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PHR1 Balances between Nutrition and Immunity in Plants

2017; Elsevier BV; Volume: 41; Issue: 1 Linguagem: Inglês

10.1016/j.devcel.2017.03.019

1878-1551

Hans Motte, Tom Beeckman,

Legume Nitrogen Fixing Symbiosis

Plants assemble beneficial root-associated microbiomes to support growth, especially in nutrient-poor conditions. To do so, however, plants have to suppress their immune system. Reporting in Nature, Castrillo et al., 2017Castrillo G. Teixeira P.J.P.L. Paredes S.H. Law T.F. de Lorenzo L. Feltcher M.E. Finkel O.M. Breakfield N.W. Mieczkowski P. Jones C.D. et al.Nature. 2017; 543: 513-518Crossref PubMed Scopus (442) Google Scholar identified PHOSPHATE STARVATION RESPONSE1 (PHR1) as a central regulator in this balance between nutrient stress response and immune regulation. Plants assemble beneficial root-associated microbiomes to support growth, especially in nutrient-poor conditions. To do so, however, plants have to suppress their immune system. Reporting in Nature, Castrillo et al., 2017Castrillo G. Teixeira P.J.P.L. Paredes S.H. Law T.F. de Lorenzo L. Feltcher M.E. Finkel O.M. Breakfield N.W. Mieczkowski P. Jones C.D. et al.Nature. 2017; 543: 513-518Crossref PubMed Scopus (442) Google Scholar identified PHOSPHATE STARVATION RESPONSE1 (PHR1) as a central regulator in this balance between nutrient stress response and immune regulation. The coevolution of plants and microbial organisms has led to well-established interactions that play key roles in the functioning of terrestrial communities and ecosystems. Some of these interactions are detrimental and lead to the development of defense mechanisms, whereas others turn out to be beneficial. The latter can be exploited by the plant and have evolved into the manifestation of stable root-associated microbiomes. How plants can become engaged in such interactions while staying protected against harmful relationships is an intriguing question. Well-balanced control of the plant immune system is thus very central, being even more challenging in changing nutrient conditions. In the latter case, plants will favor micro-organisms that might be beneficial in the given stress condition. For example, deprivation of phosphate, one of the most important plant macronutrients, leads to greater colonization by fungi that convert plant-inaccessible phosphate into bioavailable inorganic phosphate (Pi), thereby stimulating translocation of Pi in the root (Hiruma et al., 2016Hiruma K. Gerlach N. Sacristán S. Nakano R.T. Hacquard S. Kracher B. Neumann U. Ramírez D. Bucher M. O'Connell R.J. Schulze-Lefert P. Cell. 2016; 165: 464-474Abstract Full Text Full Text PDF PubMed Scopus (338) Google Scholar). Interestingly, phosphate deprivation leads simultaneously to the suppression of the plant immune system, opening the door for plant–microbe interactions. A recent study showed that a mutualistic interaction was made possible by repression of the immune response under phosphate starvation conditions (Hacquard et al., 2016Hacquard S. Kracher B. Hiruma K. Münch P.C. Garrido-Oter R. Thon M.R. Weimann A. Damm U. Dallery J.-F. Hainaut M. et al.Nat. Commun. 2016; 7: 11362Crossref PubMed Scopus (151) Google Scholar). Such observations point toward a fine-tuned interaction between the phosphate starvation response (PSR) and the immune system. Recent progress in PSR research led to the identification of key steps in its sensing and response: inositol polyphosphate molecules, assumed to show a positive correlation with Pi, bind to SPX proteins and trigger their association with other specific proteins, including the transcription factors PHOSPHATE STARVATION RESPONSE1 (PHR1) and PHR1-LIKE1 (PHL1) (Wild et al., 2016Wild R. Gerasimaite R. Jung J.-Y. Truffault V. Pavlovic I. Schmidt A. Saiardi A. Jessen H.J. Poirier Y. Hothorn M. Mayer A. Science. 2016; 352: 986-990Crossref PubMed Scopus (313) Google Scholar, Puga et al., 2014Puga M.I. Mateos I. Charukesi R. Wang Z. Franco-Zorrilla J.M. de Lorenzo L. Irigoyen M.L. Masiero S. Bustos R. Rodríguez J. et al.Proc. Natl. Acad. Sci. USA. 2014; 111: 14947-14952Crossref PubMed Scopus (264) Google Scholar) (Figure 1). Free PHR1 transcription factors bind to the PHR1 binding site (P1BS) element that is present in the promoters of phosphate starvation-induced (PSI) genes. Although PHR1 possibly controls a wide variety of genes related to diverse processes (Bustos et al., 2010Bustos R. Castrillo G. Linhares F. Puga M.I. Rubio V. Pérez-Pérez J. Solano R. Leyva A. Paz-Ares J. PLoS Genet. 2010; 6: e1001102Crossref PubMed Scopus (447) Google Scholar), PSI genes are mainly involved in mechanisms to increase Pi uptake (Figure 1). Until now, it remained unclear how PSR can interact with the plant immune system. In a recent Nature paper, Castrillo et al., 2017Castrillo G. Teixeira P.J.P.L. Paredes S.H. Law T.F. de Lorenzo L. Feltcher M.E. Finkel O.M. Breakfield N.W. Mieczkowski P. Jones C.D. et al.Nature. 