Elongation Changes of Exploratory and Root Hair Systems Induced by Aminocyclopropane Carboxylic Acid and Aminoethoxyvinylglycine Affect Nitrate Uptake and BnNrt2.1 and BnNrt1.1 Transporter Gene Expression in Oilseed Rape[W]

Ethylene is a plant hormone that plays a major role in the elongation of both exploratory and root hair systems. Here, we demonstrate in Brassica napus seedlings that treatments with the ethylene precursor, aminocyclopropane carboxylic acid (ACC) and the ethylene biosynthesis inhibitor, aminoethoxyvinylglycine (AVG), cause modification of the dynamic processes of primary root and root hair elongation in a dose-dependent way. Moreover, restoration of root elongation in AVG-treated seedlings by 1 mm l-glutamate suggested that high concentrations of AVG affect root elongation through nonoverlapping ethylene metabolic pathway involving pyridoxal 5′-P-dependent enzymes of nitrate (N) metabolism. In this respect, treatments with high concentrations of ACC and AVG (10 μm) over 5 d revealed significant differences in relationships between root growth architecture and N uptake capacities. Indeed, if these treatments decreased severely the elongation of the exploratory root system (primary root and lateral roots) they had opposing effects on the root hair system. Although ACC increased the length and number of root hairs, the rate of N uptake and the transcript level of the N transporter BnNrt2.1 were markedly reduced. In contrast, the decrease in root hair length and number in AVG-treated seedlings was overcompensated by an increase of N uptake and BnNrt2.1 gene expression. These root architectural changes demonstrated that BnNrt2.1 expression levels were more correlated to the changes of the exploratory root system than the changes of the root hair system. The difference between treatments in N transporters BnNrt1.1 and BnNrt2.1 gene expression is discussed with regard to presumed transport functions of BnNrt1.1 in relation to root elongation.

[1]  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.

[2]  L. Dolan,et al.  Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. , 1995, The Plant journal : for cell and molecular biology.

[3]  A. Liepman,et al.  Genomic Analysis of Aminotransferases in Arabidopsis thaliana , 2004 .

[4]  J. Manning,et al.  Inactivation of pyridoxal phosphate enzymes by gabaculine. Correlation with enzymic exchange of beta-protons. , 1982, The Journal of biological chemistry.

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

[6]  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.

[7]  R. Pierik,et al.  The Janus face of ethylene: growth inhibition and stimulation. , 2006, Trends in plant science.

[8]  B. Touraine,et al.  Nitrate Uptake and Its Regulation , 2001 .

[9]  D. Inzé,et al.  Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Schiefelbein,et al.  Constructing a plant cell. The genetic control of root hair development. , 2000, Plant physiology.

[11]  L. Hobbie Auxin: Molecular genetic approaches in Arabidopsis , 1998 .

[12]  Y. Tsay,et al.  Nitrate transporters and peptide transporters , 2007, FEBS letters.

[13]  A. Trubuil,et al.  Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family , 2005, Theoretical and Applied Genetics.

[14]  R. J. Pitts,et al.  Auxin and ethylene promote root hair elongation in Arabidopsis. , 1998, The Plant journal : for cell and molecular biology.

[15]  Y. Inoue,et al.  Ethylene promotes the induction by auxin of the cortical microtubule randomization required for low-pH-induced root hair initiation in lettuce (Lactuca sativa L.) seedlings. , 2003, Plant & cell physiology.

[16]  F. Berger,et al.  Control of cell division in the root epidermis of Arabidopsis thaliana. , 1998, Developmental biology.

[17]  A. Ourry,et al.  Putative role of γ ‐aminobutyric acid (GABA) as a long‐distance signal in up‐regulation of nitrate uptake in Brassica napus L. , 2004 .

[18]  C. Laloi,et al.  PDX1 is essential for vitamin B6 biosynthesis, development and stress tolerance in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[19]  S. Yang,et al.  Inactivation of 1-Aminocyclopropane-1-Carboxylate Synthase by l-Vinylglycine as Related to the Mechanism-Based Inactivation of the Enzyme by S-Adenosyl-l-Methionine. , 1989, Plant physiology.

