Metabolome Analysis Identified Okaramines in the Soybean Rhizosphere as a Legacy of Hairy Vetch

Nozomu Sakurai; Hossein Mardani-Korrani; Masaru Nakayasu; Kazuhiko Matsuda; Kumiko Ochiai; Masaru Kobayashi; Yusuke Tahara; Takeshi Onodera; Yuichi Aoki; Takashi Motobayashi; Masakazu Komatsuzaki; Makoto Ihara; Daisuke Shibata; Yoshiharu Fujii; Akifumi Sugiyama

doi:10.3389/fgene.2020.00114

Metabolome Analysis Identified Okaramines in the Soybean Rhizosphere as a Legacy of Hairy Vetch

Front Genet. 2020 Feb 24:11:114. doi: 10.3389/fgene.2020.00114. eCollection 2020.

Authors

Nozomu Sakurai^{1

2}, Hossein Mardani-Korrani³, Masaru Nakayasu⁴, Kazuhiko Matsuda⁵, Kumiko Ochiai⁶, Masaru Kobayashi⁶, Yusuke Tahara⁷, Takeshi Onodera⁸, Yuichi Aoki⁹, Takashi Motobayashi³, Masakazu Komatsuzaki¹⁰, Makoto Ihara⁵, Daisuke Shibata², Yoshiharu Fujii³, Akifumi Sugiyama⁴

Affiliations

¹ Bioinformation and DDBJ Center, National Institute of Genetics, Mishima, Japan.
² Kazusa DNA Research Institute, Kisarazu, Japan.
³ Department of International Environmental and Agricultural Sciences, Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Japan.
⁴ Research Institute for Sustainable Humanosphere, Kyoto University, Gokasho, Japan.
⁵ Department of Applied Biological Chemistry, Faculty of Agriculture, Kindai University, Nara, Japan.
⁶ Division of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Kyoto, Japan.
⁷ Research and Development Center for Five-Sense Devices, Kyushu University, Fukuoka, Japan.
⁸ Faculty of Information Science and Electrical Engineering, Kyushu University, Fukuoka, Japan.
⁹ Tohoku Medical Megabank Organization, Tohoku University, Sendai, Japan.
¹⁰ Center for Field Agriculture Research & Education, Ibaraki University, Ami, Japan.

Abstract

Inter-organismal communications below ground, such as plant-microbe interactions in the rhizosphere, affect plant growth. Metabolites are shown to play important roles in biological communication, but there still remain a large number of metabolites in soil to be uncovered. Metabolomics, a technique for the comprehensive analysis of metabolites in samples, may uncover the molecules that intermediate these interactions. We conducted a multivariate analysis using liquid chromatography (LC)-mass spectrometry (MS)-based untargeted metabolomics in several soil samples and also targeted metabolome analysis for the identification of the candidate compounds in soil. We identified okaramine A, B, and C in the rhizosphere soil of hairy vetch. Okaramines are indole alkaloids first identified in soybean pulp (okara) inoculated with Penicillium simplicissimum AK-40 and are insecticidal. Okaramine B was detected in the rhizosphere from an open field growing hairy vetch. Okaramine B was also detected in both bulk and rhizosphere soils of soybean grown following hairy vetch, but not detected in soils of soybean without hairy vetch growth. These results suggested that okaramines might be involved in indirect defense of plants against insects. To our knowledge, this is the first report of okaramines in the natural environment. Untargeted and targeted metabolomics would be useful to uncover the chemistry of the rhizosphere.

Keywords: hairy vetch; okaramine; rhizosphere; soybean; untargeted metabolomics.