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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: 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.

SUBMITTER: Finkel OM

PROVIDER: S-EPMC6876890 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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

Finkel Omri M OM Salas-González Isai I Castrillo Gabriel G Spaepen Stijn S Law Theresa F TF Teixeira Paulo José Pereira Lima PJPL Jones Corbin D CD Dangl Jeffery L JL

PLoS biology 20191113 11

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 ...[more]

PMID: 31721759

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Project description:Inorganic orthophosphate (Pi, PO43-) is the preferred phosphorus (P) source of most living cells. In enteric bacterial species such as Salmonella enterica serovar Typhimurium (Salmonella), removal of Pi from the growth medium activates a dedicated two-component signal transduction system which is composed of the membrane-bound sensor kinase PhoR and its cognate transcriptional regulator PhoB. Activated PhoB promotes transcription of genes that are involved in adaptations to low Pi conditions, such as high-affinity Pi transporters and genes required for the assimilation of alternative P sources, allowing bacteria to adapt to low Pi environments. Here, we characterize the PhoB-dependent and independent transcriptional changes elicited by Salmonella in response to P starvation. We identify a set of organic molecules that can serve as the sole P source and pinpoint genes that are involved in their assimilation. Intriguingly, a number of these genes are not under PhoB/PhoR control, indicating that in the absence of environmental Pi, Salmonella may fulfill its biosynthetic demands for P without activating a transcriptional response to Pi starvation. IMPORTANCE Phosphorus (P) is the fifth most abundant element in living cells. This element is acquired mainly as inorganic phosphate (Pi, PO43-). In enteric bacteria, P starvation activates a two-component signal transduction system which is composed of the membrane sensor protein PhoR and its cognate transcription regulator PhoB. PhoB, in turn, promotes the transcription of genes that help maintain Pi homeostasis. Here, we characterize the P starvation response of the bacterium Salmonella enterica. We determine the PhoB-dependent and independent transcriptional changes promoted by P starvation and identify proteins enabling the utilization of a range of organic substrates as sole P sources. We show that transcription and activity of a subset of these proteins are independent of PhoB and Pi availability. These results establish that Salmonella enterica can maintain Pi homeostasis and repress PhoB/PhoR activation even when cells are grown in medium lacking Pi.

Project description:Background With increasing food demand as a consequence of the growing world population, there is a corresponding demand for additional sources of phosphorus (P). Alum-phosphate (Al-P) sludge is a by-product of wastewater treatment and can be a good source of P. In this study, the response of maize (Zea mays L.) to Al-P sludge was tested. Maize was chosen as the test crop due to its prevalent use as human and animal food and as a source of biofuel. The objective of the study was to investigate Al-P sludge as a source of P compared to a commercial fertilizer (monoammonium phosphate, MAP). Methods A growth chamber assay was conducted over four cropping cycles (45 d each). The application rate was 9.7, 19.4, 29.1 and 38.8 mg P kg−1 dry soil. Amendments were applied once at the start of the first cropping cycle. Plants were harvested after each cycle and pots were re-seeded. Dry matter yield (DMY), total P uptake, Al-P uptake, soil total P and Olsen-P concentrations, pH, and EC were measured. Results DMY was significantly greater in pots amended with Al-P sludge than in pots treated with MAP. There was a significant rate × cropping cycle interaction effect on DMY with the differences among rates in cycle 1 different from those in cycle 4. Phosphorus uptake depended on cropping cycle, P source and P application rate. With sludge uptake higher than MAP in all cycles, the highest P uptake was observed at the highest application rate except for cycle 2 where this was observed at the rate of 29.1 mg kg−1. For MAP, phosphorus recovery efficiency (PRE) at the highest rate was significantly greater than that at the lowest rate whereas PRE in cycle 1 was significantly higher than that in cycle 4. In the first two cycles, aluminum uptake was negligible in both MAP and Al-P sludge treatments; however, in cycles 3 and 4, there was significantly more Al in maize from sludge amended pots. Our results show that Al-P sludge was as effective as MAP in supplying enough P for biomass yield. We, therefore, conclude that Al-P sludge could be an alternative source of P, especially for growing maize as feedstock for bioenergy.

Project description:BackgroundThe tradeoff between negative and positive interactions of facilitated species and facilitators may depend on the degree of resource availability in agroecosystems. However, the rhizospheric mechanisms driving trade-offs that occur along phosphorus (P) and water availability gradients have not yet been systematically clarified. We established three types of root isolation conditions (no barrier, nylon barrier and solid barrier) at different P and water addition levels to address the above issue in a maize-grass pea intercropping system.ResultsThe total yield and biomass net effect (NE) and the relative interaction index (RII) were significantly higher than 0 under all environmental conditions, demonstrating that plant-plant interactions generated positive effects in the intercropping system. The maize yield and biomass RII were 0.029-0.095 and 0.018-0.066, respectively, which indicated that maize growth was constantly facilitated. However, the RII for grass pea yield and biomass exhibited a different trend in comparison with maize. It was higher than 0 (as the facilitated species) under low soil P and moisture conditions and transitioned to values lower than 0 (facilitator species) under high P and moisture conditions, which showed that the type and intensity of plant-plant interactions steadily shifted with the applied stressors. Direct interactions decreased the maize rhizospheric soil pH by 1.5% and 1.9% under Low-P conditions. Notably, the rhizospheric soil acid and alkaline phosphatase secretions of maize and grass pea increased by 17.4-27.4% and 15.3-27.7%, respectively, in P-deficient soils. These results show that plant-plant interactions can effectively relieve P stress by mineralizing organophosphorus in P-deficient soils. Furthermore, the above tendency became more pronounced under drought-stressed conditions. The nylon barrier partially restricted the exchange and utilization of available nutrients and decreased the total yield and biomass by 1.8-7.8% and 1.1-7.8%, respectively. The presence of a solid barrier completely restricted interspecific rhizospheric interactions and decreased the total yield and biomass by 2.1-13.8% and 1.6-15.7%, respectively. Phytate and KH2PO4 addition intensified asymmetric interspecific competition, and grass pea was consistently subjected to competitive pressures.ConclusionBriefly, the tradeoff between facilitation and competition was driven by rhizospheric interactions, and the transition in the intensity and type of interaction was highly dependent on resource availability in a biologically diverse system.

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

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

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