Root-derived cytokinins as long-distance signals for NO3--induced stimulation of leaf growth.

Leaf growth of many plant species shows rapid changes in response to alterations of the form and the level of N supply. In hydroponically-grown tomato (Lycopersicon esculentum L.), leaf growth was rapidly stimulated by NO(3)(-) application to NH(4)(+) precultured plants, while NH(4)(+) supply or complete N deprivation to NO(3)(-) precultured plants resulted in a rapid inhibition of leaf growth. Just 10 microM NO(3)(-) supply was sufficient to stimulate leaf growth to the same extent as 2 mM. Furthermore, continuous NO(3)(-) supply induced an oscillation of leaf growth rate with a 48 h interval. Since changes in NO(3)(-) levels in the xylem exudate and leaves did not correlate with NO(3)(-)-induced alterations of leaf growth rate, additional signals such as phytohormones may be involved. Levels of a known inhibitor of leaf growth, abscisic acid (ABA), did not consistently correspond to leaf growth rates in wild-type plants. Moreover, leaf growth of the ABA-deficient tomato mutant flacca was inhibited by NH(4)(+) without an increase in ABA concentration and was stimulated by NO(3)(-) despite its excessive ethylene production. These findings suggest that neither ABA nor ethylene are directly involved in the effects of N form on leaf growth. However, under all experimental conditions, stimulation of leaf growth by NO(3)(-) was consistently associated with increased concentration of the physiologically active forms of cytokinins, zeatin and zeatin riboside, in the xylem exudate. This indicates a major role for cytokinins as long-distance signals mediating the shoot response to NO(3)(-) perception in roots.

[1]  Anders Nordström,et al.  Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[2]  T. Mizuno,et al.  The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. , 2001, Plant & cell physiology.

[3]  S. Lips,et al.  Transport and accumulation rates of abscisic acid and aldehyde oxidase activity in Pisum sativum L. in response to suboptimal growth conditions. , 2001, Journal of experimental botany.

[4]  D. Crowell,et al.  Expression and Processing of a Hormonally Regulated β-Expansin from Soybean , 2001 .

[5]  Kazuo Shinozaki,et al.  Identification of CRE1 as a cytokinin receptor from Arabidopsis , 2001, Nature.

[6]  G. Farquhar,et al.  Effects of elevated [CO(2)] and nitrogen nutrition on cytokinins in the xylem sap and leaves of cotton. , 2000, Plant physiology.

[7]  R. E. Sharp,et al.  Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene. , 2000, Journal of experimental botany.

[8]  Rongchen Wang,et al.  Genomic Analysis of a Nutrient Response in Arabidopsis Reveals Diverse Expression Patterns and Novel Metabolic and Potential Regulatory Genes Induced by Nitrate , 2000, Plant Cell.

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

[10]  M. Stitt,et al.  Nitrate regulation of metabolism and growth. , 1999, Current opinion in plant biology.

[11]  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.

[12]  T. Mizuno,et al.  Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate , 1998, FEBS letters.

[13]  H. Sakakibara,et al.  A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize. , 1998, The Plant journal : for cell and molecular biology.

[14]  R. Vaňková,et al.  Regulation of cytokinin content in plant cells , 1997 .

[15]  Mark Stitt,et al.  Accumulation of nitrate in the shoot acts as a signal to regulate shoot‐root allocation in tobacco† , 1997 .

[16]  E. Beck.  Regulation of shoot/root ratio by cytokinins from roots inUrtica dioica: Opinion , 1996, Plant and Soil.

[17]  W. Davies,et al.  Control of leaf expansion in sunflower (Helianthus annuus L.) by nitrogen nutrition. , 1996 .

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

[19]  C.-J. Li,et al.  Effect of apex excision and replacement by 1-naphthylacetic acid on cytokinin concentration and apical dominance in pea plants , 1995 .

[20]  F. Bangerth.  Response of cytokinin concentration in the xylem exudate of bean (Phaseolus vulgaris L.) plants to decapitation and auxin treatment, and relationship to apical dominance , 1994, Planta.

[21]  W. Hartung,et al.  The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. III. Long-distance transport of abscisic acid depending on nitrogen nutrition and salt stress , 1994 .

[22]  R. Travis,et al.  Comparative Induction of Nitrate and Nitrite Uptake and Reduction Systems by Ambient Nitrate and Nitrite in Intact Roots of Barley (Hordeum vulgare L.) Seedlings , 1993, Plant physiology.

