Plant phosphate status drives host microbial preferences: a trade‐off between fungi and bacteria

Recent discoveries show that plant recruitment of fungi and bacteria in a non‐mycorrhizal host follows different strategies dependent on phosphate availability. A new study by Morcillo et al (2019) demonstrates that volatile compounds synthesized by rhizobacteria contribute to phosphate starvation response‐dependent regulation of bacterial colonization and immune system activation in Arabidopsis thaliana plants.

A new study shows that phosphate availability to the host plant drives microbial colonization versus immunity activation switch in response to bacterial volatile compounds.

Soil and plant nutrient status guides morphological, metabolic and physiological changes in the root and shoot that impact plant immunity. Phosphorus is the second most important macronutrient after nitrogen in terms of limiting plant growth in soil. Both plant‐associated bacteria and fungi can solubilize phosphate in the soil. Generally, fungi are more efficient phosphorus mobilizers due to their ability to traverse long distances within the soil and to transfer phosphate directly to root cells. It is well established that symbiotic interactions between roots and arbuscular mycorrhizal fungi (AMF) are tightly regulated by phosphate status in the rhizosphere and plants (Müller & Harrison, 2019). Less is known about phosphate signalling in association with beneficial bacteria or fungi other than AMF. Recently, beneficial root endophytic fungi, such as the Ascomycota Colletotrichum tofieldiae and the Basidiomycota Serendipita indica (formerly known as Piriformospora indica), were shown to alleviate phosphate starvation in A. thaliana (Bakshi et al, 2015; Hiruma et al, 2016), suggesting that alternative partnerships have evolved to compensate for the absence of functional relationships with AMF in this host species. Also, fungi of the order Helotiales play an important role in phosphate transfer to non‐mycorrhizal plants in phosphate‐deficient soil (Almario et al, 2017; Fabianska et al, 2019). Importantly, the beneficial interaction of Arabidopsis with C. tofieldiae was shown to be controlled by the phosphate starvation response (PSR) system and plant phosphate status. Hence, in this association, symbiosis is established only under phosphate deficiency, in which case the fungus transfers phosphate to its host. Under sufficient phosphate conditions, the presence of this endophyte activates plant defences and fungal colonization is restricted by plant‐produced tryptophan (TRP)‐derived secondary metabolites. Since TRP‐derived glucosinolates also control endophytic colonization by the beneficial fungus S. indica in Arabidopsis roots (Lahrmann et al, 2015; Koprivova et al, 2019), certain glucosinolates are likely to serve as pivotal host molecules for modulating fungal symbiosis in Arabidopsis.

In this issue of the EMBO Journal, Morcillo and colleagues elegantly demonstrate that the situation is different when a beneficial bacterium, Bacillus amyloliquefaciens strain GB03, interacts with Arabidopsis roots. In phosphate‐deficient plants, this rhizobacterium induces an extreme PSR, accumulation of anthocyanin and activation of hormone‐driven defences, specifically salicylic acid (SA) biosynthesis and signalling. The same bacterium is beneficial to the plant in phosphate‐sufficient conditions, as measured by total leaf area per plant. The authors identify a bacterial volatile compound, diacetyl (DA), as the mediator of this beneficial interaction and show that DA has a dual effect on Arabidopsis depending on phosphate availability. DA exacerbates the plant PSR and induces accumulation of SA in phosphate‐depleted plants, but facilitates colonization by B. amyloliquefaciens in phosphate‐sufficient conditions without compromising plant defences against pathogens. Importantly, Morcillo and colleagues show that DA‐mediated bacterial accommodation is dependent on the plant PSR components. Thus, the study establishes a new connection between bacterial volatiles, PSR and plant immunity.

Taken together, the data suggest that Arabidopsis plants use different strategies for determining mutualism or immunity to bacteria and fungi (Fig 1). This is supported by recent findings in the group of Dangl (Finkel et al, 2019), in which a shift was observed in the effect of bacteria on the plant from a neutral or positive to a negative interaction when phosphate concentration was low, as measured by rosette size and phosphate content in Arabidopsis shoots. In this study, Finkel and colleagues report evidence that the composition of both bacterial and fungal communities is impacted by the plant PSR, but there are differences in community assembly cues for fungi or bacteria. The bacterial microbiota composition is largely driven by soil bacterial community composition. However, changes of the fungal community are uncoupled from altered soil fungal community composition, suggesting that the plant is more selective about which fungi are permitted to proliferate in the root. A recent observation that bacterial root commensals modulate fungal assemblage in the root (Duran et al, 2018) additionally points to influence on microbiota composition by plant‐driven microbial preferences that are affected by phosphate status. Finkel and colleagues use a microbiota drop‐out approach, in which one member of the microbiota is removed to investigate its function in a synthetic community (SynCom). This approach shows that certain opportunistic Burkholderia strains are specifically enriched in plant tissue under phosphate starvation and exacerbate an already tricky situation for plants under phosphate‐limiting conditions. The fact that plant enrichment of the Burkholderia under phosphate‐deficient conditions occurs via a PSR‐independent mechanism leaves open the question of which mechanism/s controls PSR‐dependent bacterial community assembly. DA could represent one of the key mediators of plant–microbe interaction with potential role in bacterial community assembly—a hypothesis that is yet to be empirically validated in a complex microbiota context.

Figure 1. Picking the winning team: plant microbial preferences are a reflection of the current needs of the host plant for phosphate.

 

These recent studies demonstrate the beauty and power of both microbiota drop‐out experiments and binary mechanistic approaches in uncovering the complex interactions between host plant nutritional status and its interactions with fungal and bacterial microbiota. Further studies will be required to validate these principles in ecological studies.

The EMBO journal (2020) 39: e104144