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Glucosinolate structural diversity shapes recruitment of a metabolic network of leaf-associated bacteria

Author

Listed:
  • Kerstin Unger

    (Friedrich Schiller University Jena)

  • Syed Ali Komail Raza

    (Friedrich Schiller University Jena)

  • Teresa Mayer

    (Friedrich Schiller University Jena
    Technical University of Munich)

  • Michael Reichelt

    (Max-Planck-Institute for Chemical Ecology)

  • Johannes Stuttmann

    (Aix Marseille University)

  • Annika Hielscher

    (Technische Universität Braunschweig)

  • Ute Wittstock

    (Technische Universität Braunschweig)

  • Jonathan Gershenzon

    (Max-Planck-Institute for Chemical Ecology)

  • Matthew T. Agler

    (Friedrich Schiller University Jena)

Abstract

Host defenses can have broader ecological roles, but how they shape natural microbiome recruitment is poorly understood. Aliphatic glucosinolates (GLSs) are secondary defense metabolites in Brassicaceae plant leaves. Their genetically defined structure shapes interactions with pests in Arabidopsis thaliana leaves, and here we find that it also shapes bacterial recruitment. In model genotype Col-0, GLSs (mostly 4-methylsulfinylbutyl-GLS) have no clear effect on natural leaf bacterial recruitment. In a genotype from a wild population, however, GLSs (mostly allyl-GLS) enrich specific taxa, mostly Comamonadaceae and Oxalobacteraceae. Consistently, Comamonadaceae are also enriched in wild A. thaliana, and Oxalobacteraceae are enriched from wild plants on allyl-GLS as carbon source, but not on 4-methylsulfinylbutyl-GLS. Recruitment differences between GLS structures most likely arise from bacterial myrosinase specificity. Community recruitment is then defined by metabolic cross-feeding among bacteria. The link of genetically defined metabolites to recruitment could lead to new strategies to shape plant microbiome balance.

Suggested Citation

  • Kerstin Unger & Syed Ali Komail Raza & Teresa Mayer & Michael Reichelt & Johannes Stuttmann & Annika Hielscher & Ute Wittstock & Jonathan Gershenzon & Matthew T. Agler, 2024. "Glucosinolate structural diversity shapes recruitment of a metabolic network of leaf-associated bacteria," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52679-7
    DOI: 10.1038/s41467-024-52679-7
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    References listed on IDEAS

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    1. Shawn M Higdon & Tania Pozzo & Nguyet Kong & Bihua C Huang & Mai Lee Yang & Richard Jeannotte & C Titus Brown & Alan B Bennett & Bart C Weimer, 2020. "Genomic characterization of a diazotrophic microbiota associated with maize aerial root mucilage," PLOS ONE, Public Library of Science, vol. 15(9), pages 1-26, September.
    2. Tao Chen & Kinya Nomura & Xiaolin Wang & Reza Sohrabi & Jin Xu & Lingya Yao & Bradley C. Paasch & Li Ma & James Kremer & Yuti Cheng & Li Zhang & Nian Wang & Ertao Wang & Xiu-Fang Xin & Sheng Yang He, 2020. "A plant genetic network for preventing dysbiosis in the phyllosphere," Nature, Nature, vol. 580(7805), pages 653-657, April.
    3. Jingyuan Chen & Chhana Ullah & Michael Reichelt & Franziska Beran & Zhi-Ling Yang & Jonathan Gershenzon & Almuth Hammerbacher & Daniel G. Vassão, 2020. "The phytopathogenic fungus Sclerotinia sclerotiorum detoxifies plant glucosinolate hydrolysis products via an isothiocyanate hydrolase," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
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