A framework integrating plant growth with hormones and nutrients.

It is well known that nutrient availability controls plant development. Moreover, plant development is finely tuned by a myriad of hormonal signals. Thus, it is not surprising to see increasing evidence of coordination between nutritional and hormonal signaling. In this opinion article, we discuss how nitrogen signals control the hormonal status of plants and how hormonal signals interplay with nitrogen nutrition. We further expand the discussion to include other nutrient-hormone pairs. We propose that nutrition and growth are linked by a multi-level, feed-forward cycle that regulates plant growth, development and metabolism via dedicated signaling pathways that mediate nutrient and hormonal regulation. We believe this model will provide a useful concept for past and future research in this field.

[1]  B. Forde Local and long-range signaling pathways regulating plant responses to nitrate. , 2002, Annual review of plant biology.

[2]  F. Daniel-Vedele,et al.  The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[3]  G. S. Avery,,et al.  AUXIN AND NITROGEN RELATIONSHIPS IN GREEN PLANTS , 1945 .

[4]  T. Kiba,et al.  Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. , 2011, Journal of experimental botany.

[5]  Pei Sun,et al.  Ethylene is involved in nitrate-dependent root growth and branching in Arabidopsis thaliana. , 2009, The New phytologist.

[6]  C. Vuylsteker,et al.  Nitrate reductase activity in chicory roots following excision , 1997 .

[7]  G. Krouk,et al.  Nitrate signaling: adaptation to fluctuating environments. , 2010, Current opinion in plant biology.

[8]  Gloria Coruzzi,et al.  Genomic Analysis of the Nitrate Response Using a Nitrate Reductase-Null Mutant of Arabidopsis1[w] , 2004, Plant Physiology.

[9]  R. Borges Do plants and animals differ in phenotypic plasticity? , 2005, Journal of Biosciences.

[10]  Javier Paz-Ares,et al.  Plant hormones and nutrient signaling , 2009, Plant Molecular Biology.

[11]  S. Mangan,et al.  Structure and function of the feed-forward loop network motif , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  D. Schachtman,et al.  Nutrient sensing and signaling: NPKS. , 2007, Annual review of plant biology.

[13]  U. Schurr,et al.  Environmental effects on spatial and temporal patterns of leaf and root growth. , 2009, Annual review of plant biology.

[14]  M. Leydecker,et al.  Cytokinin affects nitrate reductase expression through the modulation of polyadenylation of the nitrate reductase mRNA transcript , 1993 .

[15]  C. Vuylsteker,et al.  Influence of BAP and NAA on the expression of nitrate reductase in excised chicory roots , 1997 .

[16]  Uri Alon,et al.  ■ The Feed-Forward Loop Network Motif , 2006 .

[17]  Francesca Chiaromonte,et al.  Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis , 2007, Genome Biology.

[18]  Rainer Breitling,et al.  The Potassium-Dependent Transcriptome of Arabidopsis Reveals a Prominent Role of Jasmonic Acid in Nutrient Signaling1[w] , 2004, Plant Physiology.

[19]  C. Chen,et al.  Transcriptional regulation of nitrate reductase mRNA levels by cytokinin-abscisic Acid interactions in etiolated barley leaves. , 1992, Plant physiology.

[20]  M. Estelle,et al.  The F-box protein TIR1 is an auxin receptor , 2005, Nature.

[21]  G. Neumann,et al.  Root-derived cytokinins as long-distance signals for NO3--induced stimulation of leaf growth. , 2005, Journal of experimental botany.

[22]  J. Malamy,et al.  Intrinsic and environmental response pathways that regulate root system architecture. , 2005, Plant, cell & environment.

[23]  H. Marschner Mineral Nutrition of Higher Plants , 1988 .

[24]  Fusuo Zhang,et al.  Auxin transport in maize roots in response to localized nitrate supply. , 2010, Annals of botany.

[25]  Rodrigo A Gutiérrez,et al.  A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. , 2008, Current opinion in plant biology.

[26]  G. Coruzzi,et al.  Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana , 2010, Proceedings of the National Academy of Sciences.

[27]  Vívian Tamaki,et al.  Cytokinins and auxin communicate nitrogen availability as long-distance signal molecules in pineapple (Ananas comosus). , 2007, Journal of plant physiology.

[28]  Gabriel Krouk,et al.  A system biology approach highlights a hormonal enhancer effect on regulation of genes in a nitrate responsive "biomodule" , 2009, BMC Systems Biology.

