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Reprogramming of fatty acid and oxylipin synthesis in rhizobacteria-induced systemic resistance in tomato

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Abstract

The rhizobacterium Pseudomonas putida BTP1 stimulates induced systemic resistance (ISR) in tomato. A previous work showed that the resistance is associated in leaves with the induction of the first enzyme of the oxylipin pathway, the lipoxygenase (LOX), leading to a faster accumulation of its product, the free 13-hydroperoxy octadecatrienoic acid (13-HPOT), 2 days after Botrytis cinerea inoculation. In the present study, we further investigated the stimulation of the oxylipin pathway: metabolites and enzymes of the pathway were analyzed to understand the fate of the 13-HPOT in ISR. Actually the stimulation began upstream the LOX: free linolenic acid accumulated faster in P. putida BTP1-treated plants than in control. Downstream, the LOX products 13-fatty acid hydroperoxides esterified to galactolipids and phospholipids were more abundant in bacterized plants than in control before infection. These metabolites could constitute a pool that will be used after pathogen attack to produce free fungitoxic metabolites through the action of phospholipase A2, which is enhanced in bacterized plants upon infection. Enzymatic branches which can use as substrate the fatty acid hydroperoxides were differentially regulated in bacterized plants in comparison to control plants, so as to lead to the accumulation of the most fungitoxic compounds against B. cinerea. Our study, which is the first to demonstrate the accumulation of an esterified defense metabolite during rhizobacteria-mediated induced systemic resistance, showed that the oxylipin pathway is differentially regulated. It suggests that this allows the plant to prepare to a future infection, and to respond faster and in a more effective way to B. cinerea invasion.

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Abbreviations

AOS:

Allene oxide synthase

DES:

Divinyl ether synthase

ISR:

Induced systemic resistance

HL:

Hydroperoxide lyase

HPO:

Fatty acid hydroperoxide

LOX:

Lipoxygenase

PGPR:

Plant growth-promoting rhizobacteria

PLA1:

Phospholipase A1

PLA2:

Phospholipase A2

PUFA:

Poly-unsaturated fatty acid

SAR:

Systemic acquired resistance

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Acknowledgments

This work received financial support from the F.R.F.C. Projects no 2.4.624.06 and 2.4.563.08 of the Belgian National Fund for Scientific Research (FRS-F.N.R.S.). M. Mariutto is a FRS-F.N.R.S research fellow. M. Ongena is research associate at the FRS-F.N.R.S. We thank Adeline Blondiaux, Plant Biology Unit, Gembloux Agro-Bio Tech, University of Liège, for technical assistance in oxylipin profiling.

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Authors and Affiliations

  1. Laboratory of Plant Molecular Biology and Biotechnology, Department of Life Sciences, Faculty of Sciences, University of Liège, Boulevard du Rectorat, 27, Liege, Belgium

    Martin Mariutto & Jacques Dommes

  2. Plant Biology Unit, Gembloux Agro-Bio Tech, University of Liège, Passage des Déportés, 2, Gembloux, Belgium

    Marie-Laure Fauconnier & Patrick du Jardin

  3. Walloon Center of Industrial Biology, Gembloux Agro-Bio Tech, University of Liège, Passage des Déportés, 2, Gembloux, Belgium

    Marc Ongena & Philippe Thonart

  4. Laboratory of General and Organic Chemistry, Gembloux Agro-Bio Tech, University of Liège, Passage des Déportés 2, Gembloux, Belgium

    Morgan Laloux & Jean-Paul Wathelet

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  1. Martin Mariutto
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  2. Marie-Laure Fauconnier
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  8. Jacques Dommes
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Correspondence to Jacques Dommes.

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Martin Mariutto is the first author.

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11103_2013_144_MOESM1_ESM.jpg

Supplementary material 1 Time course accumulation of the LOX substrates in control (white) and treated (black) plants. Esterified linoleic (A) and esterified linolenic (B) acids were quantified before (0), one, two and four days after infection by gas-chromatography. The data presented was from a representative experiment that was independently repeated once with similar results. Stars (*) indicate statistically significant differences between control and treated plants (Student’s t test, α = 0,05)

11103_2013_144_MOESM2_ESM.jpg

Supplementary material 2 Analysis of the enantiomery of the oxylipins. Comparison of enantiomery between control (C) and P. putida BTP1-treated (T) plants. Oxylipins were extracted from leaves of control (white) and P. putida BTP1-treated (black) collected before (0), one (1), two (2), and four days (4) after pathogen inoculation and analyzed by chiral HPLC

11103_2013_144_MOESM3_ESM.jpg

Supplementary material 3 Analysis of the HL branch of the oxylipin pathway. Samples were collected before (0), one (1), two (2), and four days (4) after pathogen inoculation. A. Comparison of expression levels of HL gene in control (open diamonds, dashed line) and P. putida BTP1-treated (closed squares, continuous line) plants. Total RNA was extracted from leaves and subjected to real-time RT-PCR. Hexanal (B), cis-3 hexenol (C), trans-2-hexenal (D) and 1-hexanol (E) were extracted by SPME and quantified by GC-FID in leaves of control (white) and P. putida BTP1-treated (black) tomatoes

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Mariutto, M., Fauconnier, ML., Ongena, M. et al. Reprogramming of fatty acid and oxylipin synthesis in rhizobacteria-induced systemic resistance in tomato. Plant Mol Biol 84, 455–467 (2014). https://doi.org/10.1007/s11103-013-0144-y

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