Direct inhibition of phosphate transport by immune signaling in Arabidopsis

Dindas, Julian, DeFalco, Thomas A., Yu, Gang, Zhang, Lu, David, Pascale, Bjornson, Marta, Thibaud, Marie-Christine, Custódio, Valéria, Castrillo, Gabriel, Nussaume, Laurent, Macho, Alberto P. and Zipfel, Cyril (2022) Direct inhibition of phosphate transport by immune signaling in Arabidopsis. Current Biology, 32 (2). 488-495.e5. ISSN 0960-9822

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Abstract

Soil availability of inorganic ortho-phosphate (PO 4 3−, P i) is a key determinant of plant growth and fitness. 1 Plants regulate the capacity of their roots to take up inorganic phosphate by adapting the abundance of H +-coupled phosphate transporters of the PHOSPHATE TRANSPORTER 1 (PHT1) family 2 at the plasma membrane (PM) through transcriptional and post-translational changes driven by the genetic network of the phosphate starvation response (PSR). 3–8 Increasing evidence also shows that plants integrate immune responses to alleviate phosphate starvation stress through the association with beneficial microbes. 9–11 Whether and how such phosphate transport is regulated upon activation of immune responses is yet uncharacterized. To address this question, we first developed quantitative assays based on changes in the electrical PM potential to measure active P i transport in roots in real time. By inserting micro-electrodes into bulging root hairs, we were able to determine key characteristics of phosphate transport in intact Arabidopsis thaliana (hereafter Arabidopsis) seedlings. The fast P i-induced depolarization observed was dependent on the activity of the major phosphate transporter PHT1;4. Notably, we observed that this PHT1;4-mediated phosphate uptake is repressed upon activation of pattern-triggered immunity. This inhibition depended on the receptor-like cytoplasmic kinases BOTRYTIS-INDUCED KINASE 1 (BIK1) and PBS1-LIKE KINASE 1 (PBL1), which both phosphorylated PHT1;4. As a corollary to this negative regulation of phosphate transport by immune signaling, we found that PHT1;4-mediated phosphate uptake normally negatively regulates anti-bacterial immunity in roots. Collectively, our results reveal a mechanism linking plant immunity and phosphate homeostasis, with BIK1/PBL1 providing a molecular integration point between these two important pathways.

Item Type: Article
Additional Information: Funding Information: This work was supported by the European Research Council under the European Union (EU)'s Horizon 2020 research and innovation program (grant agreements no. 309858, project "PHOSPHinnATE" and no. 773153, project "IMMUNO-PEPTALK" to C.Z.), The Gatsby Charitable Foundation (to C.Z.), the University of Zurich (to C.Z.), and the Swiss National Science Foundation (grant 31003A_182625 to C.Z.). J.D. and T.A.D. were supported by postdoctoral fellowships from the European Molecular Biology Organization (EMBO LTFs no. 683-2018 to J.D. and no. 100-2017 to T.A.D.). T.A.D. was further supported by the Natural Sciences and Engineering Research Council of Canada (NSERC PDF-532561-2019). V.C. and G.C. were supported by the Biotechnology and Biological Sciences Research Council and National Science Foundation (BBSRC-NSF) (grant no. BB/V011294/1 to G.C.). G.Y. and L.Z. were supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant XDB27040204 to A.P.M.), the Chinese 1000 Talents Program (to A.P.M.), and the Shanghai Center for Plant Stress Biology. The authors thank all members of the Zipfel lab for fruitful discussion and feedback on the manuscript. J.D. T.A.D. and C.Z. conceived and designed the project. J.D. T.A.D. G.Y. L.Z. P.D. M.B. M.-C.T. V.C. and G.C. generated materials, performed experiments, and/or analyzed data. L.N. A.P.M. and C.Z. supervised the project. J.D. T.A.D. and C.Z. wrote the manuscript with input from all authors. The authors declare no competing interests.
Uncontrolled Keywords: pht1,electrophysiology,kinase,phosphate,plant immunity,root microbiome,neuroscience(all),biochemistry, genetics and molecular biology(all),agricultural and biological sciences(all) ,/dk/atira/pure/subjectarea/asjc/2800
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Depositing User: LivePure Connector
Date Deposited: 21 Dec 2021 13:30
Last Modified: 15 Mar 2022 01:22
URI: https://ueaeprints.uea.ac.uk/id/eprint/82760
DOI: 10.1016/j.cub.2021.11.063

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