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The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum

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Abstract

Plant root development is highly responsive both to changes in nitrate availability and beneficial microorganisms in the rhizosphere. We previously showed that Phyllobacterium brassicacearum STM196, a plant growth-promoting rhizobacteria strain isolated from rapeseed roots, alleviates the inhibition exerted by high nitrate supply on lateral root growth. Since soil-borne bacteria can produce IAA and since this plant hormone may be implicated in the high nitrate-dependent control of lateral root development, we investigated its role in the root development response of Arabidopsis thaliana to STM196. Inoculation with STM196 resulted in a 50% increase of lateral root growth in Arabidopsis wild-type seedlings. This effect was completely abolished in aux1 and axr1 mutants, altered in IAA transport and signaling, respectively, indicating that these pathways are required. The STM196 strain, however, appeared to be a very low IAA producer when compared with the high-IAA-producing Azospirillum brasilense sp245 strain and its low-IAA-producing ipdc mutant. Consistent with the hypothesis that STM196 does not release significant amounts of IAA to the host roots, inoculation with this strain failed to increase root IAA content. Inoculation with STM196 led to increased expression levels of several IAA biosynthesis genes in shoots, increased Trp concentration in shoots, and increased auxin-dependent GUS staining in the root apices of DR5::GUS transgenic plants. All together, our results suggest that STM196 inoculation triggers changes in IAA distribution and homeostasis independently from IAA release by the bacteria.

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Abbreviations

AAO1:

Arabidopsis aldehyde oxidase 1

AIR:

Auxin-induced in root cultures

ASA1:

Anthranilate synthase alpha subunit 1

ASB1:

Anthranilate synthase beta subunit 1

AXR:

Auxin resistant

AUX1:

Auxin resistant 1

AUX/IAA:

Auxin/indole acetic acid

CYP:

Cytochrome P450

DFL1:

Dwarf in light 1

GUS:

β-Glucuronidase

IAA:

Indole-3-acetic acid

IAAsp:

Indole-3-acetylaspartate

IAGlu:

Indole-3-acetylglutamate

PAS1:

Pasticcino 1

PGPR:

Plant growth-promoting rhizobacteria

PIN1:

Pin-formed 1

PXA1:

Peroxisomal ABC transporter 1

SCF:

Skp1/cullin/F-box ubiquitin ligase

SUR:

Superroot

TIR1:

Transport inhibitor response 1

YUCCA:

Flavin monooxygenase gene family

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Acknowledgments

This work was supported by a grant from the Centre Technique Interprofessionnel des Oléagineux Métropolitains (CETIOM) and the Région Languedoc-Roussillon to C. Contesto, as well as grants from the Swedish Foundation of Strategic Research (SSF) and the Swedish Research Council (VR) to C. Bellini. We acknowledge Dr. P. Lemanceau and G. Vansuyt (Microbiologie du Sol et de l’Environnement, INRA-Université de Bourgogne, Dijon, France) for fruitful discussions, and Dr. T. J. Tranbarger (Palm Developmental Biology Laboratory, IRD-Université Montpellier 2, Montpellier, France) for carefully reading and editing the manuscript.

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Author notes

  1. Sandrine Milesi

    Present address: Eurasanté, 310 rue Eugène Avinée, 59120, Loos, France

  2. Sophie Mantelin

    Present address: SCRI, Invergowrie, Dundee, DD2 5DA, Scotland, UK

  3. Anouk Zancarini

    Present address: Unité Mixte de Recherches en Génétiques et Ecophysiologie des Légumineuses à Graines, INRA, ENESAD, 21110, Bretenières, France

Authors and Affiliations

  1. Laboratoire des Symbioses Tropicales et Méditerranéennes, Université Montpellier 2, IRD, CIRAD, SupAgro, INRA, CC 002, Place Eugène Bataillon, 34095, Montpellier Cedex 05, France

    Céline Contesto, Sandrine Milesi, Sophie Mantelin, Anouk Zancarini, Guilhem Desbrosses, Fabrice Varoquaux & Bruno Touraine

  2. Department of Forest Genetics and Plant Physiology, Umeå Plant Science Center, Swedish University of Agricultural Sciences, 90183, Umeå, Sweden

    Catherine Bellini & Mariusz Kowalczyk

  3. Laboratoire de Biologie Cellulaire, Institut National de la Recherche Agronomique, 78026, Versailles Cedex, France

    Catherine Bellini

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  1. Céline Contesto
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Correspondence to Bruno Touraine.

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Supplemental Fig. S1

. Effects of the Phyllobacterium brassicacearum STM196, Azospirillum brasilense Sp245 wild type and A. brasilense ipdC mutant strains on the root system architecture of Arabidopsis Col-0 wild-type plants. Seedlings were grown in vertically oriented Petri dishes, on mineral medium, for 6 days in axenic conditions (root tip position reached at that time indicated by a black mark) and for 6 further days on a fresh axenic medium (a), or a P. brassicacearum STM196-inoculated medium (b), or a A. brasilense Sp245-inoculated medium (c) or a A. brasilense ipdC mutant-inoculated medium (d). The images are scans obtained after a typical experiment. They clearly show the typical high auxin supply effect of the A. brasilense Sp245 strain on the root system architecture (short primary root, high lateral root density), and the typical effect of P. brassicacearum STM196 i.e. enhancement of lateral root elongation rather than proliferation (PDF 65.4 kb)

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Contesto, C., Milesi, S., Mantelin, S. et al. The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum . Planta 232, 1455–1470 (2010). https://doi.org/10.1007/s00425-010-1264-0

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