High CO2- and pathogen-driven expression of the carbonic anhydrase βCA3 confers basal immunity in tomato

Abstract

Atmospheric CO2 concentrations exert a strong influence on the susceptibility of plants to pathogens. However, the mechanisms involved in the CO2-dependent regulation of pathogen resistance are largely unknown. Here we show that the expression of tomato (Solanum lycopersicum) β-CARBONIC ANHYDRASE 3 (βCA3) is induced by the virulent pathogen Pseudomonas syringae pv. tomato DC3000. The role of βCA3 in the high CO2-mediated response in tomato and two other Solanaceae crops is distinct from that in Arabidopsis thaliana. Using βCA3 knock-out and over-expression plants, we demonstrate that βCA3 plays a positive role in the activation of basal immunity, particularly under high CO2. βCA3 is transcriptionally activated by the transcription factor NAC43 and is also post-translationally regulated by the receptor-like kinase GRACE1. The βCA3 pathway of basal immunity is independent on stomatal- and salicylic-acid-dependent regulation. Global transcriptome analysis and cell wall metabolite measurement implicate cell wall metabolism/integrity in βCA3-mediated basal immunity under both CO2 conditions. These data not only highlight the importance of βCA3 in plant basal immunity under high CO2 in a well-studied susceptible crop–pathogen system, but they also point to new targets for disease management strategies in a changing climate.