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• W3217605000 abstract "Iron (Fe) and phosphate (Pi) are two essential nutrients for plant growth. Both impact plant development differently and their respective deficiency leads to multiple physiological disorders, resulting in severe reduction of crop production. The chemistry of these two elements is deeply inter-connected, as in the soil phosphate naturally associates to ferric oxides (resulting from aerobic conditions observed in most cultivated soils) to create insoluble complexes that can no longer be taken up by the plants' import systems. Modifying the concentration of either phosphate or iron in the environment (such as by using fertilizer application) has direct consequences on the bioavailability of the second element (Figure 1). For example, reducing Pi content in the growth medium of Arabidopsis plants resulted, according to the amount of iron present in the medium, in a three- to six-fold accumulation of this ion concentration in plants (Hirsch et al., 2006Hirsch J. Marin E. Floriani M. Chiarenza S. Richaud P. Nussaume L. Thibaud M.C. Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants.Biochimie. 2006; 88: 1767-1771https://doi.org/10.1016/j.biochi.2006.05.007Crossref PubMed Scopus (154) Google Scholar). Reminiscent of this observation, the low phosphate condition inhibits root growth of Arabidopsis seedlings in an Fe-dependent manner (Svistoonoff et al., 2007Svistoonoff S. Creff A. Reymond M. Sigoillot-Claude C. Ricaud L. Blanchet A. Nussaume L. Desnos T. Root tip contact with low-phosphate media reprograms plant root architecture.Nat. Genet. 2007; 39: 792-796https://doi.org/10.1038/ng2041Crossref PubMed Scopus (452) Google Scholar; Balzergue et al., 2017Balzergue C. Dartevelle T. Godon C. Laugier E. Meisrimler C. Teulon J.M. Creff A. Bissler M. Brouchoud C. Hagege A. et al.Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation.Nat. Commun. 2017; 8: 15300https://doi.org/10.1038/ncomms15300Crossref PubMed Scopus (203) Google Scholar). These interactions are not only observed in the soil (or growth medium), but also take place within the plants where such chemical associations are also observed with phytate, for example. This important source of Pi storage in many seeds also traps a lot of iron. Therefore, it is not surprising that the Fe/Pi pair, in addition to its chemical bonds, promoted adaptive responses in living beings linking these two elements. For example, one way plants cope with iron shortage is to release complexed iron by secretion of organic compounds, such as malate or citrate. Transcriptomic studies have highlighted that modification of Pi supply affected the regulation of multiple genes involved in iron (and other metals) homeostasis (Misson et al., 2005Misson J. Raghothama K.G. Jain A. Jouhet J. Block M.A. Bligny R. Ortet P. Creff A. Somerville S. Rolland N. et al.A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation.Proc. Natl. Acad. Sci. U S A. 2005; 102: 11934-11939Crossref PubMed Scopus (726) Google Scholar; Thibaud et al., 2010Thibaud M.C. Arrighi J.F. Bayle V. Chiarenza S. Creff A. Bustos R. Paz-Ares J. Poirier Y. Nussaume L. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis.Plant J. 2010; 64: 775-789https://doi.org/10.1111/j.1365-313X.2010.04375.xCrossref PubMed Scopus (233) Google Scholar). However, it is difficult to decipher whether this is a direct or indirect effect, since modifying Pi concentration also modulates iron bioavailability. Promoter analysis of these genes identified the P1BS motif, known to be the target of PHR1, the master gene controlling Pi homeostasis (Rubio et al., 2001Rubio V. Linhares F. Solano R. Martin A.C. Iglesias J. Leyva A. Paz-Ares J. