In nature, plants must respond to multiple stresses simultaneously, which likely demands cross-talk between stress-response pathways to minimize fitness costs. Here we provide genetic evidence that biotic and abiotic stress responses are differentially prioritized in Arabidopsis thaliana leaves of different ages to maintain growth and reproduction under combined biotic and abiotic stresses. Abiotic stresses, such as high salinity and drought, blunted immune responses in older rosette leaves through the phytohormone abscisic acid signaling, whereas this antagonistic effect was blocked in younger rosette leaves by PBS3 , a signaling component of the defense phytohormone salicylic acid. Plants lacking PBS3 exhibited enhanced abiotic stress tolerance at the cost of decreased fitness under combined biotic and abiotic stresses. Together with this role, PBS3 is also indispensable for the establishment of salt stress- and leaf age-dependent phyllosphere bacterial communities. Collectively, our work reveals a mechanism that balances trade-offs upon conflicting stresses at the organism level and identifies a genetic intersection among plant immunity, leaf microbiota, and abiotic stress tolerance.

Significance: Plants have evolved a powerful innate immune system to defend against microbial pathogens. Despite extensive studies, how plant immunity ultimately inhibits bacterial pathogen growth is largely unknown, due to difficulties in profiling bacterial responses in planta . In this study, we established two methods for in planta bacterial transcriptome analysis using RNA sequencing. By analyzing 27 combinations of plant immunity mutants and Pseudomonas syringae strains, we succeeded in the identification of specific bacterial transcriptomic signatures that are influenced by plant immune activation. In addition, we found that overexpression of an immune-responsive P. syringae sigma factor gene involved in iron regulation could partially counter bacterial growth restriction during plant immunity. This study illuminates the enigmatic mechanisms of bacterial growth inhibition by plant immunity.

Plants induce systemic acquired resistance (SAR) upon localized exposure to pathogens. Pipecolic acid (Pip) production via AGD2-LIKE DEFENSE RESPONSE PROTEIN1 (ALD1) is key for SAR establishment. Here, we report a positive feedback loop important for SAR induction in Arabidopsis thaliana. We showed that local activation of the MAP kinases MPK3 and MPK6 is sufficient to trigger Pip production and mount SAR. Consistent with this, mutations in MPK3 or MPK6 led to compromised Pip accumulation upon inoculation with the bacterial pathogen Pseudomonas syringae pv tomato DC3000 (Pto) AvrRpt2, which triggers strong sustained MAPK activation. By contrast, P. syringae pv maculicola and Pto, which induce transient MAPK activation, trigger Pip biosynthesis and SAR independently of MPK3/6. ALD1 expression, Pip accumulation, and SAR were compromised in mutants defective in the MPK3/6-regulated transcription factor WRKY33. Chromatin immunoprecipitation showed that WRKY33 binds to the ALD1 promoter. We found that Pip triggers activation of MPK3 and MPK6 and that MAPK activation after Pto AvrRpt2 inoculation is compromised in wrky33 and ald1 mutants. Collectively, our results reveal a positive regulatory loop consisting of MPK3/MPK6, WRKY33, ALD1, and Pip in SAR induction and suggest the existence of distinct SAR activation pathways that converge at the level of Pip biosynthesis.

Summary: Beneficial microorganisms (BMs) promote plant growth and enhance stress resistance. This review summarizes how BMs induce growth promotion by improving nutrient uptake, producing growth‐promoting hormones and stimulating root development. How BMs enhance disease resistance and help protect plants from abiotic stresses has also been explored. Growth‐defense trade‐offs are known to affect the ability of plants to survive under unfavourable conditions. This review discusses studies demonstrating that BMs regulate growth‐defense trade‐offs through microbe‐associated molecular patterns and multiple pathways, including the leucine‐rich repeat receptor‐like kinase pathway, abscisic acid signalling pathway and specific transcriptional factor regulation. This multifaceted relationship underscores the significance of BMs in sustainable agriculture. Finally, the need for integration of artificial intelligence to revolutionize biofertilizer research has been highlighted. This review also elucidates the cutting‐edge advancements and potential of plant‐microbe synergistic microbial agents.

Pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) are required for host defense against pathogens. Although PTI and ETI are intimately connected, the underlying molecular mechanisms remain elusive. In this study, we demonstrate that flg22 priming attenuates Pseudomonas syringae pv. tomato DC3000 (Pst) AvrRpt2-induced hypersensitive cell death, resistance, and biomass reduction in Arabidopsis. Mitogen-activated protein kinases (MAPKs) are key signaling regulators of PTI and ETI. The absence of MPK3 and MPK6 significantly reduces pre-PTI-mediated ETI suppression (PES). We found that MPK3/MPK6 interact with and phosphorylate the downstream transcription factor WRKY18, which regulates the expression of AP2C1 and PP2C5, two genes encoding protein phosphatases. Furthermore, we observed that the PTI-suppressed ETI-triggered cell death, MAPK activation, and growth retardation are significantly attenuated in wrky18/40/60 and ap2c1 pp2c5 mutants. Taken together, our results suggest that the MPK3/MPK6-WRKYs-PP2Cs module underlies PES and is essential for the maintenance of plant fitness during ETI.