The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response

Finkel, Omri M.; Salas-Gonz�lez, Isai; Castrillo, Gabriel; Spaepen, Stijn; Law, Theresa F.; Teixeira, Paulo Jos� Pereira Lima; Jones, Corbin D.; Dangl, Jeffery L.

Abstract

Phosphate starvation response (PSR) in nonmycorrhizal plants comprises transcriptional reprogramming resulting in severe physiological changes to the roots and shoots and repression of plant immunity. Thus, plant-colonizing microorganisms-the plant microbiota-are exposed to direct influence by the soil's phosphorus (P) content itself as well as to the indirect effects of soil P on the microbial niches shaped by the plant. The individual contribution of these factors to plant microbiota assembly remains unknown. To disentangle these direct and indirect effects, we planted PSR-deficient Arabidopsis mutants in a long-term managed soil P gradient and compared the composition of their shoot and root microbiota to wild-type plants across different P concentrations. PSR-deficiency had a larger effect on the composition of both bacterial and fungal plant-associated microbiota than soil P concentrations in both roots and shoots. To dissect plant-microbe interactions under variable P conditions, we conducted a microbiota reconstitution experiment. Using a 185-member bacterial synthetic community (SynCom) across a wide P concentration gradient in an agar matrix, we demonstrated a shift in the effect of bacteria on the plant from a neutral or positive interaction to a negative one, as measured by rosette size. This phenotypic shift was accompanied by changes in microbiota composition: the genus Burkholderia was specifically enriched in plant tissue under P starvation. Through a community drop-out experiment, we demonstrated that in the absence of Burkholderia from the SynCom, plant shoots accumulated higher ortophosphate (Pi) levels than shoots colonized with the full SynCom but only under Pi starvation conditions. Therefore, Pi-stressed plants are susceptible to colonization by latent opportunistic competitors found within their microbiome, thus exacerbating the plant's Pi starvation.

Citation

Finkel, O. M., Salas-González, I., Castrillo, G., Spaepen, S., Law, T. F., Teixeira, P. J. P. L., Jones, C. D., & Dangl, J. L. (2019). The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response. PLoS Biology, 17(11), 1-34. https://doi.org/10.1371/journal.pbio.3000534

• Journal Article Type: Article
• Acceptance Date: Oct 24, 2019
• Online Publication Date: Nov 13, 2019
• Publication Date: Nov 13, 2019
• Deposit Date: Jul 27, 2020
• Publicly Available Date: Jul 30, 2020
• Journal: PLoS Biology
• Print ISSN: 1544-9173
• Electronic ISSN: 1545-7885
• Publisher: Public Library of Science
• Peer Reviewed: Peer Reviewed
• Volume: 17
• Issue: 11
• Article Number: e3000534
• Pages: 1-34
• DOI: https://doi.org/10.1371/journal.pbio.3000534
• Keywords: General Agricultural and Biological Sciences; General Immunology and Microbiology; General Biochemistry, Genetics and Molecular Biology; General Neuroscience
• Public URL: https://nottingham-repository.worktribe.com/output/3548896
• Publisher URL: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3000534