Methyl farnesoate synthesis is necessary for the environmental sex determination in the water flea Daphnia pulex

Kenji Toyota, Hitoshi Miyakawa, Chizue Hiruta, Kenjiro Furuta, Yukiko Ogino, Tetsuro Shinoda, Norihisa Tatarazako, Shinichi Miyagawa, Joseph R. Shaw, Taisen Iguchi

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

Sex-determination systems can be divided into two groups: genotypic sex determination (GSD) and environmental sex determination (ESD). ESD is an adaptive life-history strategy that allows control of sex in response to environmental cues in order to optimize fitness. However, the molecular basis of ESD remains largely unknown. The micro crustacean Daphnia pulex exhibits ESD in response to various external stimuli. Although methyl farnesoate (MF: putative juvenile hormone, JH, in daphnids) has been reported to induce male production in daphnids, the role of MF as a sex-determining factor remains elusive due to the lack of a suitable model system for its study. Here, we establish such a system for ESD studies in D. pulex. The WTN6 strain switches from producing females to producing males in response to the shortened day condition, while the MFP strain only produces females, irrespective of day-length. To clarify whether MF has a novel physiological role as a sex-determining factor in D. pulex, we demonstrate that a MF/JH biosynthesis inhibitor suppressed male production in WTN6 strain reared under the male-inducible condition, shortened day-length. Moreover, we show that juvenile hormone acid O-methyltransferase (JHAMT), a critical enzyme of MF/JH biosynthesis, displays MF-generating activity by catalyzing farnesoic acid. Expression of the JHAMT gene increased significantly just before the MF-sensitive period for male production in the WTN6 strain, but not in the MFP strain, when maintained under male-inducible conditions. These results suggest that MF synthesis regulated by JHAMT is necessary for male offspring production in D. pulex. Our findings provide novel insights into the genetic underpinnings of ESD and they begin to shed light on the physiological function of MF as a male-fate determiner in D. pulex.

Original languageEnglish
Pages (from-to)22-30
Number of pages9
JournalJournal of insect physiology
Volume80
DOIs
Publication statusPublished - Aug 11 2015

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Cladocera
Daphnia
Daphnia pulex
synthesis
gender
Juvenile Hormones
juvenile hormones
Methyltransferases
methyltransferases
Sex Factors
acids
Acids
methyl farnesoate
photoperiod
biosynthesis
Cues

All Science Journal Classification (ASJC) codes

  • Physiology
  • Insect Science

Cite this

Methyl farnesoate synthesis is necessary for the environmental sex determination in the water flea Daphnia pulex. / Toyota, Kenji; Miyakawa, Hitoshi; Hiruta, Chizue; Furuta, Kenjiro; Ogino, Yukiko; Shinoda, Tetsuro; Tatarazako, Norihisa; Miyagawa, Shinichi; Shaw, Joseph R.; Iguchi, Taisen.

In: Journal of insect physiology, Vol. 80, 11.08.2015, p. 22-30.

Research output: Contribution to journalArticle

Toyota, K, Miyakawa, H, Hiruta, C, Furuta, K, Ogino, Y, Shinoda, T, Tatarazako, N, Miyagawa, S, Shaw, JR & Iguchi, T 2015, 'Methyl farnesoate synthesis is necessary for the environmental sex determination in the water flea Daphnia pulex', Journal of insect physiology, vol. 80, pp. 22-30. https://doi.org/10.1016/j.jinsphys.2015.02.002
Toyota, Kenji ; Miyakawa, Hitoshi ; Hiruta, Chizue ; Furuta, Kenjiro ; Ogino, Yukiko ; Shinoda, Tetsuro ; Tatarazako, Norihisa ; Miyagawa, Shinichi ; Shaw, Joseph R. ; Iguchi, Taisen. / Methyl farnesoate synthesis is necessary for the environmental sex determination in the water flea Daphnia pulex. In: Journal of insect physiology. 2015 ; Vol. 80. pp. 22-30.
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abstract = "Sex-determination systems can be divided into two groups: genotypic sex determination (GSD) and environmental sex determination (ESD). ESD is an adaptive life-history strategy that allows control of sex in response to environmental cues in order to optimize fitness. However, the molecular basis of ESD remains largely unknown. The micro crustacean Daphnia pulex exhibits ESD in response to various external stimuli. Although methyl farnesoate (MF: putative juvenile hormone, JH, in daphnids) has been reported to induce male production in daphnids, the role of MF as a sex-determining factor remains elusive due to the lack of a suitable model system for its study. Here, we establish such a system for ESD studies in D. pulex. The WTN6 strain switches from producing females to producing males in response to the shortened day condition, while the MFP strain only produces females, irrespective of day-length. To clarify whether MF has a novel physiological role as a sex-determining factor in D. pulex, we demonstrate that a MF/JH biosynthesis inhibitor suppressed male production in WTN6 strain reared under the male-inducible condition, shortened day-length. Moreover, we show that juvenile hormone acid O-methyltransferase (JHAMT), a critical enzyme of MF/JH biosynthesis, displays MF-generating activity by catalyzing farnesoic acid. Expression of the JHAMT gene increased significantly just before the MF-sensitive period for male production in the WTN6 strain, but not in the MFP strain, when maintained under male-inducible conditions. These results suggest that MF synthesis regulated by JHAMT is necessary for male offspring production in D. pulex. Our findings provide novel insights into the genetic underpinnings of ESD and they begin to shed light on the physiological function of MF as a male-fate determiner in D. pulex.",
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