The potential role of juvenile hormone acid methyltransferase in methyl farnesoate (MF) biosynthesis in the swimming crab, Portunus trituberculatus

Abstract

Juvenile hormone (JH) and methyl farnesoate (MF) play essential roles in the development and reproduction of insects and crustaceans respectively. Juvenile hormone acid methyltransferase (JHAMT) catalyzes the methyl esterification in insect JH biosynthesis, while the corresponding step in crustacean MF biosynthesis was long thought to be catalyzed by farnesoic acid O-methyltransferase (FAMeT). However, the new discovery of JHAMT orthologs in crustaceans indicates that JHAMT may also play essential role in the MF biosynthesis in crustaceans. Here we cloned and characterized the full-length cDNA encoding JHAMT in the swimming crab Portunus trituberculatus (PtJHAMT). Sequence and structure analysis of PtJHAMT revealed that it was composed of a 6-stranded β sheet with 9 α helices, and contained a signature Sadenosyl-L-methionine (SAM) binding motif, which is the hallmark in all SAM dependent methyltransferases (SAM-MTs). Several active sites that are critical for the interaction of SAM and JH/FA substrate were also conserved in PtJHAMT. The gene expression of PtJHAMT was highly specific to the mandibular organ, which is the sole site of MF synthesis. PtJHAMT expression significantly increased in the late-vitellogenic stage and mature stage, which suggests a possible role of PtJHAMT in modulating ovarian development. The role of PtJHAMT and PtFAMeT in MF biosynthesis was further investigated by RNA interfering (RNAi). Injection of PtJHAMT and PtFAMeT dsRNA both led to a decrease in hemolymph MF titers. Injection of PtHMGR dsRNA caused the decrease in PtJHAMT expression, but had no effect on mRNA level of PtFAMeT. Together these results suggested that JHAMT and FAMeT are both involved in the MF biosynthesis in crustaceans, while the JHAMT is highly specific to FA substrate, and FAMeT may have more catalytic functions.

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

“…Following Schenk et al (2016) and given our results (including those for methoprene tolerant receptor, above), a similar pathway seems to occur in annelids, with the synthesis of some form of sesquiterpenoid regulating reproduction, as occurs in arthropods (Xie et al 2016).…”

“…Comparably to JH in insects, MF regulates many aspects of crustacean physiology, including reproduction (Xie et al 2016). In this context, MF is more actively synthetized by females during vitellogenesis, and higher levels of MF are associated with large reproductive systems and aggressive mating behavior in males of the spider crab Libinia emarginata (Laufer et al 1992).…”

“…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). Other hormones have also been proposed to play essential roles in annelids reproduction, such as the prostomium (i.e.…”

Complementary roles of photoperiod and temperature in environmental sex determination in Daphnia spp

“…In daphnids, methyl farnesoate is responsible for programming developing oocytes into male offspring (LeBlanc and Medlock, 2015; Olmstead and LeBlanc, 2002;Toyota et al, 2015a). Methyl farnesoate is a sesquiterpenoid hormone produced by the enzymes farnesoic acid O-methyltransferase (FAMT) and juvenile hormone acid O-methyltransferase (JHAMT) (Xie et al, 2016). Methyl farnesoate activates the methyl farnesoate receptor (MfR) which is a heterodimer of the proteins methoprene-tolerant (Met) and steroid receptor co-activator (SRC) (Kakaley et al, 2017;LeBlanc et al, 2013;Miyakawa et al, 2013;Toyota et al, 2015a).…”

Relative expression of three key genes involved in the hormonal cycle of the freshwater amphipod, Gammarus pulex

“…This conversion has been observed in several crustaceans such as the shrimps Penaeus monodon , Fenneropenaeus merguiensis and Metapenaeus ensis (Hui, Tobe, & Chan, ; Kuballa et al, ) and the lobster Homarus americanus (Holford et al, ). Besides, although MF synthesis has been shown to be catalyzed by the juvenile hormone acid methyltransferase enzyme (JHAMT) in the crab Portunus trituberculatus (Xie et al, ), to our knowledge, no putative JHAMT has been sequenced in gammarid species, such as G. pulex (Gismondi & Thomé, ) or G. fossarum (Trapp, ). Finally, MO is also controlled by the MO inhibiting hormone, which can suppress the MF production by inhibiting FAMeT enzyme (Wainwright, Webster, & Rees, ).…”