[29]  L. Dolan,et al.  Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. , 2004, The Plant journal : for cell and molecular biology.

[30]  Gabriel Krouk,et al.  Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. , 2010, Developmental cell.

[31]  Akiko Maruyama-Nakashita,et al.  A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. , 2004, The Plant journal : for cell and molecular biology.

[32]  G. S. Avery,,et al.  NUTRIENT DEFICIENCIES AND GROWTH HORMONE CONCENTRATION IN HELIANTHUS AND NICOTIANA , 1937 .

[33]  G. Neumann,et al.  Rapid effects of nitrogen form on leaf morphogenesis in tobacco. , 2000, Journal of experimental botany.

[34]  C. Curie,et al.  Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth-dependent pathway. , 2008, The Plant journal : for cell and molecular biology.

[35]  B. Touraine,et al.  N Demand and the Regulation of Nitrate Uptake , 1994, Plant physiology.

[36]  N. Crawford,et al.  Nitrate: nutrient and signal for plant growth. , 1995, The Plant cell.

[37]  P W Barlow,et al.  Dual pathways for regulation of root branching by nitrate. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Y. Tsay,et al.  CHL1 Functions as a Nitrate Sensor in Plants , 2009, Cell.

[39]  N. Crawford,et al.  The herbicide sensitivity gene CHL1 of arabidopsis encodes a nitrate-inducible nitrate transporter , 1993, Cell.

[40]  G. Coruzzi,et al.  Cell-specific nitrogen responses mediate developmental plasticity , 2008, Proceedings of the National Academy of Sciences.

[41]  Hitoshi Sakakibara,et al.  Interactions between nitrogen and cytokinin in the regulation of metabolism and development. , 2006, Trends in plant science.

[42]  Fusuo Zhang,et al.  Auxin transport from shoot to root is involved in the response of lateral root growth to localized supply of nitrate in maize , 2005 .

[43]  Bertrand Muller,et al.  A Role for Auxin Redistribution in the Responses of the Root System Architecture to Phosphate Starvation in Arabidopsis1 , 2005, Plant Physiology.

[44]  Brian G Forde,et al.  Nitrogen regulation of root branching. , 2006, Annals of botany.

[45]  P. Gresshoff,et al.  Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type , 2000, Planta.

[46]  W. G. Brenner,et al.  Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. , 2005, The Plant journal : for cell and molecular biology.

[47]  V. Rubio,et al.  Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[48]  Javier Paz-Ares,et al.  Interaction between Phosphate-Starvation, Sugar, and Cytokinin Signaling in Arabidopsis and the Roles of Cytokinin Receptors CRE1/AHK4 and AHK31 , 2005, Plant Physiology.

[49]  C. Foyer,et al.  ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[50]  O. Leyser,et al.  Strigolactones Are Transported through the Xylem and Play a Key Role in Shoot Architectural Response to Phosphate Deficiency in Nonarbuscular Mycorrhizal Host Arabidopsis1[C][W][OA] , 2010, Plant Physiology.

[51]  Rongchen Wang,et al.  The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is regulated by auxin in both shoots and roots. , 2002, Journal of experimental botany.

[52]  W. Cao,et al.  Involvement of endogenous plant hormones in the effect of mixed nitrogen source on growth and tillering of wheat , 1998 .

[53]  P. Tillard,et al.  The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches , 2006, Proceedings of the National Academy of Sciences.

[54]  A. Gojon,et al.  Root uptake regulation: a central process for NPS homeostasis in plants. , 2009, Current opinion in plant biology.

[55]  T. Kuromori,et al.  AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. , 2004, Plant & cell physiology.

[56]  J. Ecker,et al.  Functional Genomic Analysis of the AUXIN/INDOLE-3-ACETIC ACID Gene Family Members in Arabidopsis thaliana[W] , 2005, The Plant Cell Online.

[57]  Y. Kamiya,et al.  Inhibition of shoot branching by new terpenoid plant hormones , 2008, Nature.

[58]  Charlie Chang,et al.  Functional Genomic Analysis of the AUXIN RESPONSE FACTOR Gene Family Members in Arabidopsis thaliana: Unique and Overlapping Functions of ARF7 and ARF19w⃞ , 2005, The Plant Cell Online.

[59]  Elliot M Meyerowitz,et al.  Plants Compared to Animals: The Broadest Comparative Study of Development , 2002, Science.

[60]  S. Filleur,et al.  Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana , 2005, Planta.