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae.Genes Dev. 2001; 15: 2122-2133https://doi.org/10.1101/gad.204401Crossref PubMed Scopus (962) Google Scholar). For some of them, such as those encoding ferritin, additional experiments (such as the yeast one-hybrid assay) confirmed the reality of this association (Bournier et al., 2013Bournier M. Tissot N. Mari S. Boucherez J. Lacombe E. Briat J.F. Gaymard F. Arabidopsis FERRITIN 1 (AtFer1) gene regulation by the PHOSPHATE STARVATION RESPONSE 1 (AtPHR1) transcription factor reveals a direct molecular link between iron and phosphate homeostasis.J. Biol. Chem. 2013; https://doi.org/10.1074/jbc.M113.482281Abstract Full Text Full Text PDF PubMed Scopus (117) Google Scholar). Genetic experiments even provided an opportunity to demonstrate that, despite the presence of an iron-dependent regulatory sequence in the promoter of this gene, the induction observed during Pi deficiency resulted only from the activity of the PHR and PHL gene families (Bournier et al., 2013Bournier M. Tissot N. Mari S. Boucherez J. Lacombe E. Briat J.F. Gaymard F. Arabidopsis FERRITIN 1 (AtFer1) gene regulation by the PHOSPHATE STARVATION RESPONSE 1 (AtPHR1) transcription factor reveals a direct molecular link between iron and phosphate homeostasis.J. Biol. Chem. 2013; https://doi.org/10.1074/jbc.M113.482281Abstract Full Text Full Text PDF PubMed Scopus (117) Google Scholar). These results clearly indicate the tight link between Pi and iron raised during plant evolution. A recent study by Dr. Yi’s group (Guo et al., 2021Guo M. Ruan W. Zhang Y. Zhang Y. Wang X. Guo Z. Wang L. Zhou T. Paz-Ares J. Yi K. A reciprocal inhibitory module for Pi and iron signaling.Mol. Plant. 2021; https://doi.org/10.1016/j.molp.2021.09.011Abstract Full Text Full Text PDF Scopus (26) Google Scholar) represents a major advance in the field by establishing that HRZs (hemerythrin motif-containing really interesting new gene and zinc-finger proteins) also regulates PHR2, the rice homolog of Arabidopsis PHR1. Interestingly, HRZ proteins are the rice homologs of the Arabidopsis iron deficiency-induced E3 ligases named BTS for Brutus (Long et al., 2010Long T.A. Tsukagoshi H. Busch W. Lahner B. Salt D.E. Benfey P.N. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots.Plant Cell. 2010; 22: 2219-2236https://doi.org/10.1105/tpc.110.074096Crossref PubMed Scopus (453) Google Scholar). The Arabidopsis BTS targets the transcription factor complex PYE/PYEL (Popeye/Popeye-like) (Long et al., 2010Long T.A. Tsukagoshi H. Busch W. Lahner B. Salt D.E. Benfey P.N. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots.Plant Cell. 2010; 22: 2219-2236https://doi.org/10.1105/tpc.110.074096Crossref PubMed Scopus (453) Google Scholar), a crucial actor controlling iron homeostasis. Under iron deficiency, BTS promotes the degradation of PYEL, whereas iron destabilizes HRZ/Brutus (Selote et al., 2018Selote D. Matthiadis A. Gillikin J.W. Sato M.H. Long T.A. The E3 ligase BRUTUS facilitates degradation of VOZ1/2 transcription factors.Plant Cell Environ. 2018; 41: 2463-2474https://doi.org/10.1111/pce.13363Crossref PubMed Scopus (30) Google Scholar), thereby favoring the transcriptional activity of the PYE/PYL complex. Interestingly, it was reported 3 years ago that BTS targets other transcription factors regulating drought and cold stress (Selote et al., 2018Selote D. Matthiadis A. Gillikin J.W. Sato M.H. Long T.A. The E3 ligase BRUTUS facilitates degradation of VOZ1/2 transcription factors.Plant Cell Environ. 2018; 41: 2463-2474https://doi.org/10.1111/pce.13363Crossref PubMed Scopus (30) Google Scholar), suggesting that it may integrate responses to other abiotic stresses. The results now presented by the Yi group clearly confirm this view by connecting the HRZ proteins with phosphate homeostasis (Guo et al., 2021Guo M. Ruan W. Zhang Y. Zhang Y. Wang X. Guo Z. Wang L. Zhou T. Paz-Ares J. Yi K. A reciprocal inhibitory module for Pi and iron signaling.Mol. Plant. 2021; https://doi.org/10.1016/j.molp.2021.09.011Abstract Full Text Full Text PDF Scopus (26) Google Scholar)! Iron deficiency reduced the rice responses to phosphate deficiency thereby promoting fine-tuning between these two elements. It is worth noting that, under rich phosphate conditions, the SPX1 proteins repress the transcriptional activity of the PHR proteins. The HRZ/BTS proteins act clearly at a distinct level by controlling directly the abundance of PHR proteins. In return, PHR also negatively regulates the expression of BTS during phosphate starvation, highlighting the close relationship observed in the present article between iron and phosphate (Guo et al., 2021Guo M. Ruan W. Zhang Y. Zhang Y. Wang X. Guo Z. Wang L. Zhou T. Paz-Ares J. Yi K. A reciprocal inhibitory module for Pi and iron signaling.Mol. Plant. 