[20]  D. Pilbeam,et al.  Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. , 2007, Journal of experimental botany.

[21]  B. Forde,et al.  Glutamate in plants: metabolism, regulation, and signalling. , 2007, Journal of experimental botany.

[22]  H. Klee,et al.  Root formation in ethylene-insensitive plants. , 1999, Plant physiology.

[23]  Y. Esashi,et al.  Effects of α‐aminoisobutyric acid and D‐ and L‐amino acids on ethylene production and content of 1‐aminocyclopropane‐1‐carboxylic acid in cotyledonary segments of cocklebur seeds , 1982 .

[24]  T. Baskin,et al.  Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. , 2003, Plant & cell physiology.

[25]  Rongchen Wang,et al.  The Arabidopsis Dual-Affinity Nitrate Transporter Gene AtNRT1.1 (CHL1) Is Activated and Functions in Nascent Organ Development during Vegetative and Reproductive Growth , 2001, The Plant Cell Online.

[26]  J. Murray,et al.  Triggering the cell cycle in plants. , 2000, Trends in cell biology.

[27]  P. Tillard,et al.  A Central Role for the Nitrate Transporter NRT2.1 in the Integrated Morphological and Physiological Responses of the Root System to Nitrogen Limitation in Arabidopsis1 , 2006, Plant Physiology.

[28]  G. Engler,et al.  The Arabidopsis 1-Aminocyclopropane-1-Carboxylate Synthase Gene 1 Is Expressed during Early Development. , 1993, The Plant cell.

[29]  L. Herrera-Estrella,et al.  The role of nutrient availability in regulating root architecture. , 2003, Current opinion in plant biology.

[30]  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.

[31]  D. Straeten,et al.  Ethylene and vegetative development , 1997 .

[32]  D. Straeten,et al.  In the early response of Arabidopsis roots to ethylene, cell elongation is up- and down-regulated and uncoupled from differentiation. , 2001, Plant physiology.

[33]  Jian-Kang Zhu,et al.  SOS4, A Pyridoxal Kinase Gene, Is Required for Root Hair Development in Arabidopsis1 , 2002, Plant Physiology.

[34]  P. Morris,et al.  Contrasting effects of ethylene perception and biosynthesis inhibitors on germination and seedling growth of barley (Hordeum vulgare L.). , 2000, Journal of experimental botany.

[35]  O. Jones,et al.  Haem synthesis during cytochrome P-450 induction in higher plants. 5-Aminolaevulinic acid synthesis through a five-carbon pathway in Helianthus tuberosus tuber tissues aged in the dark. , 1988, The Biochemical journal.

[36]  H. Vogel,et al.  Nitrogen-15 NMR studies of nitrogen metabolism in Picea glauca buds. , 2004, Plant physiology and biochemistry : PPB.

[37]  B. Keller,et al.  The Arabidopsis root hair mutants der2-der9 are affected at different stages of root hair development. , 2005, Plant & cell physiology.

[38]  Rishikesh Bhalerao,et al.  Ethylene Upregulates Auxin Biosynthesis in Arabidopsis Seedlings to Enhance Inhibition of Root Cell Elongation[W] , 2007, The Plant Cell Online.

[39]  R. Leegood Faculty Opinions recommendation of Molecular and physiological analysis of Arabidopsis mutants defective in cytosolic or chloroplastic aspartate aminotransferase. , 2002 .

[40]  F. Daniel-Vedele,et al.  Molecular and functional regulation of two NO3- uptake systems by N- and C-status of Arabidopsis plants. , 1999, The Plant journal : for cell and molecular biology.

[41]  K. Ljung,et al.  Ethylene Regulates Root Growth through Effects on Auxin Biosynthesis and Transport-Dependent Auxin Distribution[W] , 2007, The Plant Cell Online.

