Constitutive cyclic GMP accumulation in Arabidopsis thaliana compromises systemic acquired resistance induced by an avirulent pathogen by modulating local signals.

Jamshaid Hussain,Raman Pachaiappan,Alexander Graf,Diana Bellin,Alex Costa,Jian Chen,Silvia Martínez-Jaime,Elodie Vandelle,Laura De Gara,Mabrouk Bouneb,Paola Fincato,Vittoria Locato,Smrutisanjita Behera,Sara Cimini,Maria Concetta De Pinto,Francesca Griggio,Emanuela Blanco,Wilma Sabetta

doi:10.1038/srep36423

Abstract

The infection of Arabidopsis thaliana plants with avirulent pathogens causes the accumulation of cGMP with a biphasic profile downstream of nitric oxide signalling. However, plant enzymes that modulate cGMP levels have yet to be identified, so we generated transgenic A. thaliana plants expressing the rat soluble guanylate cyclase (GC) to increase genetically the level of cGMP and to study the function of cGMP in plant defence responses. Once confirmed that cGMP levels were higher in the GC transgenic lines than in wild-type controls, the GC transgenic plants were then challenged with bacterial pathogens and their defence responses were characterized. Although local resistance was similar in the GC transgenic and wild-type lines, differences in the redox state suggested potential cross-talk between cGMP and the glutathione redox system. Furthermore, large-scale transcriptomic and proteomic analysis highlighted the significant modulation of both gene expression and protein abundance at the infection site, inhibiting the establishment of systemic acquired resistance. Our data indicate that cGMP plays a key role in local responses controlling the induction of systemic acquired resistance in plants challenged with avirulent pathogens.

Highlights

Plants respond to the presence of microorganisms by deploying efficient defence mechanisms leading to incompatible plant–pathogen interactions
To monitor the concentration of cGMP in A. thaliana plants we developed a new technique based on Perkin Elmer AlphaScreen technology
The method optimized in this work for plant samples was able to detect cGMP increase in A. thaliana leaves infiltrated with the cGMP-specific phosphodiesterase inhibitor sildenafil 1 mg/mL30, reaching around 70 pmol/g FW 4 hours post-infiltration (Supplementary Fig. S1a)

Summary

Introduction

Plants respond to the presence of microorganisms by deploying efficient defence mechanisms leading to incompatible plant–pathogen interactions These mechanisms include a basal defence response following the recognition of common microbial features, known as pathogen-associated molecular patterns or microbe-associated molecular patterns. As well as inducing cell death, NO regulates the expression of a battery of defence genes allowing the establishment of local resistance, and systemic acquired resistance (SAR)[6] The latter is a broad and long-lasting systemic response that protects uninfected tissues against subsequent infections by diverse pathogens, and this requires the careful balancing of phytohormone cross-talk, which strongly influences the outcome of plant immunity[7,8]. A cGMP-specific PDE activity has been detected in A. thaliana seedlings[29] but the corresponding gene(s) have not been isolated

Methods

Results

Conclusion