2021; https://doi.org/10.1016/j.molp.2021.09.011Abstract Full Text Full Text PDF Scopus (26) Google Scholar). This work thus illustrates the fine-tuning of the multiple regulations used by plants to adapt to their environment and the reciprocal controls between these nutrients. One surprising phenomenon observed with bts mutants is their enhanced development compared with wild-type control when grown under low iron conditions: mutant harboring longer roots and reduced chlorosis (Long et al., 2010Long T.A. Tsukagoshi H. Busch W. Lahner B. Salt D.E. Benfey P.N. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots.Plant Cell. 2010; 22: 2219-2236https://doi.org/10.1105/tpc.110.074096Crossref PubMed Scopus (453) Google Scholar; Selote et al., 2018Selote D. Matthiadis A. Gillikin J.W. Sato M.H. Long T.A. The E3 ligase BRUTUS facilitates degradation of VOZ1/2 transcription factors.Plant Cell Environ. 2018; 41: 2463-2474https://doi.org/10.1111/pce.13363Crossref PubMed Scopus (30) Google Scholar). A similar observation can be seen by combining the effects of phosphate and iron deficiency. Surprisingly, this partially rescues the severe growth defect affecting iron-starved rice plantlets (Mongon et al., 2017Mongon J. Chaiwong N. Bouain N. Prom U.T.C. Secco D. Rouached H. Phosphorus and iron deficiencies influences rice shoot growth in an oxygen dependent manner: insight from upland and lowland rice.Int. J. Mol. Sci. 2017; 18https://doi.org/10.3390/ijms18030607Crossref PubMed Scopus (14) Google Scholar). In the future, it will therefore be interesting to check whether the increased activity of PHR1 (due to the absence of BTS repression in the bts mutant or by the release of SPX inhibitory effect during Pi starvation) could explain such results that defy synergistic effects (as here less by less gives more). The homeostasis of other nutrients is also linked with that of phosphate. One of the main ones is another crucial macronutrient, nitrate. Interestingly, this link also involves an E3 ubiquitin ligase named NLA for NITROGEN LIMITATION ADAPTATION (Kant et al., 2011Kant S. Peng M. Rothstein S.J. Genetic regulation by NLA and MicroRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis.PLoS Genet. 2011; 7: e1002021https://doi.org/10.1371/journal.pgen.1002021Crossref PubMed Scopus (298) Google Scholar). NLA modulates the abundance of Pi transporters, indicating another crucial regulatory step of Pi homeostasis (Lin et al., 2013Lin W.Y. Huang T.K. Chiou T.J. NITROGEN LIMITATION ADAPTATION, a target of MicroRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis.Plant Cell. 2013; 25: 4061-4074https://doi.org/10.1105/tpc.113.116012Crossref PubMed Scopus (240) Google Scholar; Park et al., 2014Park B.S. Seo J.S. Chua N.H. NITROGEN LIMITATION ADAPTATION recruits PHOSPHATE2 to target the phosphate transporter PT2 for degradation during the regulation of Arabidopsis phosphate homeostasis.Plant Cell. 2014; 26: 454-464https://doi.org/10.1105/tpc.113.120311Crossref PubMed Scopus (190) Google Scholar). All these results are clear illustrations of the importance of multi-ion controls. They also pinpoint the importance during plant nutrition physiological experiments to tightly control the ionic concentrations present in the culture medium. This is really crucial, given the important crosstalks observed, especially when they can promote antagonistic responses that may mislead our reasoning if they are not taken into account! We thank S. Hani for her critical reading and C. Mercier for her graphic talents. No conflict of interest declared. The ANR projects BIOPHYT (ANR-18-CE20-023) and ULTIM (ANR-21-CE12-0016) supported respectively T.D. and L.N." @default.
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• W3217605000 title "“Je t'aime moi non plus: A love-hate relationship between iron and phosphate" @default.
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