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Recent Advances in Nutrient Sensing and Signaling

2012; Elsevier BV; Volume: 5; Issue: 6 Linguagem: Inglês

10.1093/mp/sss109

1674-2052

Daniel P. Schachtman,

Plant Stress Responses and Tolerance

Nutrient sensing and signaling is an important area of plant biological research because of the role of plant nutrition in crop production and the constraints that nutrient limitations put on plant growth and optimal yields. The increasing cost, the limited supplies, and the negative impacts of excess application of fertilizer on the environment have all led to more research into understanding how plants acquire, sense, and utilize nutrients. Approximately two and a half years ago, Molecular Plant published a special issue (March 2010) with a series of review articles and original research papers on nutrient sensing and signaling. Many reviews have appeared and provide excellent summaries for research advances in this area (Ho and Tsay, 2010Ho C.H. Tsay Y.F. Nitrate, ammonium, and potassium sensing and signaling.Curr. Opin. Plant Biol. 2010; 13: 604-610Crossref PubMed Scopus (94) Google Scholar; Krouk et al., 2010aKrouk G. Crawford N.M. Coruzzi G.M. Tsay Y.F. Nitrate signaling: adaptation to fluctuating environments.Curr. Opin. Plant Biol. 2010; 13: 266-273Crossref PubMed Scopus (262) Google Scholar; Chiou and Lin, 2011Chiou T.J. Lin S.I. Signaling network in sensing phosphate availability in plants.Annu. Rev. Plant Biol. 2011; 62: 185-206Crossref PubMed Scopus (525) Google Scholar; Gutierrez, 2012Gutierrez R.A. Systems biology for enhanced plant nitrogen nutrition.Science. 2012; 336: 1673-1675Crossref PubMed Scopus (144) Google Scholar). This highlight updates readers on some of the advances and emerging themes in this field of research since the special issue. Transcriptional profiling has been widely used over the past 10 years to discover genes involved in response to changes in nutrients and has been one important tool used to understand and elucidate signal transduction mechanisms in plants. Regulation at the transcription level is a key part of response to changes in nutrient concentrations, with many transcription factors playing key roles in the signal transduction cascades for nutrient sensing. Other levels of regulation have also been shown to be involved in responses to changes in mineral nutrients including posttranscriptional regulation due to micro-RNAs (miRNAs), chromatin modification, posttranslational modifications, protein–protein interactions, and hormone regulation. Posttranscriptional regulation due to miRNAs is an active area of research which has been enabled by advances in sequencing technologies. The induction and repression of miRNAs have been found in response to changes in external phosphorus, nitrogen, and sulfur. Recent surveys have revealed over 40micro-RNAs whose expression is altered by plant phosphorus status. Many of these miRNAs target a class of genes which are P starvation-responsive (PSR) (Kuo and Chiou, 2011Kuo H.F. Chiou T.J. The role of microRNAs in phosphorus deficiency signaling.Plant Physiol. 2011; 156: 1016-1024Crossref PubMed Scopus (126) Google Scholar). Some of the miRNAs such as miR399, miR827, and miR2111 are specifically induced by P deficiency, while others such as miRNA169, miR395, and miR398 are also induced by N, K, Cu, Fe, and S deficiency (Kuo and Chiou, 2011Kuo H.F. Chiou T.J. The role of microRNAs in phosphorus deficiency signaling.Plant Physiol. 2011; 156: 1016-1024Crossref PubMed Scopus (126) Google Scholar). In Arabidopsis, miR393 was identified as being induced by high nitrate and controls root architecture by inhibiting root growth through targeting transcripts encoding the auxin receptor AFB3 (Vidal et al., 2010Vidal E.A. Araus V. Lu C. Parry G. Green P.J. Coruzzi G.M. Gutierrez R.A. Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana.Proc. Natl Acad. Sci. U S A. 2010; 107: 4477-4482Crossref PubMed Scopus (459) Google Scholar). Nitrate transport is also regulated in response to changes in nitrate concentrations by miRNAs such as miR169. When MIR169a is overexpressed, this leads to a decrease in the expression of AtNRT1.1 and AtNRT2.1 whereas, under low-nitrogen conditions, miR169 is down-regulated (Zhao et al., 2011Zhao M. Ding H. Zhu J.K. Zhang F. Li W.X. Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis.New Phytol. 2011; 190: 906-915Crossref PubMed Scopus (282) Google Scholar). The change in expression of nitrate transporters due to microRNA regulation is an indirect effect of targeting NFYA transcription factors. In corn, a survey of miRNAs also showed that miR169a was down-regulated under N-starvation conditions. In addition, 99 new loci belonging to 47 miRNAs families were also identified. Although predictions are available for targets of some of these miRNAs, further work will be needed to demonstrate their involvement in the regulation of gene expression (Zhao et al., 2012Zhao M. Tai H. Sun S. Zhang F. Xu Y. Li W.X. Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency.PLoS One. 2012; 7: e29669Crossref PubMed Scopus (135) Google Scholar). Micro-RNAs have also been found in phloem sap, as is the case for miR399, and represents one of the first examples of a mobile signal in plants for signaling nutrient status between roots and shoots (Chiou and Lin, 2011Chiou T.J. Lin S.I. Signaling network in sensing phosphate availability in plants.Annu. Rev. Plant Biol. 2011; 62: 185-206Crossref PubMed Scopus (525) Google Scholar). Epigenetic control of response to mineral nutrients has been recently highlighted in a couple of reports on mutants that lack specific responses to nitrogen and phosphorus. In the case of phosphorus deprivation, histone H2AZ, which is a component of the SWR1, a chromatin remodeling complex, is involved in the control of a subset of PSR genes. Under phosphorus-replete conditions, this complex suppresses phosphorus starvation induced gene expression (Smith et al., 2011Smith A.P. Jain A. Deal R.B. Nagarajan V.K. Poling M.D. Raghothama K.G. Meagher R.B. Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator.Plant Physiol. 2011; 152: 217-225Crossref Scopus (135) Google Scholar). The identification of the high nitrogen-insensitive mutant (hni9) led to the association between nitrogen response and a conserved protein that belongs to an RNA polymerase II complex (Widiez et al., 2011Widiez T. El Kafafi el S. Girin T. Berr A. Ruffel S. Krouk G. Vayssières A. Shen W.H. Coruzzi G.M. Gojon A. et al.High nitrogen insensitive 9 (HNI9)-mediated systemic repression of root NO3– uptake is associated with changes in histone methylation.Proc. Natl Acad. Sci. U S A. 2011; 108: 13329-13334Crossref PubMed Scopus (85) Google Scholar). In the hni9-1 mutant, the nitrate transporter NRT2.1 is not repressed by high nitrogen, whereas, in wild-type Arabidopsis, the expression of this transporter is normally repressed by high-nitrogen conditions. The methylation (H3K27me3) of the cis-acting sequences upstream of the TATA-box in NRT2.1 was found to be associated with the repression of NRT2.1 expression under nitrogen-replete conditions due to the presence of HNI9. The involvement of methylation in the control of transporter expression is a novel finding illustrating a new mode for the regulation of plant response to low nutrients. There are few examples of proteins in plants that act as ‘sensors’ of changes in mineral nutrient concentrations. Transceptors have been described in yeast, but, until recently, were not identified in plants (Gojon et al., 2011Gojon A. Krouk G. Perrine-Walker F. Laugier E. Nitrate transceptor(s) in plants.J. Exp. Bot. 2011; 62: 2299-2308Crossref PubMed Scopus (196) Google Scholar). Transceptor is a term that is used to describe membrane-bound transporter proteins that also act as a receptor or sensor. The NRT1.1 transporter is the first identified transceptor in plants involved in sensing nutrient concentrations. The breakthrough in this field was made through in-depth studies of NRT1.1 using the multiple mutant alleles (Gojon et al., 2011Gojon A. Krouk G. Perrine-Walker F. Laugier E. Nitrate transceptor(s) in plants.J. Exp. Bot. 2011; 62: 2299-2308Crossref PubMed Scopus (196) Google Scholar). In addition to the sensing role for NRT1.1 and the induction of downstream genes involved in nitrogen response, this transporter has also been shown to transport auxin. The surprising finding that a nitrate transporter is also permeable to auxin provides a link to the changes that are observed in lateral root development (Krouk et al., 2010bKrouk G. Lacombe B. Bielach A. Perrine-Walker F. Malinska K. Mounier E. Hoyerova K. Tillard P. Leon S. Ljung K. et al.Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants.Dev. Cell. 2010; 18: 927-937Abstract Full Text Full Text PDF PubMed Scopus (706) Google Scholar) under different nitrate concentrations. The evidence-based hypothesis is that, under low-nitrate conditions, NRT1.1 is involved in the repression of lateral roots because it facilitates auxin movement out of lateral root primordial, whereas, at higher-nitrate concentrations, NRT1.1 is involved in the stimulation of lateral root development because the lateral root tips accumulate more auxin. In addition to the role that auxin plays in nitrate responses, hormones such as cytokinin (Ruffel et al., 2011Ruffel S. Krouk G. Ristova D. Shasha D. Birnbaum K.D. Coruzzi G.M. Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand.Proc. Natl Acad. Sci. U S A. 2011; 108: 18524-18529Crossref PubMed Scopus (279) Google Scholar), ethylene (Jung et al., 2009Jung J.Y. Shin R. Schachtman D.P. Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis.Plant Cell. 2009; 21: 607-621Crossref PubMed Scopus (249) Google Scholar), and strigalactone (Kohlen et al., 2011Kohlen W. Charnikhova T. Liu Q. Bours R. Domagalska M.A. Beguerie S. Verstappen F. Leyser O. Bouwmeester H. Ruyter-Spira C. Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis.Plant Physiol. 