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

The impacts of rising atmospheric CO₂ concentrations on plant disease have received increasing attention, but with little consensus emerging on the direct mechanisms by which CO₂ shapes plant immunity. Furthermore, the impact of sub-ambient CO₂ concentrations, which plants have experienced repeatedly over the past 800 000 yr, has been largely overlooked. A combination of gene expression analysis, phenotypic characterisation of mutants and mass spectrometry-based metabolic profiling was used 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 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.