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Biochemical characterization of allene oxide synthases from the liverwort Marchantia polymorpha and green microalgae Klebsormidium flaccidum provides insight into the evolutionary divergence of the plant CYP74 family

Planta volume 242, pages 1175–1186 (2015)Cite this article

Abstract

Main conclusion

Allene oxide synthases (AOSs) were isolated from liverworts and charophytes. These AOSs exhibited enzymatic properties similar to those of angiosperms but formed a distinct phylogenetic clade.

Allene oxide synthase (AOS) and hydroperoxide lyase (HPL) mediate the formation of precursors of jasmonates and carbon-six volatiles, respectively. AOS and HPL utilize fatty acid hydroperoxides and belong to the plant cytochrome P450 74 (CYP74) family that mediates plant defense against herbivores, pathogens, or abiotic stresses. Although members of the CYP74 family have been reported in mosses and other species, the evolution and function of multiple CYP74 genes in plants remain elusive. Here, we show that the liverwort Marchantia polymorpha belongs to a basal group in the evolution of land plants; has two closely related proteins (59 % identity), MpAOS1 and MpAOS2, that are similar to moss PpAOS1 (49 and 47 % identity, respectively); and exhibits AOS activity but not HPL activity. We also found that the green microalgae Klebsormidium flaccidum, consist of multicellular and non-branching filaments, contains an enzyme, KfAOS, that is similar to PpAOS1 (37 % identity), and converts 13-hydroperoxide of linolenic acid to 12-oxo-phytodienoic acid in a coupled reaction with allene oxide cyclase. Phylogenetic analysis showed two evolutionarily distinct clusters. One cluster comprised AOS and HPL from charophytic algae, liverworts, and mosses, including MpAOSs and KfAOS. The other cluster was formed by angiosperm CYP74. Our results suggest that plant CYP74 enzymes with AOS, HPL, and divinyl ether synthase activities have arisen multiple times and in the two different clades, which occurred prior to the divergence of the flowering plant lineage.

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Abbreviations

AOS:

Allene oxide synthase

HPL:

Hydroperoxide lyase

DES:

Divinyl ether synthase

OPDA:

12-Oxo-phytodienoic acid

9-HPOD:

9-Hydroperoxy-(E,Z)-10,12-octadecadienoic acid

9-HPOT:

9-Hydroperoxy-(E,Z,Z)-10,12,15-octadecatrienoic acid

13-HPOD:

13-Hydroperoxy-(E,Z)-9,11-octadecadienoic acid

13-HPOT:

13-Hydroperoxy-(E,Z,Z)-9,11,15-octadecatrienoic acid

12-HPETE:

12-Hydroperoxy-(Z,Z,E,Z)-5,8,10,14-eicosatetraenoic acid

15-HPETE:

15-Hydroperoxy-(Z,Z,Z,E)-5,8,11,13-eicosatetraenoic acid

15-HPEPE:

15-Hydroperoxy-(Z,Z,Z,E,Z)-5,8,11,13,17-eicosapentaenoic acid

HPO:

Hydroperoxide

CYP74:

Cytochrome P450 family 74

JA:

Jasmonic acid

JA-Ile:

Jasmonic acid-isoleucine

EST:

Expressed sequence tag

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Acknowledgments

We wish to thank Dr. Mitsuo Jisaka and Dr. Kazushige Yokota (Shimane University) for providing the GmAOS construct and human platelet 12-lipoxygenase used in this study. We also thank Maya Tanaka (Yamaguchi University) for preparation of 12-HPETE. This work was supported by JSPS KAKENHI Grant Number 24580162.

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Authors and Affiliations

  1. Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, 753-8515, Japan

    Takao Koeduka & Kenji Matsui

  2. Graduate School of Science, Kobe University, Kobe, 657-8501, Japan

    Kimitsune Ishizaki

  3. Applied Molecular Bioscience, Graduate School of Medicine, Yamaguchi University, Yamaguchi, 753-8515, Japan

    Cynthia Mugo Mwenda & Kenji Matsui

  4. Center for Biological Resources and Informatics, Tokyo Institute of Technology, Kanagawa, 226-8501, Japan

    Koichi Hori & Hiroyuki Ohta

  5. Earth-Life Science Institute, Tokyo Institute of Technology, Tokyo, 152-8551, Japan

    Yuko Sasaki-Sekimoto & Hiroyuki Ohta

  6. Graduate School of Biostudies, Kyoto University, Kyoto, 606-8502, Japan

    Takayuki Kohchi

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  1. Takao Koeduka
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  2. Kimitsune Ishizaki
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Correspondence to Takao Koeduka or Kenji Matsui.

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Koeduka, T., Ishizaki, K., Mwenda, C.M. et al. Biochemical characterization of allene oxide synthases from the liverwort Marchantia polymorpha and green microalgae Klebsormidium flaccidum provides insight into the evolutionary divergence of the plant CYP74 family. Planta 242, 1175–1186 (2015). https://doi.org/10.1007/s00425-015-2355-8

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  • DOI: https://doi.org/10.1007/s00425-015-2355-8

Keywords

  • Allene oxide synthase
  • Plant evolution
  • CYP74
  • Hydroperoxide lyase
  • C8 volatiles