Spermine deficiency shifts the balance between jasmonic acid and salicylic acid-mediated defence responses in Arabidopsis

Polyamines are small aliphatic polycations present in all living organisms. In plants, the most abundant polyamines are putrescine (Put), spermidine (Spd) and spermine (Spm). Polyamine levels change in response to different pathogens, including Pseudomonas syringae pv. tomato DC3000 (Pst DC3000). However, the regulation of polyamine metabolism and their specific contributions to defence are not fully understood. Here we report that stimulation of Put biosynthesis by Pst DC3000 is dependent on coronatine (COR) perception and jasmonic acid (JA) signalling, independently of salicylic acid (SA). Conversely, lack of Spm in spermine synthase (spms) mutant stimulated galactolipids and JA biosynthesis, and JA signalling under basal conditions and during Pst DC3000 infection, whereas compromised SA-pathway activation and defence outputs through SA–JA antagonism. The dampening of SA responses correlated with COR and Pst DC3000-inducible deregulation of ANAC019 expression and its key SA-metabolism gene targets. Spm deficiency also led to enhanced disease resistance to the necrotrophic fungal pathogen Botrytis cinerea and stimulated endoplasmic reticulum (ER) stress signalling in response to Pst DC3000. Overall, our findings provide evidence for the integration of polyamine metabolism in JA- and SA-mediated defence responses, as well as the participation of Spm in buffering ER stress during defence.

This work was financially supported by the grants: PID2021-126896OB-I00 funded by Ministerio de Ciencia e Innovación MCIN/Agencia Estatal de Investigación AEI/10.13039/501100011033 (Spain) and by the “European Regional Development Fund (ERDF) a way of making Europe”; PDC2021-121267-I00 funded by Ministerio de Ciencia e Innovación MCIN/Agencia Estatal de Investigación AEI/10.13039/501100011033 (Spain) and European Union Next GenerationEU/PRTR. A.G-C. acknowledges support from Generalitat Valenciana (CIAICO/2021/063). C.Z., J.Z. and C.D. acknowledge support from the CSC (China Scholarship Council) for funding their doctoral fellowship. E.M. is holder of the grant PRE2018-083289 funded by MCIN/AEI/10.13039/501100011033 and by “European Social Fund Investing in your future”.

Peer reviewed