The N -acyl homoserine-lactone depleted Rhizobium radiobacter mutant RrF4NM13 shows reduced growth-promoting and resista

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ORIGINAL ARTICLE

The N‑acyl homoserine‑lactone depleted Rhizobium radiobacter mutant RrF4NM13 shows reduced growth‑promoting and resistance‑inducing activities in mono‑ and dicotyledonous plants Ibrahim Alabid1,2 · Martin Hardt4 · Jafargholi Imani1   · Anton Hartmann5,8 · Michael Rothballer6 · Dan Li5 · Jenny Uhl7 · Philippe Schmitt‑Kopplin7   · Stefanie Glaeser3 · Karl‑Heinz Kogel1  Received: 7 April 2020 / Accepted: 15 July 2020 © The Author(s) 2020

Abstract The Alphaproteobacterium Rhizobium radiobacter (syn. Agrobacterium tumefaciens, “A. fa brum”) can live in close association with the sebacinoid fungus Serendipita (syn. Piriformospora) indica that forms a mutualistic Sebacinalean symbiosis with a wide range of host plants. The endobacterial strain R. radiobacter F4 (RrF4), which was originally isolated from the fungus, has plant growth promotion and resistance-inducing activities resembling the beneficial activities known from the endobacteria-containing S. indica. The mechanism by which free endobacterial cells influence growth and disease resistance of colonized host plants is not fully understood. Here, we show that RrF4 produces a spectrum of quorum sensing-mediating N-acyl-homoserine lactones (AHLs) with acyl chains of C8, C10, and C12 as well as hydroxyl- or oxo-substitutions at the C3 position. In addition, and in line with previous findings showing that AHLs increase plant biomass and induce systemic resistance, the AHL-depleted lactonase-overexpressing transconjugant RrF4NM13 was partially compromised in promoting growth and inducing resistance against bacterial pathogens in both Arabidopsis thaliana and wheat (Triticum aestivum). Scanning and transmission electron microscopy proved that RrF4NM13, in contrast to RrF4, does not form cellulose-like fiber scaffolds for efficient root surface attachment. Moreover, RrF4NM13 does not penetrate into the intercellular space of the cortical tissue, which in contrast is strongly colonized by RrF4. We discuss the possibility that AHLs contribute to the outcome of the Sebacinalean symbiosis. Keywords  Quorum sensing · Homoserine lactones · Pseudomonas · Rhizobium · Piriformospora

Stefanie Glaeser and Karl-Heinz Kogel: Shared last author. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s4134​8-020-00360​-8) contains supplementary material, which is available to authorized users. * Karl‑Heinz Kogel karl‑[email protected]‑giessen.de 1



Research Centre for BioSystems, Institute of Phytopathology, Justus Liebig University, 35392 Giessen, Germany

2



Department of Plant Protection, Faculty of Agriculture, Tishreen University, PO Box 2233, Lattakia, Syrian Arab Republic

3

Research Centre for BioSystems, Institute of Applied Microbiology, Justus Liebig University, 35392 Giessen, Germany

4

Imaging Unit, Justus Liebig University, 35392 Giessen, Germany





5



Research Unit Microbe‑Plant Interactions, German Research Center for Environmental Health, Helmholtz Zentrum München, 85764 Neuherberg, Germany