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The sesquiterpene botrydial from Botrytis cinerea induces phosphatidic acid production in tomato cell suspensions

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Abstract

Main conclusion

The phytotoxin botrydial triggers PA production in tomato cell suspensions via PLD and PLC/DGK activation. PLC/DGK-derived PA is partially required for botrydial-induced ROS generation.

Phosphatidic acid (PA) is a phospholipid second messenger involved in the induction of plant defense responses. It is generated via two distinct enzymatic pathways, either via phospholipase D (PLD) or by the sequential action of phospholipase C and diacylglycerol kinase (PLC/DGK). Botrydial is a phytotoxic sesquiterpene generated by the necrotrophic fungus Botrytis cinerea that induces diverse plant defense responses, such as the production of reactive oxygen species (ROS). Here, we analyzed PA and ROS production and their interplay upon botrydial treatments, employing tomato (Solanum lycopersicum) cell suspensions as a model system. Botrydial induces PA production within minutes via PLD and PLC/DGK. Either inhibition of PLC or DGK diminishes ROS generation triggered by botrydial. This indicates that PLC/DGK is upstream of ROS production. In tomato, PLC is encoded by a multigene family constituted by SlPLC1–SlPLC6 and the pseudogene SlPLC7. We have shown that SlPLC2-silenced plants have reduced susceptibility to B. cinerea. In this work, we studied the role of SlPLC2 on botrydial-induced PA production by silencing the expression of SlPLC2 via a specific artificial microRNA. Upon botrydial treatments, SlPLC2-silenced-cell suspensions produce PA levels similar to wild-type cells. It can be concluded that PA is a novel component of the plant responses triggered by botrydial.

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Abbreviations

DGK:

Diacylglycerol kinase

DPI:

Diphenyleneiodonium chloride

EtAc:

Ethyl acetate

MAMP:

Microbe-associated molecular patterns

PA:

Phosphatidic acid

PIP:

Phosphatidylinositol 4-phosphosphate

PIP2 :

Phosphatidylinositol 45-bisphosphate

PLC:

Phospholipase C

PLD:

Phopholipase D

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Funding

This work was financially supported by the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), Universidad Nacional de Mar del Plata (UNMdP) and the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). J.M.D’Ambrosio is a postdoctoral researcher of the research career of CONICET. G. Gonorazky, A.M. Laxalt, and L. Lamattina are members of the research career of CONICET.

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Author notes

  1. Juan Martin D’Ambrosio and Gabriela Gonorazky contributed equally.

Authors and Affiliations

  1. Instituto de Investigaciones Biológicas, CONICET, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, CC. 1245, 7600, Mar del Plata, Argentina

    Juan Martin D’Ambrosio, Gabriela Gonorazky, Andrés Arruebarrena Di Palma, Lorenzo Lamattina & Ana Maria Laxalt

  2. Department of Plant Sciences, University of Oxford, Oxford, UK

    Daniela J. Sueldo

  3. Departamento de Química Orgánica, Universidad de Cádiz, Cadiz, Spain

    Javier Moraga & Isidro González Collado

Authors
  1. Juan Martin D’Ambrosio
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  2. Gabriela Gonorazky
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  8. Ana Maria Laxalt
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Correspondence to Ana Maria Laxalt.

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D’Ambrosio, J.M., Gonorazky, G., Sueldo, D.J. et al. The sesquiterpene botrydial from Botrytis cinerea induces phosphatidic acid production in tomato cell suspensions. Planta 247, 1001–1009 (2018). https://doi.org/10.1007/s00425-018-2843-8

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