2011; 155: 974-987Crossref PubMed Scopus (330) Google Scholar) also appear to be important in the regulation and feedback of responses to mineral nutrients. Studies on ammonium transporters also indicate that one member of the AMT family may regulate changes in root architecture independently of changes in ammonium uptake (Lima et al., 2010Lima J.E. Kojima S. Takahashi H. von Wiren N. Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner.Plant Cell. 2010; 22: 3621-3633Crossref PubMed Scopus (247) Google Scholar) and may function as a transceptor. In addition to roles in sensing and regulating nitrogen responses, the AMTs and NRTs are also prominent examples of transporters that are regulated at the posttranslational level in response to changes in nutrient concentrations. For NRT1.1, the dual affinity modes (Ho and Tsay, 2010Ho C.H. Tsay Y.F. Nitrate, ammonium, and potassium sensing and signaling.Curr. Opin. Plant Biol. 2010; 13: 604-610Crossref PubMed Scopus (94) Google Scholar) are regulated by phosphorylation of specific amino acid residues. In addition, the ammonium transporter AMT1.1 is specifically phosphorylated at the T460 residue when ammonium concentrations are altered (Lanquar et al., 2009Lanquar V. Loque D. Hormann F. Yuan L. Bohner A. Engelsberger W.R. Lalonde S. Schulze W.X. von Wiren N. Frommer W.B. Feedback inhibition of ammonium uptake by a phospho-dependent allosteric mechanism in Arabidopsis.Plant Cell. 2009; 21: 3610-3622Crossref PubMed Scopus (142) Google Scholar). Phosphorylation in response to increasing external ammonium concentrations allows Arabidopsis roots to fine tune their uptake of ammonium over a wide range of external concentrations. Protein–protein interactions that regulate many different responses are another emerging theme in nutrient sensing and signaling. Two prominent proteins that appear to be involved in protein–protein interactions include SPX domain-containing (Secco et al., 2012Secco D. Wang C. Arpat B.A. Wang Z. Poirier Y. Tyerman S.D. Wu P. Shou H. Whelan J. The emerging importance of the SPX domain-containing proteins in phosphate homeostasis.New Phytol. 2012; 193: 842-851Crossref PubMed Scopus (199) Google Scholar) and 14–3–3 proteins. SPX domain-containing proteins are present in plant genomes and have been implicated in phosphate homeostasis phosphate transport and response to nitrogen (Secco et al., 2012Secco D. Wang C. Arpat B.A. Wang Z. Poirier Y. Tyerman S.D. Wu P. Shou H. Whelan J. The emerging importance of the SPX domain-containing proteins in phosphate homeostasis.New Phytol. 2012; 193: 842-851Crossref PubMed Scopus (199) Google Scholar). 14–3–3 proteins play many roles in different processes in plant metabolism, particularly as regulators of nitrogen and carbon metabolism (Diaz et al., 2011Diaz C. Kusano M. Sulpice R. Araki M. Redestig H. Saito K. Stitt M. Shin R. Determining novel functions of Arabidopsis 14–3–3 proteins in central metabolic processes.BMC Syst. Biol. 2011; 5: 192Crossref PubMed Scopus (49) Google Scholar). Future studies on the specific roles for SPX-containing and 14–3–3 proteins will provide greater insight into how members of these protein families are involved in the signal transduction networks that allow plants to adapt to changes in internal and external nutrient concentrations. Many new aspects of nutrient sensing and signaling await future discovery. The novel experimental and computational tools that are being developed (Ehrhardt and Frommer, 2012Ehrhardt D.W. Frommer W.B. New technologies for 21st century plant science.Plant Cell. 2012; 24: 374-394Crossref PubMed Scopus (48) Google Scholar) will be vital in the development of strategies to elucidate new aspects of plant nutrient sensing and signaling networks. Systems biology computational approaches provide integrated views of networks and have mainly been applied to understanding responses to added nitrogen (Gutierrez, 2012Gutierrez R.A. Systems biology for enhanced plant nitrogen nutrition.Science. 2012; 336: 1673-1675Crossref PubMed Scopus (144) Google Scholar). Over the past few years, our understanding of how plants sense and signal changes in nutrient concentrations has advanced significantly. The current state of the field of nutrient sensing is exciting and dynamic, with new discoveries on many fronts that have been facilitated by the application of new technologies and powerful genetic tools. Understanding how plants respond to changes in nutrient concentrations will become increasingly important as the basic research findings are translated to increasing the nutrient efficiency of crop plants. Stay tuned for many new findings in the future as scientists worldwide dig further into understanding and unraveling the complex networks that plants use to sense and signal the changes in mineral nutrient concentrations. Thanks to Monsanto Company for providing the author with the time to complete this update. Apologies to colleagues whose work could not be cited due to space constraints. No conflict of interest declared.