[23]  E. Beck,et al.  Cytokinins in the perennial herb Urtica dioica L. as influenced by its nitrogen status , 1993, Planta.

[24]  M. Redinbaugh,et al.  Glutamine Synthetase and Ferredoxin-Dependent Glutamate Synthase Expression in the Maize (Zea mays) Root Primary Response to Nitrate (Evidence for an Organ-Specific Response) , 1993, Plant physiology.

[25]  T. Nielsen,et al.  Cytokinins and leaf development in sweet pepper (Capsicum annuum L.) , 1992, Planta.

[26]  J. M. Robertson,et al.  Developmental Responses to Drought and Abscisic Acid in Sunflower Roots 2. MITOTIC ACTIVITY , 1990 .

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

[28]  D. Kuiper.  Growth Responses of Plantago major L. ssp. pleiosperma (Pilger) to Changes in Mineral Supply : Evidence for Regulation by Cytokinins. , 1988, Plant physiology.

[29]  J. Bohner,et al.  Cell number, cell size and hormone levels in semi‐isogenic mutants of Lycopersicon pimpinellifolium differing in fruit size , 1988 .

[30]  M. Staal,et al.  THE EFFECTS OF EXOGENOUSLY APPLIED PLANT-GROWTH SUBSTANCES ON THE PHYSIOLOGICAL PLASTICITY IN PLANTAGO-MAJOR SSP PLEIOSPERMA - RESPONSES OF GROWTH, SHOOT TO ROOT RATIO AND RESPIRATION , 1987 .

[31]  W. Davies,et al.  Root and Shoot Growth of Plants Treated with Abscisic Acid , 1981 .

[32]  M. Tal.  Abnormal Stomatal Behavior and Hormonal Imbalance in flacca, a Wilty Mutant of Tomato: V. Effect of Abscisic Acid on Indoleacetic Acid Metabolism and Ethylene Evolution. , 1979, Plant physiology.

[33]  H. Marschner,et al.  Nitrogen Nutrition and Cytokinin Activity in Solanum tuberosum , 1978 .

[34]  D. Imber,et al.  Abnormal Stomatal Behaviour and Hormonal Imbalance in flacca, a Wilty Mutant of Tomato EFFECT OF ABSCISIC ACID AND AUXIN ON STOMATAL BEHAVIOUR AND PEROXIDASE ACTIVITY , 1974 .

[35]  H. Stubbe.  Mutanten der KulturtomateLycopersicon esculentum Miller VI , 1972, Die Kulturpflanze.

[36]  H. Stubbe.  Mutanten der KulturtomateLycopersicon esculentum Miller I , 2005, Die Kulturpflanze.

[37]  D. Sorrell,et al.  The interface between the cell cycle and plant growth regulators: a mini review , 2004, Plant Growth Regulation.

[38]  G. Neumann,et al.  Effects of long-term and short-term supply of NO3- or NH4+ on Cytokinin levels and leaf expansion rate in tomato (Lycopersicon esculentum L. cv. Moneymaker). , 2001 .

[39]  W. Horst.  Plant nutrition : food security and sustainability of agro-ecosystems through basic and applied research , 2001 .

[40]  D. Clarkson,et al.  Nitrate and ammonium nutrition of plants: physiological and molecular perspectives , 1999 .

[41]  W. Hartung.  Abscisic Acid—A Hormonal Long-Distance Stress Signal in Plants Under Drought and Salt Stress , 1999 .

[42]  J. Bryant,et al.  Plant cell proliferation and its regulation in growth and development , 1998 .

[43]  J. Murray,et al.  A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. , 1995, The Plant cell.

[44]  I. Bertling,et al.  Changes in hormonal pattern of the new growth of Sclerocarya birrea after rejuvenation treatment with GA3 and "heading back". , 1995 .

[45]  C. Larsson,et al.  Nitrate regulation of zeation riboside levels in barley roots: effects of inhibitors of N assimilation and comparison with ammonium , 1993 .

[46]  T. Nielsen,et al.  I. Spatial distribution of endogenous cytokinins in relation to leaf growth , 1992 .

[47]  Lesley L. Beuning,et al.  Cytokinins and the division or expansion of plant cells. , 1988 .