Gluconacetobacter diazotrophicus triggers ISR involving SA and JA/Et defense-related pathways to respond against Ralstonia solanacearum in Arabidopsis and optimizes the cellular redox state maintaining reduced FITNESS levels

Abstract

Background and Aims: This research investigates the biocontrol mechanisms of Gluconacetobacter diazotrophicus against the harmful bacterium Ralstonia pseudosolanacearum, causal agent of bacterial wilt disease. Given the ongoing need for effective control strategies, our focus lies in understanding the hormonal pathways, particularly the salicylic acid (SA) and jasmonic acid/ethylene (JA/Et) signaling pathways, involved in plant defense. Methods: Effects of SA signalization deficiencies in plant-endophyte-pathogen interactions were observed through colonization ability, morpho-anatomical, physiological and disease severity parameters of sid2 (unable to produce SA via isochorismate synthase 1) and NahG (unable to accumulate SA) compared to wild-type Col0 plants treated with G. diazotrophicus, R. pseudosolanacearum or both bacteria. Additionally, pr1, pr5, myc2, pdf1.2 (associated with SA or JA/Et defense response), and fitness (linked to redox homeostasis) relative expression were analyzed in Col0 plants. Results: G. diazotrophicus increased root hairs in Col0 and NahG. This correlates with a higher endophytic colonization frequency, enhanced lignification and xylem expansion. However, chlorophyll content and bacterial counts indicated an endophyte-NahG imbalance. Disease index, R. pseudosolanacearum bacterial counts and H2O2 accumulation were lower in G. diazotrophicus inoculated Col0 and expression analysis revealed up-regulation of pr1 and myc2. R. pseudosolanacearum infection increased 15.2 times pdf1.2 levels, which is significantly further in co-inoculated plants than in those inoculated with pathogenic bacteria alone. G. diazotrophicus managed to maintain fitness low levels even after R. pseudosolanacearum infection. Conclusions: The interplay G. diazotrophicus-Arabidopsis, mediated by the expression of pr, myc2 and fitness primes for subsequent infection with R. pseudosolanacearum, triggering the expression of JA/Et pathway genes.