Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens

Ken Ichiro Hayashi, Keisuke Horie, Yuji Hiwatashi, Hiroshi Kawaide, Shinjiro Yamaguchi, Atsushi Hanada, Tamotsu Nakashima, Masatoshi Nakajima, Lewis N. Mander, Hisakazu Yamane, Mitsuyasu Hasebe, Hiroshi Nozaki

    Research output: Contribution to journalArticle

    59 Citations (Scopus)

    Abstract

    Gibberellins (GAs) are a group of diterpene-type plant hormones biosynthesized from ent-kaurene via ent-kaurenoic acid. GAs are ubiquitously present in seed plants. The GA signal is perceived and transduced by the GID1 GA receptor/DELLA repressor pathway. The lycopod Selaginella moellendorffii biosynthesizes GA and has functional GID1-DELLA signaling components. In contrast, no GAs or functionally orthologous GID1-DELLA components have been found in the moss Physcomitrella patens. However, P. patens produces ent-kaurene, a common precursor for GAs, and possesses a functional ent-kaurene synthase, PpCPS/KS. To assess the biological role of ent-kaurene in P. patens, we generated a PpCPS/KS disruption mutant that does not accumulate ent-kaurene. Phenotypic analysis demonstrates that the mutant has a defect in the protonemal differentiation of the chloronemata to caulonemata. Gas chromatography-mass spectrometry analysis shows that P. patens produces ent-kaurenoic acid, an ent-kaurene metabolite in the GA biosynthesis pathway. The phenotypic defect of the disruptant was recovered by the application of ent-kaurene or ent-kaurenoic acid, suggesting that ent-kaurenoic acid, or a downstream metabolite, is involved in protonemal differentiation. Treatment with uniconazole, an inhibitor of ent-kaurene oxidase in GA biosynthesis, mimics the protonemal phenotypes of the PpCPS/KS mutant, which were also restored by ent-kaurenoic acid treatment. Interestingly, the GA9 methyl ester, a fern antheridiogen, rescued the protonemal defect of the disruption mutant, while GA3 and GA4, both of which are active GAs in angiosperms, did not. Our results suggest that the moss P. patens utilizes a diterpene metabolite from ent-kaurene as an endogenous developmental regulator and provide insights into the evolution of GA functions in land plants.

    Original languageEnglish
    Pages (from-to)1085-1097
    Number of pages13
    JournalPlant physiology
    Volume153
    Issue number3
    DOIs
    Publication statusPublished - 2010 Jul 1

    ASJC Scopus subject areas

    • Physiology
    • Genetics
    • Plant Science

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  • Cite this

    Hayashi, K. I., Horie, K., Hiwatashi, Y., Kawaide, H., Yamaguchi, S., Hanada, A., Nakashima, T., Nakajima, M., Mander, L. N., Yamane, H., Hasebe, M., & Nozaki, H. (2010). Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant physiology, 153(3), 1085-1097. https://doi.org/10.1104/pp.110.157909