Intrinsic non-stomatal resilience to drought of the photosynthetic apparatus in Coffea spp. is strengthened by elevated air [CO₂]

Growing water restrictions associated with climate changes constitute daunting challenges to crop performance. This study unveils the impacts of moderate (MWD) or severe (SWD) water deficit, and their interaction with air [CO2], on the photosynthetic apparatus of Coffea canephora Pierre ex A. Froehner cv. Conilon Clone 153 (CL153) and Coffea arabica L. cv. Icatu. Seven year-old potted plants grown under 380 (aCO2) or 700 μl l -1 (eCO2) [CO2] gradually reached predawn water potentials between -1.6 and -2.1 MPa (MWD), and below -3.5 MPa (SWD). Under drought, stomata closure was chiefly related to abscisic acid (ABA) rise. Increasing drought severity progressively affected gas exchange and fluorescence parameters in both genotypes, with non-stomatal limitations becoming gradually dominating, especially regarding the photochemical and biochemical components of CL153 SWD plants. In contrast, Icatu plants were highly tolerant to SWD, with minor, if any, negative impacts on the potential photosynthetic functioning and components (e.g., Amax, Fv/Fm, electron carriers, photosystems (PSs) and ribulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO) activities). Besides, drought-stressed Icatu plants displayed increased abundance of a large set of proteins associated with the photosynthetic apparatus (PSs, light-harvesting complexes, cyclic electron flow, RuBisCO activase) regardless of [CO2]. Single eCO2 did not promote stomatal and photosynthetic down-regulation in both genotypes. Instead, eCO2 increased photosynthetic performance, moderately reinforced photochemical (PSs activity, electron carriers) and biochemical (RuBisCO, ribulose-5-phosphate kinase) components, whereas photoprotective mechanisms and protein abundance remained mostly unaffected. In both genotypes, under MWD, eCO2 superimposition delayed stress severity and promoted photosynthetic functioning with lower energy dissipation and PSII impacts, whereas stomatal closure was decoupled from increases in ABA. In SWD plants, most impacts on the photosynthetic performance were reduced by eCO2, especially in the moderately drought affected CL153 genotype, although maintaining RuBisCO as the most sensitive component, deserving special breeder's attention to improve coffee sustainability under future climate scenarios.