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Balancing Trade-Offs Between Biotic and Abiotic Stress Responses Through Leaf Age-Dependent Variation in Stress Hormone Cross-Talk

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Balancing Trade-Offs Between Biotic and Abiotic Stress Responses Through Leaf Age-Dependent Variation in Stress Hormone Cross-Talk Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk Matthias L. Berensa, Katarzyna W. Wolinskaa, Stijn Spaepena, Jörg Zieglerb, Tatsuya Noboria, Aswin Naira,1, Verena Krülera,2, Thomas M. Winkelmüllera, Yiming Wanga, Akira Minea,3, Dieter Beckera, Ruben Garrido-Otera,c, Paul Schulze-Leferta,c,4, and Kenichi Tsudaa,4 aDepartment of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany; bDepartment of Molecular Signal Processing, Leibnitz Institute of Plant Biochemistry, 06120 Halle, Germany; and cCluster of Excellence on Plant Sciences, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany Contributed by Paul Schulze-Lefert, December 10, 2018 (sent for review October 8, 2018; reviewed by Xinnian Dong and Murray R. Grant) In nature, plants must respond to multiple stresses simultaneously, microbiota (7), which contribute to plant performance under which likely demands cross-talk between stress-response pathways adverse environmental conditions (8–11). SA modulates coloni- to minimize fitness costs. Here we provide genetic evidence that zation of the A. thaliana root microbiota by specific bacterial biotic and abiotic stress responses are differentially prioritized in taxa, although this was not accompanied by a detectable impact Arabidopsis thaliana leaves of different ages to maintain growth on host survival of the tested SA biosynthesis and signaling and reproduction under combined biotic and abiotic stresses. Abi- mutants (12, 13). In field experiments, drought induced a relative otic stresses, such as high salinity and drought, blunted immune enrichment of multiple lineages of Actinobacteria and Chloro- responses in older rosette leaves through the phytohormone absci- flexi in the rice root microbiota, whereas, in sorghum roots, sic acid signaling, whereas this antagonistic effect was blocked in relative enrichments of Actinobacteria and Firmicutes were ob- – younger rosette leaves by PBS3, a signaling component of the de- served (14 17). Whether and how cross-talk between biotic and fense phytohormone salicylic acid. Plants lacking PBS3 exhibited abiotic stress response pathways impacts the assembly of the enhanced abiotic stress tolerance at the cost of decreased fitness plant microbiota remains unknown. under combined biotic and abiotic stresses. Together with this role, PBS3 is also indispensable for the establishment of salt stress- and Significance leaf age-dependent phyllosphere bacterial communities. Collec- tively, our work reveals a mechanism that balances trade-offs upon Plants are exposed to conflicting stresses simultaneously in nature. conflicting stresses at the organism level and identifies a genetic As stress responses are costly, plants likely coordinate these re- intersection among plant immunity, leaf microbiota, and abiotic sponses to minimize fitness costs. The nature and extent to which stress tolerance. plants employ inducible mechanisms to cope with combined physical and biological stresses remains unknown. We identify a combined stress | phytohormone | plant fitness | microbiota | stress trade-off genetic mechanism by which leaves of distinct ages differentially control stress-response cross-talk. At the organism level, this n nature, plants encounter and must appropriately respond to mechanism balances stress-response trade-offs to maintain plant Idiverse stresses to survive and reproduce. Different stress sig- growth and reproduction during combined stresses. We also show naling pathways are connected, providing regulatory potential to that this leaf age-dependent stress-response prioritization influ- maximize fitness (1). For instance, plants exposed to abiotic ences the establishment of plant-associated leaf bacterial com- stresses such as high salinity and drought often display reduced munities. This study illustrates the importance of active balancing immune activity (2). As stress responses are costly, prioritization of stress-response trade-offs for plant fitness maintenance and in stress responses would allow plants to allocate more resources for interaction with the plant microbiota. to abiotic stress responses and increase plant fitness in the ab- Author contributions: M.L.B., P.S.-L., and K.T. designed research; M.L.B., K.W.W., J.Z., A.N., sence of biotic stress (3). However, this prioritization does not V.K., T.M.W., Y.W., and D.B. performed research; R.G.-O. contributed new reagents/analytic explain how plants maintain fitness when simultaneously exposed tools; M.L.B., K.W.W., S.S., J.Z., T.N., T.M.W., A.M., P.S.