Mechanisms of glacial-to-future atmospheric CO2 effects on plant immunity

• Impacts of rising atmospheric CO2 concentrations on plant disease have received much attention recently. Nonetheless, evidence about the direct mechanisms by which CO2 shapes plant immunity remains fragmented and controversial. Furthermore, the impact of sub-ambient CO2 concentrations, which plants have experienced repeatedly over the past 800,000 years, has been largely overlooked.

• A combination of gene expression analysis, phenotypic characterisation of mutants and mass spectrometry-based metabolic profiling, was implemented to determine development-independent effects of sub-ambient CO2 (saCO2) and elevated CO2 (eCO2) on Arabidopsis immunity.

• Resistance to the necrotrophic Plectosphaerella cucumerina (Pc) was repressed at saCO2 and enhanced at eCO2. This CO2-dependent resistance was associated with priming of jasmonic acid (JA)-dependent gene expression and required intact JA biosynthesis and signalling. Resistance to the biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa) increased at both eCO2 and saCO2. Although eCO2 primed salicylic acid (SA)-dependent gene expression, mutations affecting SA signalling only partially suppressed Hpa resistance at eCO2, suggesting additional mechanisms are involved. Induced production of intracellular reactive oxygen species (ROS) at saCO2 corresponded to a loss of resistance in glycolate oxidase (GOX) mutants and increased transcription of the peroxisomal catalase gene CAT2, unveiling a mechanism by which photorespiration-derived ROS determined Hpa resistance at saCO2.

• By separating indirect developmental impacts from direct immunological effects, we uncover distinct mechanisms by which CO2 shapes plant immunity and discuss their evolutionary significance.