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Mechanisms of xylanase-induced nitric oxide and phosphatidic acid production in tomato cells

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Abstract

The second messenger nitric oxide (NO), phosphatidic acid (PA) and reactive oxygen species (ROS) are involved in the plant defense response during plant–pathogen interactions. NO has been shown to participate in PA production in response to the pathogen-associated molecular pattern xylanase in tomato cell suspensions. Defense responses downstream of PA include ROS production. The goal of this work was to study the signaling mechanisms involved in PA production during the defense responses triggered by xylanase and mediated by NO in the suspension-cultured tomato cells. We analyzed the participation of protein kinases, guanylate cyclase and the NO-mediated posttranslational modification S-nitrosylation, by means of pharmacology and biochemistry. We showed that NO, PA and ROS levels are significantly diminished by treatment with the general protein kinase inhibitor staurosporine. This indicates that xylanase-induced protein phosphorylation events might be the important components leading to NO formation, and hence for the downstream regulation of PA and ROS levels. When assayed, a guanylate cyclase inhibitor or a cGMP analog did not alter the PA accumulation. These results suggest that a cGMP-mediated pathway is not involved in xylanase-induced PA formation. Finally, the inhibition of protein S-nitrosylation did not affect NO formation but compromised PA and ROS production. Data collectively indicate that upon xylanase perception, cells activate a protein kinase pathway required for NO formation and that, S-nitrosylation-dependent mechanisms are involved in downstream signaling leading to PA and ROS.

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Abbreviations

8-Br-cGMP:

8-Bromoguanosine 3′,5′-cyclic monophosphate sodium salt monohydrate

AU:

Arbitrary unit

CDPK:

Ca2+-dependent protein kinase

CFM:

Cell free medium

DAF-FM-DA:

3-Amino,4-aminomethyl-2′,7′-difluorescein diacetate

H2DCF-DA:

2′,7′,-Dichlorofluorescein diacetate

LY83583:

6-Anilino-5,8-quinolinequinone

MAPK:

Mitogen-activated protein kinase

NEM:

N-Ethylmaleimide

NO:

Nitric oxide

PA:

Phosphatidic acid

PAMP:

Pathogen-associated molecular pattern

PD098059:

2-(2-Amino-3-methoxyphenyl)-4H-1-benzopyran-4-one

PLC:

Phospholipase C

PLD:

Phospholipase D

ROS:

Reactive oxygen species

SB202190:

4-(4-Fluorophenyl)-2-(4-hydroxyphenyl)-5-(4-pyridyl)-1H-imidazole

SPL:

Structural phospholipids

TFP:

Trifluoperazine dihydrochloride

TLC:

Thin layer chromatography

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Acknowledgments

This work was supported by Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), Universidad Nacional de Mar del Plata (UNMdP) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). The authors wish to thank our colleagues from Molecular and Integrative Physiology Laboratory (IIB-CONICET-UNMdP) for constructive comments and suggestions.

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  1. Instituto de Investigaciones Biológicas (IIB-CONICET-UNMdP), Universidad Nacional de Mar del Plata, CC 1245, 7600, Mar del Plata, Argentina

    M. Luciana Lanteri, Lorenzo Lamattina & Ana M. Laxalt

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  1. M. Luciana Lanteri
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  2. Lorenzo Lamattina
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  3. Ana M. Laxalt
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Correspondence to Ana M. Laxalt.

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Lanteri, M.L., Lamattina, L. & Laxalt, A.M. Mechanisms of xylanase-induced nitric oxide and phosphatidic acid production in tomato cells. Planta 234, 845–855 (2011). https://doi.org/10.1007/s00425-011-1446-4

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