-L., and K.T. analyzed data; and M.L.B., to biotic and abiotic stresses. P.S.-L., and K.T. wrote the paper. Phytohormones play critical roles in stress responses and pri- Reviewers: X.D., Duke University; and M.R.G., University of Warwick. oritization (4). In an evolutionarily conserved mechanism, phy- The authors declare no conflict of interest. tohormone signaling mediated by abscisic acid (ABA) promotes This open access article is distributed under Creative Commons Attribution License 4.0 abiotic stress tolerance and suppresses signaling of the biotic (CC BY). stress-related phytohormone salicylic acid (SA). Consequently, Data deposition: The data reported in this paper have been deposited in the Gene Ex- plant immunity is lowered during abiotic stresses such as drought pression Omnibus (GEO) database, https://www.ncbi.nlm.nih.gov/geo (accession no. and salt stress (5). In Arabidopsis thaliana, ABA suppresses ex- GSE114645) and in the European Nucleotide Archive, https://www.ebi.ac.uk/ena (acces- pression of the SA biosynthesis gene SA INDUCTION DEFICIENT sion no. PRJEB26793). 2 (SID2) (5). ABA application causes proteasome-mediated deg- 1Present address: Albrecht-von-Haller-Institut für Pflanzenwissenschaften, Georg-August- radation of the SA receptor NONEXPRESSOR OF PR GENE 1 Universität Göttingen, D–37073 Göttingen, Germany. (NPR1) (6). Molecular cross-talk between ABA and SA provides 2Present address: Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms a plausible mechanism for prioritization of abiotic over biotic Universität, 48149 Münster, Germany. stress responses. Such a mechanism would provide plants with 3Present address: Ritsumeikan Global Innovation Research Organization, Ritsumeikan adaptive potential when abiotic stresses are major threats. How- University, 525-8577 Shiga, Japan. ever, it is unknown whether this hormonal cross-talk is still 4To whom correspondence may be addressed. Email: [email protected] or tsuda@ advantageous when plants simultaneously encounter biotic and mpipz.mpg.de. abiotic stresses. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. In natural soils, healthy plants are colonized by taxonomically 1073/pnas.1817233116/-/DCSupplemental. structured microbial communities, collectively called the plant Published online January 23, 2019. 2364–2373 | PNAS | February 5, 2019 | vol. 116 | no. 6 www.pnas.org/cgi/doi/10.1073/pnas.1817233116 Downloaded by guest on September 30, 2021 Age and developmental stage are important factors influenc- markedly prolonged (28). However, similar to WT, we observed − ing stress responses in animals and plants. For instance, as A. that ABA effects on Pto hrcC growth were dependent on leaf age thaliana plants age, SA-mediated immunity is enhanced (18). Plants despite the juvenile trait being manifest in younger and older also display age-dependent responses at the organ level. Young A. leaves (Fig. 1 F and G). Thus, leaf age but not vegetative phase thaliana rosette leaves exhibit greater SA accumulation and SA- change likely controls ABA–SA cross-talk, with marked conse- mediated immunity in comparison with older rosette leaves (19). quences for the SA response and bacterial resistance. Evidence for leaf age-dependent variation also exists for abiotic stress (20, 21). Based on the optimal defense theory (ODT), in ABA Suppresses Immunity via the ABA RESPONSIVE ELEMENT BINDING defending themselves against herbivores, plants prioritize tissues, PROTEIN–SNAC-A Transcription Factor Cascade. ABA RESPONSIVE such as young leaves, that are more valuable for the whole plant ELEMENT (ABRE) BINDING PROTEIN (AREB) transcription (22). However, whether leaf age-dependent variation in stress re- factors (TFs) redundantly regulate a major part of ABA-mediated sponses is a simple prioritization analogous to the ODT or an active transcriptional changes (24) (SI Appendix,Fig.S2A). We found − strategy to increase plant fitness is not understood. that ABA-triggered suppression of immunity against Pto hrcC in Here we show that biotic and abiotic stress responses are dif- old leaves was compromised in areb triple mutant plants (areb1 ferentially prioritized in a leaf age-dependent manner in A. thali- areb2 abf3) (24), indicating that ABA-triggered immune suppres- ana to maintain fitness under combined stresses. Abiotic stresses sion requires AREB-mediated transcription. Next, we further dis- dampen immunity in old rosette leaves, whereas the SA signaling sected this transcriptional cascade. AREB TFs have been shown to components PBS3 and NPR1 protected young rosette leaves from bind to the promoters of SNAC-A TFs in vitro (29), and a subset of ABA-mediated immune suppression. pbs3 mutant plants exhibited SNAC-A TFs, ANAC019, 055, and 072, whose gene expression is enhanced abiotic stress tolerance but showed compromised fitness
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