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Thaxtomin A induces programmed cell death in Arabidopsis thaliana suspension-cultured cells

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Abstract

Thaxtomin A is the main phytotoxin produced by Streptomyces scabiei, the causative agent of common scab disease of potato. Pathogenicity of S. scabiei is dependent on the production of thaxtomin A which is required for the development of disease symptoms, such as growth inhibition and cell death. We investigated whether thaxtomin A-induced cell death was similar to the hypersensitive cell death that often occurs in response to specific pathogens or phytotoxins during the so-called hypersensitive response (HR). We demonstrated that thaxtomin A induced in Arabidopsis thaliana suspension-cultured cells a genetically controlled cell death that required active gene expression and de novo protein synthesis, and which involved fragmentation of nuclear DNA, a characteristic hallmark of apoptosis. The thaxtomin A-induced form of programmed cell death (PCD) was not a typical HR, since defence responses generally preceding or associated with the HR, such as rapid medium alkalization, oxidative burst and expression of defence-related genes PR1 and PDF1.2, were not observed in plant cells following addition of thaxtomin A. Thaxtomin A has been shown to inhibit cellulose biosynthesis (Scheible et al. in Plant Cell 15:1781, 2003). We showed that isoxaben, a specific inhibitor of cellulose biosynthesis, also induced in Arabidopsis cell suspensions a PCD similar to that induced by thaxtomin A. These data suggested that rapid changes in the plant cell wall composition and organization can induce PCD in plant cells. We discuss how rapid inhibition of cellulose biosynthesis may trigger this process.

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Abbreviations

AGPs:

Arabinogalactan proteins

CESA:

Cellulose synthase

DCB:

Dichlobenil

ET:

Ethylene

FB1:

Fumonisin B1

HR:

Hypersensitive response

JA:

Jasmonic acid

MAPK:

Mitogen-activated protein kinase

PAL:

Phenylalanine ammonia-lyase

PCD:

Programmed cell death

PLD:

Phospholipase D

ROS:

Reactive oxygen species

SA:

Salicylic acid

TUNEL:

Terminal deoxynucleotidyl transferase-mediated dUTP nick end labelling

WAKS:

Cell wall-associated kinases

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Acknowledgements

Financial support was provided by NSERC as individual grants to N.B. and C.B., and by FQRNT and Université de Sherbrooke to N.B. We also wish to thank K. Bouarab for the Arabidopsis suspension cultures, O. Domingue for initial characterization of the effects of thaxtomin A, A. Djoumad for help with DNA gel electrophoresis and northern blot analyses, and G. Grondin for help with microscopy work.

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  1. Département de biologie, Faculté des sciences, Université de Sherbrooke, Sherbrooke, QC, Canada, J1K 2R1

    Isabelle Duval, Viviane Brochu, Mathieu Simard, Carole Beaulieu & Nathalie Beaudoin

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  1. Isabelle Duval
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  2. Viviane Brochu
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Correspondence to Nathalie Beaudoin.

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Duval, I., Brochu, V., Simard, M. et al. Thaxtomin A induces programmed cell death in Arabidopsis thaliana suspension-cultured cells. Planta 222, 820–831 (2005). https://doi.org/10.1007/s00425-005-0016-z

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