2017; 543: 513-518Crossref PubMed Scopus (442) Google Scholar tackled this issue by exploiting a synthetic bacterial community (SynCom) representative for a wild-type root endophytic community and studying its effect on the PSR. By comparing wild-type plants with plants carrying a mutation in the PHR1 gene, a master regulator of PSR, the authors could demonstrate an enhanced immune function in the mutants, arguing for PHR1 being involved in the PSR immune response crosstalk. In addition, different transcriptome and ChIP-seq experiments revealed a direct link between immune responses and the PSR: PHR1 itself directly targets genes involved in immune system responses such as jasmonic acid and/or salicylic acid (SA) pathway genes. Interestingly, the authors showed via mutant studies that PHR1 in general suppresses the SA-responsive genes, which were previously shown to be involved in the defense against improper root colonizers (Lebeis et al., 2015Lebeis S.L. Paredes S.H. Lundberg D.S. Breakfield N. Gehring J. McDonald M. Malfatti S. Glavina del Rio T. Jones C.D. Tringe S.G. Dangl J.L. Science. 2015; 349: 860-864Crossref PubMed Scopus (613) Google Scholar). In addition, responses triggered by the bacterial elicitor flg22 were increased in phr1;phl1 mutants, again pointing to a negative regulation of the immune responses by PHR1 (Castrillo et al., 2017Castrillo G. Teixeira P.J.P.L. Paredes S.H. Law T.F. de Lorenzo L. Feltcher M.E. Finkel O.M. Breakfield N.W. Mieczkowski P. Jones C.D. et al.Nature. 2017; 543: 513-518Crossref PubMed Scopus (442) Google Scholar). Because PHR1 suppresses the immune response, Castrillo et al., 2017Castrillo G. Teixeira P.J.P.L. Paredes S.H. Law T.F. de Lorenzo L. Feltcher M.E. Finkel O.M. Breakfield N.W. Mieczkowski P. Jones C.D. et al.Nature. 2017; 543: 513-518Crossref PubMed Scopus (442) Google Scholar hypothesized that phr1;phl1 mutants should be less susceptible to pathogens. Indeed, although these mutants will not be able to cope with phosphate starvation, they showed an enhanced disease resistance to different pathogens. A remarkable conclusion of the experiments using the SynCom communities is that the induction of PSI genes, and thus a functional PSR in low-phosphate conditions, depends on the presence of a microbial community. This supports the idea that plant roots are by definition accompanied by an ever-present association of micro-organisms that are able to respond to phosphate starvation conditions. This seems to be true for at least fungi, which have been hypothesized to have facilitated the colonization of land by plants 460 million years ago (Redecker et al., 2000Redecker D. Kodner R. Graham L.E. Science. 2000; 289: 1920-1921Crossref PubMed Scopus (768) Google Scholar). But why had plants not uncoupled the PSR and the immune response during evolution? Possibly, because phosphate is an essential element for plants, they redirect all available resources toward mechanisms to cope with phosphate starvation during phosphate stress. The risk for infections might be less detrimental than phosphate shortage, and hence plants may have prioritized the PSR and suppressed the immune system. PHR1, however, does not necessarily block the entire immune system. For example, immune responses will still be activated by certain pathogens, even in low-phosphate conditions (Hacquard et al., 2016Hacquard S. Kracher B. Hiruma K. Münch P.C. Garrido-Oter R. Thon M.R. Weimann A. Damm U. Dallery J.-F. Hainaut M. et al.Nat. Commun. 2016; 7: 11362Crossref PubMed Scopus (151) Google Scholar). Hence, it might be more likely that the coupling of the PSR and the immune system exists to allow, in low-phosphate conditions, colonization of the root by Pi-mobilizing micro-organisms. Accordingly, production of indole glucosinolates, also induced by PHR1, is known to stimulate the beneficial interaction with mycorrhizal fungi (Hiruma et al., 2016Hiruma K. Gerlach N. Sacristán S. Nakano R.T. Hacquard S. Kracher B. Neumann U. Ramírez D. Bucher M. O'Connell R.J. Schulze-Lefert P. Cell. 2016; 165: 464-474Abstract Full Text Full Text PDF PubMed Scopus (338) Google Scholar). Overall, it seems that plants have difficulties coping with phosphate starvation and pathogens at the same time. If phosphate resources are depleted, PHR1 suppresses immune responses and prioritizes phosphate stress responses. Some pathogens apparently have evolved to exploit this vulnerability in low-phosphate conditions. For example, phytoplasmas (Lu et al., 2014Lu Y.-T. Li M.-Y. Cheng K.-T. Tan C.M. Su L.-W. Lin W.-Y. Shih H.-T. Chiou T.-J. Yang J.-Y. Plant Physiol. 2014; 164: 1456-1469Crossref PubMed Scopus (56) Google Scholar) and presumably citrus pathogens from the genus Candidatus liberibacter (Zhao et al., 2013Zhao H. Sun R. Albrecht U. Padmanabhan C. Wang A. Coffey M.D. Girke T. Wang Z. Close T.J. Roose M. et al.Mol. Plant. 2013; 6: 301-310Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar) both induce a PHR1-dependent PSR to suppress the defense mechanisms of the host plants and are as such able to infect them. In general, the finding of a direct coupling between PSR and the immune system may inspire new approaches toward tackling plant disease problems and nutrient stress. In conclusion, Castrillo et al., 2017Castrillo G. Teixeira P.J.P.L. Paredes S.H. Law T.F. de Lorenzo L. Feltcher M.E. Finkel O.M. Breakfield N.W. Mieczkowski P. Jones C.D. et al.Nature. 2017; 543: 513-518Crossref PubMed Scopus (442) Google Scholar demonstrated the direct integration of PSR and immune responses by PHR1 and provided useful insights that might be used to increase phosphate use efficiency and disease control. The question remains of how soil microbiota activate PHR1. Inositol polyphosphate decomposition, PHR1-SPX dissociation, or PHR1 itself might need extra factors that are induced by sugars or microbial metabolites or proteins. These parts of the PSR pathway are subjects for future research to further unravel the microbiota-dependent PSR.