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Ethylene induced plant stress tolerance by Enterobacter sp. SA187 is mediated by 2-keto-4-methylthiobutyric acid production

Authors :
Kiruthiga Mariappan
Axel de Zélicourt
Dominique Van Der Straeten
Thomas Depaepe
Moussa Benhamed
Heribert Hirt
Eleonora Rolli
Rewaa S. Jalal
Florence Guérard
Maged M. Saad
Ihsanullah Daur
Yakun Xie
Hanin S. Alzubaidy
Jean Colcombet
Lukas Synek
Cristina Andrés-Barrao
Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403))
Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-Université Paris Diderot - Paris 7 (UPD7)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS)
Université Sorbonne Paris Cité (COMUE) (USPC)
Division of Biological and Environmental Sciences and Engineering
King Abdullah University of Science and Technology (KAUST)
King Abdulaziz University
Universiteit Gent = Ghent University (UGENT)
King Abdullah University of Science and Technology (KAUST) BAS/1/1062-01-01
Agreenskills fellowship programme from the EU's Seventh Framework Programme FP7-609398.
Universiteit Gent = Ghent University [Belgium] (UGENT)
De Julien De Zelicourt, Axel
Synek, Lukas
Saad, Maged
Hirt, Heribert
Source :
PLoS Genetics, PLoS Genetics, 2018, 14 (3), pp.e1007273. ⟨10.1371/journal.pgen.1007273⟩, PLoS Genetics, Vol 14, Iss 3, p e1007273 (2018), PLoS Genetics, Public Library of Science, 2018, 14 (3), pp.e1007273. ⟨10.1371/journal.pgen.1007273⟩, Plos Genetics 3 (14), e1007273. (2018), PLOS GENETICS
Publication Year :
2018
Publisher :
HAL CCSD, 2018.

Abstract

Several plant species require microbial associations for survival under different biotic and abiotic stresses. In this study, we show that Enterobacter sp. SA187, a desert plant endophytic bacterium, enhances yield of the crop plant alfalfa under field conditions as well as growth of the model plant Arabidopsis thaliana in vitro, revealing a high potential of SA187 as a biological solution for improving crop production. Studying the SA187 interaction with Arabidopsis, we uncovered a number of mechanisms related to the beneficial association of SA187 with plants. SA187 colonizes both the surface and inner tissues of Arabidopsis roots and shoots. SA187 induces salt stress tolerance by production of bacterial 2-keto-4-methylthiobutyric acid (KMBA), known to be converted into ethylene. By transcriptomic, genetic and pharmacological analyses, we show that the ethylene signaling pathway, but not plant ethylene production, is required for KMBA-induced plant salt stress tolerance. These results reveal a novel molecular communication process during the beneficial microbe-induced plant stress tolerance.<br />Author summary Plants as sessile organisms are facing multiple stresses during their lifetime. Among them, abiotic stresses, such as salt stress, can cause severe crop yield reduction, leading to food security issues in many regions of the world. In order to respond to growing food demands, especially in the context of the global climate change and increasing world population, it then becomes urgent to develop new strategies to yield crops more tolerant to abiotic stresses. One way to overcome these challenges is to take advantage of plant beneficial microbes, defined as plant growth promoting bacteria (PGPB). In this study, we report the beneficial effect of Enterobacter sp. SA187 on plant growth under salt stress conditions. SA187 increased the yield of the forage crop alfalfa when submitted to different saline irrigations in field trials. Moreover, using the model plant Arabidopsis thaliana, we demonstrate that SA187 mediates its beneficial activity by producing 2-keto-4-methylthiobutyric acid (KMBA), which modulates the plant ethylene signaling pathway. This study highlights a novel mechanism involved in plant-PGPB interaction, and proves that endophytic bacteria can be efficiently used to enhance yield of current crops under salt stress conditions.

Subjects

Subjects :
0106 biological sciences
0301 basic medicine
Salinity
Cancer Research
Ethylene
[SDV]Life Sciences [q-bio]
Arabidopsis
PROTEIN
Fractional Precipitation
Plant Science
Plant Roots
Biochemistry
Physical Chemistry
01 natural sciences
chemistry.chemical_compound
Methionine
Gene Expression Regulation, Plant
SALINITY
Plant Resistance to Abiotic Stress
Arabidopsis thaliana
Plant Hormones
Genetics (clinical)
GROWTH-PROMOTING RHIZOBACTERIA
2. Zero hunger
Abiotic component
Ecology
biology
SALT-TOLERANCE
Organic Compounds
Plant Biochemistry
Salting Out
Plant Anatomy
Eukaryota
food and beverages
Agriculture
Plants
Adaptation, Physiological
Precipitation Techniques
Chemistry
INDUCED SYSTEMIC RESISTANCE
Experimental Organism Systems
Plant Physiology
BACTERIA
Physical Sciences
Shoot
Plant Shoots
Root Hairs
Research Article
ROOT MORPHOGENESIS
EXPRESSION
lcsh:QH426-470
Arabidopsis Thaliana
Enterobacter
Crops
Brassica
Root hair
Research and Analysis Methods
03 medical and health sciences
Model Organisms
Biosynthesis
Stress, Physiological
Plant and Algal Models
Plant-Environment Interactions
Botany
Genetics
[SDV.BV]Life Sciences [q-bio]/Vegetal Biology
BIOSYNTHESIS
Plant Defenses
Molecular Biology
Ecology, Evolution, Behavior and Systematics
Plant Ecology
Ecology and Environmental Sciences
Organic Chemistry
fungi
Organisms
Chemical Compounds
Biology and Life Sciences
Ethylenes
Plant Pathology
15. Life on land
biology.organism_classification
Hormones
lcsh:Genetics
030104 developmental biology
Chemical Properties
chemistry
Seedlings
13. Climate action
ARABIDOPSIS-THALIANA
Potassium
Bacteria
Crop Science
010606 plant biology & botany

Details

Language :
English
ISSN :
15537390 and 15537404
Database :
OpenAIRE
Journal :
PLoS Genetics, PLoS Genetics, 2018, 14 (3), pp.e1007273. ⟨10.1371/journal.pgen.1007273⟩, PLoS Genetics, Vol 14, Iss 3, p e1007273 (2018), PLoS Genetics, Public Library of Science, 2018, 14 (3), pp.e1007273. ⟨10.1371/journal.pgen.1007273⟩, Plos Genetics 3 (14), e1007273. (2018), PLOS GENETICS
Accession number :
edsair.doi.dedup.....328c30bba8aac3b139e188d96c738a29
Full Text :
https://doi.org/10.1371/journal.pgen.1007273⟩