Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition.

A subtractive tomato (Lycopersicon esculentum) root cDNA library enriched in genes up-regulated by changes in plant mineral status was screened with labeled mRNA from roots of both nitrate-induced and mineral nutrient-deficient (-nitrogen [N], -phosphorus, -potassium [K], -sulfur, -magnesium, -calcium, -iron, -zinc, and -copper) tomato plants. A subset of cDNAs was selected from this library based on mineral nutrient-related changes in expression. Additional cDNAs were selected from a second mineral-deficient tomato root library based on sequence homology to known genes. These selection processes yielded a set of 1,280 mineral nutrition-related cDNAs that were arrayed on nylon membranes for further analysis. These high-density arrays were hybridized with mRNA from tomato plants exposed to nitrate at different time points after N was withheld for 48 h, for plants that were grown on nitrate/ammonium for 5 weeks prior to the withholding of N. One hundred-fifteen genes were found to be up-regulated by nitrate resupply. Among these genes were several previously identified as nitrate responsive, including nitrate transporters, nitrate and nitrite reductase, and metabolic enzymes such as transaldolase, transketolase, malate dehydrogenase, asparagine synthetase, and histidine decarboxylase. We also identified 14 novel nitrate-inducible genes, including: (a) water channels, (b) root phosphate and K(+) transporters, (c) genes potentially involved in transcriptional regulation, (d) stress response genes, and (e) ribosomal protein genes. In addition, both families of nitrate transporters were also found to be inducible by phosphate, K, and iron deficiencies. The identification of these novel nitrate-inducible genes is providing avenues of research that will yield new insights into the molecular basis of plant N nutrition, as well as possible networking between the regulation of N, phosphorus, and K nutrition.

[1]  Chung,et al.  The 14-3-3 proteins: cellular regulators of plant metabolism. , 1999, Trends in plant science.

[2]  J. Pate,et al.  Effects of P deficiency on assimilation and transport of nitrate and phosphate in intact plants of castor bean (Ricinus communis L.) , 1997 .

[3]  S. Kay,et al.  Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. , 2000, Science.

[4]  F. Daniel-Vedele,et al.  Nitrate transport: a key step in nitrate assimilation. , 1998, Current opinion in plant biology.

[5]  B. Forde,et al.  Nitrate transporters in plants: structure, function and regulation. , 2000, Biochimica et biophysica acta.

[6]  R. E. Hirsch,et al.  Improving nutrient capture from soil by the genetic manipulation of crop plants , 1999, Trends in biotechnology.

[7]  C. Maurel.  AQUAPORINS AND WATER PERMEABILITY OF PLANT MEMBRANES. , 1997, Annual review of plant physiology and plant molecular biology.

[8]  T. Ohyama,et al.  Deficiency of N, P, K, Ca, Mg, or Fe Mineral Nutrients in Narcissus cv. “Garden Giant” , 1996 .

[9]  W. Frommer,et al.  Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[11]  B. Forde,et al.  An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. , 1998, Science.

[12]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[13]  P. Waggoner,et al.  Nitrogen fertilizer: retrospect and prospect. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[14]  G. Hagen,et al.  ARF1, a transcription factor that binds to auxin response elements. , 1997, Science.

[15]  R. Hedrich,et al.  KDC1, a Novel Carrot Root Hair K+Channel , 2000, The Journal of Biological Chemistry.

[16]  J. Mun,et al.  Characterization of cDNAs encoding cytoplasmic ribosomal protein L15 and L27a in petunia (Petunia hybrida): primary structures and coordinate expression. , 1999, Gene.

[17]  N. Crawford,et al.  Molecular and physiological aspects of nitrate uptake in plants , 1998 .

[18]  W. Frommer,et al.  Differential regulation of three functional ammonium transporter genes by nitrogen in root hairs and by light in leaves of tomato. , 2000, The Plant journal : for cell and molecular biology.

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

[20]  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.

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

[22]  New Regulatory Steps in Nitrate Assimilation of Lower and Higher Plants , 1990 .

[23]  C. Larsson,et al.  The role of aquaporins in cellular and whole plant water balance. , 2000, Biochimica et biophysica acta.

[24]  Wang,et al.  Rapid Up-regulation of HKT1, a high-affinity potassium transporter gene, in roots of barley and wheat following withdrawal of potassium , 1998, Plant physiology.

[25]  K. Raghothama,et al.  Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. , 1998, Plant physiology.

[26]  W. Pettigrew,et al.  Dry matter production, nutrient uptake, and growth of cotton as affected by potassium fertilization , 1997 .

[27]  W. Wei,et al.  hrp gene-dependent induction of hin1: a plant gene activated rapidly by both harpins and the avrPto gene-mediated signal. , 1996, The Plant journal : for cell and molecular biology.

[28]  J. Vidmar,et al.  Isolation and characterization of HvNRT2.3 and HvNRT2.4, cDNAs encoding high-affinity nitrate transporters from roots of barley. , 2000, Plant physiology.

[29]  W. H. Mager,et al.  Control of ribosomal protein gene expression. , 1988, Biochimica et biophysica acta.

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

[31]  W. Frommer,et al.  Regulation of mineral nitrogen uptake in plants , 1997 .

[32]  F. Katagiri,et al.  Two tobacco DNA-binding proteins with homology to the nuclear factor CREB , 1989, Nature.