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

The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response
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DOI:
10.1371/journal.pbio.3000534
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发表时间:
2019-11-01
期刊:
影响因子:
9.8
通讯作者:
Dangl, Jeffery L.
Dangl, Jeffery L.
中科院分区:
生物学1区
文献类型:
--
作者:
Finkel, Omri M.;Salas-Gonzalez, Isai;Dangl, Jeffery L.

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非菌根植物的磷饥饿反应(PSR)包括转录重编程,导致根和芽的严重生理变化和植物免疫抑制。因此,植物定殖微生物-植物微生物群-暴露于土壤磷(P)含量本身的直接影响,以及土壤P对植物形成的微生物生态位的间接影响。这些因素对植物微生物群组装的单独贡献仍然未知。为了解开这些直接和间接的影响,我们种植PSR缺陷的拟南芥突变体在长期管理的土壤磷梯度,并比较其地上部和根部微生物群的组成,野生型植物在不同的磷浓度。PSR-缺陷有一个更大的影响,细菌和真菌植物相关的微生物群的组成比土壤中的磷浓度在根和芽。为了剖析在可变P条件下的植物-微生物相互作用,我们进行了微生物群重构实验。使用185个成员的细菌合成社区(SynCom)在琼脂基质中的广泛的P浓度梯度,我们证明了细菌对植物的影响从中性或积极的相互作用到一个负面的转变,如莲座大小所测量的。这种表型转变伴随着微生物群组成的变化:伯克霍尔德氏菌属是特别丰富的植物组织下磷饥饿。通过社区辍学实验,我们表明,在没有伯克霍尔德氏菌的SynCom,植物枝条积累较高的正磷酸盐(Pi)水平比枝条殖民地与充分的SynCom,但只有在Pi饥饿条件下。因此,Pi胁迫的植物容易受到在其微生物组内发现的潜在机会竞争者的定殖,从而加剧植物的Pi饥饿。
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.