify this hormone as the sesquiterpenoid methylfarnesoate. Methylfarnesoate suppresses transcript levels of the yolk precursor Vitellogenin both in cell culture and in vivo, directly inhibiting a central energy–costly step of reproductive maturation. We reveal that contrary to common assumptions, sesquiterpenoids are ancient animal hormones present in marine and terrestrial lophotrochozoans. In turn, insecticides targeting this pathway suppress vitellogenesis in cultured worm cells. These findings challenge current views of animal hormone evolution, and indicate that non-target species and marine ecosystems are susceptible to commonly used insect larvicides.DOI: http://dx.doi.org/10.7554/eLife.17126.001

Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction in Annelida

“…7A). In agreement with Schenk et al (2016), our results also confirmed that annelid MTr is clearly an ortholog of insects and crustaceans MTrs (Fig. 7A).…”

“…In the annelid C. teleta, exogenous extracts of MF were found to affect larval metamorphosis and settlement (Laufer and Biggers 2001), and MF has been recently demonstrated to be directly involved in P. dumerilii regeneration and female sexual maturation (Schenk et al 2016). This latter study not only showed that the decrease of MF levels in the brain induces reproduction and suppresses regenerative capacities in P. dumerilii, but it also reported an ortholog of the MF receptor of arthropods (bHLH-PAS-domain-containing transcription factor methoprene-tolerant receptor, MTr) in the eleocytes (coelomic cells that synthesize yolk via production of Vtg protein), demonstrating that this hormone is not restricted to arthropods, as it was assumed (Schenk et al 2016).…”

“…In the annelid C. teleta, exogenous extracts of MF were found to affect larval metamorphosis and settlement (Laufer and Biggers 2001), and MF has been recently demonstrated to be directly involved in P. dumerilii regeneration and female sexual maturation (Schenk et al 2016). This latter study not only showed that the decrease of MF levels in the brain induces reproduction and suppresses regenerative capacities in P. dumerilii, but it also reported an ortholog of the MF receptor of arthropods (bHLH-PAS-domain-containing transcription factor methoprene-tolerant receptor, MTr) in the eleocytes (coelomic cells that synthesize yolk via production of Vtg protein), demonstrating that this hormone is not restricted to arthropods, as it was assumed (Schenk et al 2016). Since detection of MF is not possible in RNAseq data, in order to assess whether S. magadalena could use a similar molecular signal to determine when to divert resources from somatic functions to reproduction, we investigated if S. magdalena also possessed an ortholog of MTr, identified as the arthropod and lophotrochozoan sesquiterpenoid receptor (e.g., Konopova and Jindra 2007;Miyakawa et al 2013;Jindra et al 2015;Schenk et al 2016).…”

“…4 sesquiterpenoid methyl farnesoate (MF), the brain neurohormone that directly regulates Vtg in yolk production of P. dumerilii females, therefore influencing the correct development of oocytes (Schenk et al 2016). Particularly, a decrease in MF levels in the brain of P. dumerilii during reproduction allowed oocyte maturation but suppressed normal somatic functions and caudal regenerative capacities (Schenk et al 2016). In crustaceans, MF has been showed to play essential roles in development and reproduction (Xie et al 2016), similar to the role of Juvenile Hormone (JH) in insects (Riddiford 1994;Wyatt and Davey 1996).…”

“…Hormonal factors have also been suggested to drive the sexual differentiation of the stolon (Franke 1980;Heacox and Schroeder 1982), in particular the female stolon, given that it seems that male stolon differentiation occurs autonomously, whereas female stolon differentiation may depend on hormone release by male stolons (Franke 1999). However, no candidate hormone has been proposed to control reproduction and regeneration processes in syllids, although it seems clear that there might be several involved, not only in the brain, but also in the proventricle (e.g., Schroeder and Hermans 1975;Franke 1999;Weidhase et al 2016) In summary, although molecular mechanisms underlying reproduction are relatively well studied in a few annelids (e.g., Kang et al 2002;Thamm and Seaver 2008;Giani et al 2011;Novo et al 2013;Schenk et al 2016), the molecular toolkit involved in the stolonization process of syllids has not been examined yet. Thus, our aim in the present study is to provide a first glimpse into the gene expression patterns occurring during the stolonization process in the syllid species Syllis magdalena.…”