[42]  F. Daniel-Vedele,et al.  The Arabidopsis nitrate transporter AtNRT2.1 is targeted to the root plasma membrane. , 2007, Plant physiology and biochemistry : PPB.

[43]  D. Inzé,et al.  The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 Gene Defines a Glutathione-Dependent Pathway Involved in Initiation and Maintenance of Cell Division during Postembryonic Root Development , 2000, Plant Cell.

[44]  L. Xiong,et al.  Pyridoxine is required for post-embryonic root development and tolerance to osmotic and oxidative stresses. , 2005, The Plant journal : for cell and molecular biology.

[45]  J. Hancock,et al.  Nitric oxide signalling in plants. , 2003, The New phytologist.

[46]  J. Schiefelbein,et al.  The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process , 1994, Plant physiology.

[47]  L. Dolan,et al.  Building a hair: tip growth in Arabidopsis thaliana root hairs. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[48]  W. Frommer,et al.  Analysis of the Arabidopsis rsr4-1/pdx1-3 Mutant Reveals the Critical Function of the PDX1 Protein Family in Metabolism, Development, and Vitamin B6 Biosynthesis[W] , 2006, The Plant Cell Online.

[49]  M. Tester,et al.  Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. , 2006, Plant & cell physiology.

[50]  Stuart A. Casson,et al.  Genes and signalling in root development , 2003 .

[51]  J. Schiefelbein,et al.  Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. , 1996, The Plant cell.

[52]  Broome,et al.  Literature cited , 1924, A Guide to the Carnivores of Central America.

[53]  D. Straeten,et al.  Position and cell type‐dependent microtubule reorientation characterizes the early response of the Arabidopsis root epidermis to ethylene , 2004 .

[54]  Pascal Gantet,et al.  Transcription Factor Networks. Pathways to the Knowledge of Root Development , 2004, Plant Physiology.

[55]  B. Ney,et al.  Modeling Nitrogen Uptake in Oilseed Rape cv Capitol during a Growth Cycle Using Influx Kinetics of Root Nitrate Transport Systems and Field Experimental Data , 2004, Plant Physiology.

[56]  E. Spalding,et al.  Calcium Entry Mediated by GLR3.3, an Arabidopsis Glutamate Receptor with a Broad Agonist Profile1[W][OA] , 2006, Plant Physiology.

[57]  Keith Lindsey,et al.  The POLARIS Peptide of Arabidopsis Regulates Auxin Transport and Root Growth via Effects on Ethylene Signaling[OA] , 2006, The Plant Cell Online.

[58]  Filip Vandenbussche,et al.  Circadian Rhythms of Ethylene Emission in Arabidopsis1[w] , 2004, Plant Physiology.

[59]  G. Sandberg,et al.  Dissecting Arabidopsis lateral root development. , 2003, Trends in plant science.

[60]  P. Benfey,et al.  Down and out in Arabidopsis: the formation of lateral roots , 1997 .

[61]  W. Frommer,et al.  Arabidopsis LHT1 Is a High-Affinity Transporter for Cellular Amino Acid Uptake in Both Root Epidermis and Leaf Mesophyll[W] , 2006, The Plant Cell Online.

[62]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[63]  K. Roberts,et al.  Ethylene-induced microtubule reorientations: mediation by helical arrays , 1985, Planta.

[64]  X. Deng,et al.  A Rice Glutamate Receptor–Like Gene Is Critical for the Division and Survival of Individual Cells in the Root Apical Meristem[W] , 2005, The Plant Cell Online.

[65]  R. Rando Irreversible inhibition of aspartate aminotransferase by 2-amino-3-butenoic acid. , 1974, Biochemistry.

[66]  A. Ourry,et al.  Putative role of g-aminobutyric acid ( GABA ) as a long-distance signal in up-regulation of nitrate uptake in Brassica napus , 2004 .

[67]  G. Viennois,et al.  Regulation of Root Nitrate Uptake at the NRT2.1 Protein Level in Arabidopsis thaliana* , 2007, Journal of Biological Chemistry.