The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response
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: themore »
- Authors:
-
[1];
[1];
[1];
[2];
[1];
[1]
- Univ. of North Carolina, Chapel Hill, NC (United States)
- Max Planck Inst. for Plant Breeding Research, Köln (Germany)
- Publication Date:
- Research Org.:
- Univ. of Nebraska, Lincoln, NE (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Science Foundation (NSF)
- OSTI Identifier:
- 1599047
- Grant/Contract Number:
- SC0014395; SC001043; F32-GM117758-02; IOS-1917270; IOS-1343020
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Biology (Online)
- Additional Journal Information:
- Journal Name: PLoS Biology (Online); Journal Volume: 17; Journal Issue: 11; Journal ID: ISSN 1545-7885
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Finkel, Omri M., Salas-González, Isai, Castrillo, Gabriel, Spaepen, Stijn, Law, Theresa F., Teixeira, Paulo José Pereira Lima, Jones, Corbin D., and Dangl, Jeffery L. The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response. United States: N. p., 2019.
Web. doi:10.1371/journal.pbio.3000534.
Finkel, Omri M., Salas-González, Isai, Castrillo, Gabriel, Spaepen, Stijn, Law, Theresa F., Teixeira, Paulo José Pereira Lima, Jones, Corbin D., & Dangl, Jeffery L. The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response. United States. https://doi.org/10.1371/journal.pbio.3000534
Finkel, Omri M., Salas-González, Isai, Castrillo, Gabriel, Spaepen, Stijn, Law, Theresa F., Teixeira, Paulo José Pereira Lima, Jones, Corbin D., and Dangl, Jeffery L. Wed .
"The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response". United States. https://doi.org/10.1371/journal.pbio.3000534. https://www.osti.gov/servlets/purl/1599047.
@article{osti_1599047,
title = {The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response},
author = {Finkel, Omri M. and Salas-González, Isai and Castrillo, Gabriel and Spaepen, Stijn and Law, Theresa F. and Teixeira, Paulo José Pereira Lima and Jones, Corbin D. and Dangl, Jeffery L.},
abstractNote = {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.},
doi = {10.1371/journal.pbio.3000534},
journal = {PLoS Biology (Online)},
number = 11,
volume = 17,
place = {United States},
year = {Wed Nov 13 00:00:00 EST 2019},
month = {Wed Nov 13 00:00:00 EST 2019}
}
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Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi
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