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While the response of Arabidopsis thaliana to drought, herbivory or fungal infection has been well-examined, the consequences of exposure to a series of such (a)biotic stresses are not well studied. This work reports on the genetic mechanisms underlying the Arabidopsis response to single osmotic stress, and to combinatorial stress, either fungal infection using Botrytis cinerea or herbivory using Pieris rapae caterpillars followed by an osmotic stress treatment. Several small-effect genetic loci associated with rosette dry weight (DW), rosette water content (WC), and the projected rosette leaf area in response to combinatorial stress were mapped using univariate and multi-environment genome-wide association approaches. A single-nucleotide polymorphism (SNP) associated with DROUGHT-INDUCED 19 (DI19) was identified by both approaches, supporting its potential involvement in the response to combinatorial stress. Several SNPs were found to be in linkage disequilibrium with known stress-responsive genes such as PEROXIDASE 34 (PRX34), BASIC LEUCINE ZIPPER 25 (bZIP25), RESISTANCE METHYLATED GENE 1 (RMG1) and WHITE RUST RESISTANCE 4 (WRR4). An antagonistic effect between biotic and osmotic stress was found for prx34 and arf4 mutants, which suggests PRX34 and ARF4 play an important role in the response to the combinatorial stress., (© 2024 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.)

In nature, roots of healthy plants are colonized by multikingdom microbial communities that include bacteria, fungi, and oomycetes. A key question is how plants control the assembly of these diverse microbes in roots to maintain host-microbe homeostasis and health. Using microbiota reconstitution experiments with a set of immunocompromised Arabidopsis thaliana mutants and a multikingdom synthetic microbial community (SynCom) representative of the natural A. thaliana root microbiota, we observed that microbiota-mediated plant growth promotion was abolished in most of the tested immunocompromised mutants. Notably, more than 40% of between-genotype variation in these microbiota-induced growth differences was explained by fungal but not bacterial or oomycete load in roots. Extensive fungal overgrowth in roots and altered plant growth was evident at both vegetative and reproductive stages for a mutant impaired in the production of tryptophan-derived, specialized metabolites ( cyp79b2/b3 ). Microbiota manipulation experiments with single- and multikingdom microbial SynComs further demonstrated that 1) the presence of fungi in the multikingdom SynCom was the direct cause of the dysbiotic phenotype in the cyp79b2/b3 mutant and 2) bacterial commensals and host tryptophan metabolism are both necessary to control fungal load, thereby promoting A. thaliana growth and survival. Our results indicate that protective activities of bacterial root commensals are as critical as the host tryptophan metabolic pathway in preventing fungal dysbiosis in the A. thaliana root endosphere., Competing Interests: The authors declare no competing interest., (Copyright © 2021 the Author(s). Published by PNAS.)

Reminiscent to the microbiota-gut-brain axis described in animals, recent advances indicate that plants can take advantage of belowground microbial commensals to orchestrate aboveground stress responses. Integration of plant responses to microbial cues belowground and environmental cues aboveground emerges as a mechanism that promotes stress tolerance in plants. Using recent examples obtained from reductionist and community-level approaches, we discuss the extent to which perception of aboveground biotic and abiotic stresses can cascade along the shoot-root axis to sculpt root microbiota assembly and modulate the growth of root commensals that bolster aboveground stress tolerance. We propose that host modulation of microbiota-root-shoot circuits contributes to phenotypic plasticity and decision-making in plants, thereby promoting adaptation to rapidly changing environmental conditions., (Copyright © 2021 Elsevier Ltd. All rights reserved.)

In nature, plants need to be able to quickly adapt to changing environments during their lifetime in order to maintain fitness. Different defense responses are not only costly, but often also antagonistic to one another. Hence, when faced with multiple stresses simultaneously, plants likely have to prioritize their defense responses. This type of crosstalk between different stress response pathways is suggested to balance the high costs of triggering and maintaining stress responses with the limited amount of resources available to a plant. This assumption is in accordance with the optimal defense theory (ODT), which states that living organisms put more resources into protection of the most valuable tissues, but does not explain how plants survive combined stress conditions in nature. In this review, we describe recent evidence that expands on the framework of the ODT by suggesting that under combined stress plants spatially separate contrasting stress responses, rather than protecting the most valuable tissues to simultaneously protect themselves from contrasting stressors. We discuss the implications of these findings for understanding plant responses to combined stresses and suggest potentially fruitful avenues for further research.

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., Competing Interests: The authors declare no conflict of interest., (Copyright © 2019 the Author(s). Published by PNAS.)