Climate change and the associated increase in atmospheric CO₂ levels may affect the severity of plant diseases and threaten future crop yields. Here, we compared responses of the model plant Arabidopsis thaliana to leaf and root pathogens with hemi-biotrophic or necrotrophic infection strategies under pre-industrial, current, and future atmospheric CO₂ conditions. Defenses against biotrophs are generally regulated by salicylic acid (SA) signaling, whereas jasmonic acid (JA) signaling controls defenses against necrotrophs. Under the CO₂ conditions tested, basal expression of the JA-responsive marker gene PDF1.2 increased at increasing CO₂ concentrations. The SA-responsive marker genes ICS1 and FRK1 showed an opposite behavior, being lower expressed under high CO₂ and higher expressed under low CO₂, respectively. Accordingly, plants showed enhanced resistance to the necrotrophic leaf pathogen Botrytis cinerea under high CO₂, while resistance to the hemi-biotrophic leaf pathogen Pseudomonas syringae pv. tomato was reduced. The opposite was true for plants grown under low CO₂. Disease severity caused by the soil-borne pathogens Fusarium oxysporum f.sp. raphani and Rhizoctonia solani was similar under all CO₂ conditions tested. Collectively, our results stress the notion that atmospheric CO₂ impacts the balance between SA- and JA-dependent defenses and concomitant resistance against foliar (hemi)biotrophic and necrotrophic pathogens. The direction of the CO₂-mediated effects on SA- and JA-mediated defenses varies between reported studies, suggesting that the defense output is influenced by environmental context. These findings highlight that a wider dynamic range of climate change parameters should be studied simultaneously to harness plant traits for the development of future climate-resilient crops.

Main conclusion: Carbonic anhydrases CA1 and CA4 attenuate plant immunity and can contribute to altered disease resistance levels in response to changing atmospheric CO₂ conditions. β-Carbonic anhydrases (CAs) play an important role in CO₂ metabolism and plant development, but have also been implicated in plant immunity. Here we show that the bacterial pathogen Pseudomonas syringae and application of the microbe-associated molecular pattern (MAMP) flg22 repress CA1 and CA4 gene expression in Arabidopsis thaliana. Using the CA double-mutant ca1ca4, we provide evidence that CA1 and CA4 play an attenuating role in pathogen- and flg22-triggered immune responses. In line with this, ca1ca4 plants exhibited enhanced resistance against P. syringae, which was accompanied by an increased expression of the defense-related genes FRK1 and ICS1. Under low atmospheric CO₂ conditions (150 ppm), when CA activity is typically low, the levels of CA1 transcription and resistance to P. syringae in wild-type Col-0 were similar to those observed in ca1ca4. However, under ambient (400 ppm) and elevated (800 ppm) atmospheric CO₂ conditions, CA1 transcription was enhanced and resistance to P. syringae reduced. Together, these results suggest that CA1 and CA4 attenuate plant immunity and that differential CA gene expression in response to changing atmospheric CO₂ conditions contribute to altered disease resistance levels.

Atmospheric CO2 influences plant growth and stomatal aperture. Effects of high or low CO2 levels on plant disease resistance are less well understood. Here, resistance of Arabidopsis thaliana against the foliar pathogen Pseudomonas syringae pv. tomato DC3000 (Pst) was investigated at three different CO2 levels: high (800 ppm), ambient (450 ppm) and low (150 ppm). Under all conditions tested, infection by Pst resulted in stomatal closure within 1 h after inoculation. However, subsequent stomatal reopening at 4 h, triggered by the virulence factor coronatine (COR), occurred only at ambient and high CO2, but not at low CO2. Moreover, infection by Pst was reduced at low CO2 to the same extent as infection by mutant Pst cor-. Under all CO2 conditions, the ABA mutants aba2-1 and abi1-1 were as resistant to Pst as wild-type plants under low CO2, which contained less ABA. Moreover, stomatal reopening mediated by COR was dependent on ABA. Our results suggest that reduced ABA levels at low CO2 contribute to the observed enhanced resistance to Pst by deregulation of virulence responses. This implies that enhanced ABA levels at increasing CO2 levels may have a role in weakening plant defense.

Plant hormone abscisic acid (ABA) is essential for regulating plant growth and various stress responses. ABA-mediated signaling depends on local ABA levels rather than the overall cellular ABA concentration. While cellular concentration of ABA can be detected using Förster resonance energy transfer (FRET)-based ABA probes, direct imaging of subcellular ABA levels remains unsolved. Here, we modified the previously reported ABAleon2.1 and generated a new ABA sensor, named ABAleon2.1_Tao3. Via transient expression in tobacco (Nicotiana tabacum) protoplasts, we targeted ABAleon2.1_Tao3s to the endoplasmic reticulum (ER) membrane with the ABA sensing unit facing the cytosol and the ER, respectively, through a nanobody–epitope-mediated protein interaction. Combining FRET with fluorescence lifetime imaging microscopy, ABA-triggered-specific increases in the fluorescence lifetime of the donor mTurquoise in the ABAleon2.1_Tao3 were detected in both transient assays and stably transformed Arabidopsis plants. In tobacco protoplasts, ER membrane-targeted ABAleon2.1_Tao3s showed a generally higher basal level of ABA in the ER than that in the cytosol and ER-specific alterations in the level of ABA upon environmental cues. In ABAleon2.1_Tao3-transformed Arabidopsis roots, mannitol triggered increases in cytosolic ABA in the division zone and increases in ER ABA in the elongation and maturation zone within 1 h after treatment, both of which were abolished in the bg1-2 mutant, suggesting the requirement for BG1 in osmotic stress-triggered early ABA induction in Arabidopsis roots. These data demonstrate that ABAleon2.1_Tao3s can be used to monitor ABA levels in the cytosol and the ER, providing key information on stress-induced changes in the level of ABA in different subcellular compartments.

The symbiosis between plants and root‐colonizing arbuscular mycorrhizal (AM) fungi is one of the most ecologically important examples of interspecific cooperation in the world. AM fungi provide benefits to plants; in return plants allocate carbon resources to fungi, preferentially allocating more resources to higher‐quality fungi. However, preferential allocations from plants to symbionts may vary with environmental context, particularly when resource availability affects the relative value of symbiotic services. We ask how differences in atmospheric CO₂‐levels influence root colonization dynamics between AMF species that differ in their quality as symbiotic partners. We find that with increasing CO₂‐conditions and over multiple plant generations, the more beneficial fungal species is able to achieve a relatively higher abundance. This suggests that increasing atmospheric carbon supply enables plants to more effectively allocate carbon to higher‐quality mutualists, and over time helps reduce lower‐quality AM abundance. Our results illustrate how environmental context may affect the extent to which organisms structure interactions with their mutualistic partners and have potential implications for mutualism stability and persistence under global change.