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

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.

Genetic buffering of cyclic AMP in Arabidopsis thaliana compromises the plant immune response triggered by an avirulent strain of Pseudomonas syringae pv. tomato

“…Peptide mixtures were desalted using SepPak columns (Teknokroma), eluted with 60% acetonitrile (ACN) and 0.1% TFA, dried in a SpeedVac evaporator (SAVANT SPD131DDA, Thermo Fisher) and stored at −20°C prior to mass spectrometry analysis, which was conducted as reported in Hussain et al . ().…”

“…The bacterial suspension was infiltrated from the abaxial side into leaves using a 1‐mL syringe without a needle. Control (mock) inoculations were carried out with 10 m m MgCl 2 as previously described (Hussain et al ., ; Doccula et al ., ).…”

“…Whole leaves from 5‐ to 6‐week‐old cASxNES‐YC3.6NES‐YC3.6 plants, inoculated with 10 7 cfu mL −1 of avirulent PstAvrB or 10 m m MgCl 2 as a control, were cut at the level of the petiole, gently placed on a slide and covered with a coverslip (Hussain et al ., ; Doccula et al ., ), and viewed using a Nikon Ti‐E inverted fluorescence microscope (Ti‐E; http://www.nikon.com/) with a CFI 4× 0.13 dry objective. Excitation light was produced by a fluorescence lamp (Prior Lumen 200 PRO; Prior Scientific; http://www.prior.com) at 440 nm (436/20 nm) set to 50%.…”

“…As a consequence of a generally disturbed cell homeostasis, a prompt response to alleviate the impact of stress is necessary. Major players of this early phase of defence response are signalling molecules, including secondary messengers such as calcium ions (Ca 2+ ) or cyclic nucleotides (cNMP; Gao et al ., ; Van Damme et al ., ; Hussain et al ., ).…”

An Arabidopsis thaliana leucine-rich repeat protein harbors an adenylyl cyclase catalytic center and affects responses to pathogens

“…We have also shown that the early response of the phenylalanine ammonia lyase gene (PALa) and the late response of the gene encoding the pathogenesis-related protein (PR1a) show critical dependence on cGMP and importantly, that differential cGMP signatures occur in responses to virulent and avirulent Pst strains (Meier et al, 2009). Accordingly, a key role of cGMP in the induction of systemic acquired response in plants challenged with avirulent pathogens has been reported (Hussain et al, 2016). These observations were an indication that the growing family of structurally diverse molecules with functional mononucleotide cyclase domains (ACs and GCs), have critical and specific roles in many plant processes including defence against pathogens (Meier et al, 2007).…”