Coumarin biosynthesis genes are required after foliar pathogen infection for the creation of a microbial soil-borne legacy that primes plants for SA-dependent defenses

Gilles Vismans, Sietske van Bentum, Jelle Spooren, Yang Song, Pim Goossens, Josep Valls, Basten L Snoek, Benjamin Thiombiano, Mario Schilder, Lemeng Dong, Harro J Bouwmeester, Pierre Pétriacq, Corné M J Pieterse, Peter A H M Bakker, Roeland L Berendsen*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Plants deposit photosynthetically-fixed carbon in the rhizosphere, the thin soil layer directly around the root, thereby creating a hospitable environment for microbes. To manage the inhabitants of this nutrient-rich environment, plant roots exude and dynamically adjust microbe-attracting and -repelling compounds to stimulate specific members of the microbiome. Previously, we demonstrated that foliar infection of Arabidopsis thaliana by the biotrophic downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa) leads to a disease-induced modification of the rhizosphere microbiome. Soil conditioned with Hpa-infected plants provided enhanced protection against foliar downy mildew infection in a subsequent population of plants, a phenomenon dubbed the soil-borne legacy (SBL). Here, we show that for the creation of the SBL, plant-produced coumarins play a prominent role as coumarin-deficient myb72 and f6'h1 mutants were defective in creating a Hpa-induced SBL. Root exudation profiles changed significantly in Col-0 upon foliar Hpa infection, and this was accompanied by a compositional shift in the root microbiome that was significantly different from microbial shifts occurring on roots of Hpa-infected coumarin-deficient mutants. Our data further show that the Hpa-induced SBL primes Col-0 plants growing in SBL-conditioned soil for salicylic acid (SA)-dependent defenses. The SA-signaling mutants sid2 and npr1 were unresponsive to the Hpa-induced SBL, suggesting that the protective effect of the Hpa-induced shift in the root microbiome results from an induced systemic resistance that requires SA-signaling in the plant.

Original languageEnglish
Article number22473
Number of pages12
JournalScientific Reports
Volume12
Issue number1
DOIs
Publication statusPublished - 28 Dec 2022

Keywords

  • Arabidopsis Proteins/genetics
  • Salicylic Acid/pharmacology
  • Arabidopsis/metabolism
  • Oomycetes
  • Peronospora
  • Coumarins/pharmacology
  • Plant Diseases/genetics
  • Gene Expression Regulation, Plant

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