Boron deficiency increases expressions of asparagine synthetase, glutamate dehydrogenase and glutamine synthetase genes in tobacco roots irrespective of the nitrogen source

REFERENCES

• Beato VM, Navarro-Gochicoa MT, Rexach J, Herrera-Rodríguez MB, Camacho-Cristóbal JJ, Kempa S, Weckwerth W, González-Fontes A 2011: Expression of root glutamate dehydrogenase genes in tobacco plants subjected to boron deprivation. Plant Physiol. Biochem., 49, 1350–1354.
   PubMed Web of Science ®Google Scholar
• Beato VM, Rexach J, Navarro-Gochicoa MT, Camacho-Cristóbal JJ, Herrera-Rodríguez MB, Maldonado JM, González-Fontes A 2010: A tobacco asparagine synthetase gene responds to carbon and nitrogen status and its root expression is affected under boron stress. Plant Sci., 178, 289–298.
   Web of Science ®Google Scholar
• Blevins DG, Lukaszewski KM 1998: Boron in plant structure and function. Annu. Rev. Plant Physiol. Plant Mol. Biol., 49, 481–500.
   PubMed Web of Science ®Google Scholar
• Bolaños L, Lukaszewski K, Bonilla I, Blevins D 2004: Why boron?. Plant Physiol. Biochem., 42, 907–912.
   PubMed Web of Science ®Google Scholar
• Britto DT, Kronzucker HJ 2002: NH4+ toxicity in higher plants: a critical review. J. Plant Physiol., 159, 567–584.
   Web of Science ®Google Scholar
• Camacho-Cristóbal JJ, Anzelotti D, González-Fontes A 2002: Changes in phenolic metabolism of tobacco plants during short-term boron deficiency. Plant Physiol. Biochem., 40, 997–1002.
   Web of Science ®Google Scholar
• Camacho-Cristóbal JJ, González-Fontes A 1999: Boron deficiency causes a drastic decrease in nitrate content and nitrate reductase activity, and increases the content of carbohydrates in leaves from tobacco plants. Planta, 209, 528–536.
   PubMed Web of Science ®Google Scholar
• Camacho-Cristóbal JJ, González-Fontes A 2007: Boron deficiency decreases plasmalemma H+-ATPase expression and nitrate uptake, and promotes ammonium assimilation into asparagine in tobacco roots. Planta., 226, 443–451.
   PubMed Web of Science ®Google Scholar
• Camacho-Cristóbal JJ, Rexach J, González-Fontes A 2008: Boron in plants: deficiency and toxicity. J. Integr. Plant Biol., 50, 1247–1255.
   PubMed Web of Science ®Google Scholar
• Caputo C, Criado MV, Roberts IN, Gelso MA, Barneix AJ 2009: Regulation of glutamine synthetase 1 and amino acids transport in the phloem of young wheat plants. Plant Physiol. Biochem., 47, 335–342.
   PubMed Web of Science ®Google Scholar
• Chevalier C, Bourgeois E, Just D, Raymond P 1996: Metabolic regulation of asparagine synthetase gene expression in maize (Zea mays L.) root tips. Plant J., 9, 1–11.
   PubMed Web of Science ®Google Scholar
• Dubois F, Brugière N, Sangwan RS, Hirel B 1996: Localization of tobacco cytosolic glutamine synthetase enzymes and the corresponding transcripts shows organ- and cell-specific patterns of protein synthesis and gene expression. Plant Mol. Biol., 31, 803–817.
   PubMed Web of Science ®Google Scholar
• Dubois F, Tercé-Laforgue T, González-Moro MB, Estavillo JM, Sangwan R, Gallais A, Hirel B 2003: Glutamate dehydrogenase in plants: is there a new story for an old enzyme?. Plant Physiol. Biochem., 41, 565–576.
   Web of Science ®Google Scholar
• Feng J, Barker AV 1993: Ethylene evolution and ammonium accumulation by tomato plants under water and salinity stresses. J. Plant Nutr., 15, 2471–2490.
   Web of Science ®Google Scholar
• Ferraro G, Bortolotti S, Mortera P, Schlereth A, Stitt M, Carrari F, Kamenetzky L, Valle EM 2012: Novel glutamate dehydrogenase genes show increased transcript and protein abundances in mature tomato fruits. J. Plant Physiol., 169, 899–907.
   PubMed Web of Science ®Google Scholar
• Fontaine JX, Tercé-Laforgue T, Armengaud P et al. 2012: Characterization of a NADH-dependent glutamate dehydrogenase mutant of Arabidopsis demonstrates the key role of this enzyme in root carbon and nitrogen metabolism. Plant Cell, 24, 4044–4065.
   PubMed Web of Science ®Google Scholar
• Forde BG, Lea PJ 2007: Glutamate in plants: metabolism, regulation, and signalling. J. Exp. Bot., 58, 2339–2358.
   PubMed Web of Science ®Google Scholar
• Garthwaite AJ, von Bothmer R, Colmer TD 2005: Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl- into the shoots. J. Exp. Bot., 56, 2365–2378.
   PubMed Web of Science ®Google Scholar
• Gilbert GA, Gadush MV, Wilson C, Madore MA 1998: Amino acid accumulation in sink and source tissues of Coleus blumei Benth. during salinity stress. J. Exp. Bot., 49, 107–114.
   Web of Science ®Google Scholar
• Herrera-Rodríguez MB, Carrasco-Ballesteros S, Maldonado JM, Pineda M, Aguilar M, Pérez-Vicente R 2002: Three genes showing distinct regulatory patterns encode the asparagine synthetase of sunflower (Helianthus annuus). New Phytol., 155, 33–45.
   PubMed Web of Science ®Google Scholar
• Herrera-Rodríguez MB, González-Fontes A, Rexach J, Camacho-Cristóbal JJ, Maldonado JM, Navarro-Gochicoa MT 2010: Role of boron in vascular plants and response mechanisms to boron stresses. Plant Stress, 4, 115–122.
   Google Scholar
• Herrera-Rodríguez MB, Maldonado JM, Pérez-Vicente R 2004: Light and metabolic regulation of HAS1, HAS1.1 and HAS2, three asparagine synthetase genes in Helianthus annuus. Plant Physiol. Biochem., 42, 511–518.
   PubMed Web of Science ®Google Scholar
• Herrera-Rodríguez MB, Pérez-Vicente R, Maldonado JM 2007: Expression of asparagine synthetase genes in sunflower (Helianthus annuus) under various environmental stresses. Plant Physiol. Biochem., 45, 33–38.
   PubMed Web of Science ®Google Scholar
• Ishiyama K, Inoue E, Watanabe-Takahashi A, Obara M, Yamaya T, Takahashi H 2004: Kinetic properties and ammonium-dependent regulation of cytosolic isoenzymes of glutamine synthetase in Arabidopsis. J. Biol. Chem., 279, 16598–16605.
   PubMed Web of Science ®Google Scholar
• Kastori R, Petrovic N 1989: Effect of boron on nitrate reductase activity in young sunflower plants. J. Plant Nutr., 12, 621–632.
   Web of Science ®Google Scholar
• Kobayashi M, Matoh T, Azuma J 1996: Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol., 110, 1017–1020.
   PubMed Web of Science ®Google Scholar
• Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM 1996: The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 47, 569–593.
   PubMed Web of Science ®Google Scholar
• Lam HM, Peng SSY, Coruzzi GM 1994: Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol., 106, 1347–1357.
   PubMed Web of Science ®Google Scholar
• Lea PJ, Miflin BJ 1974: Alternative route for nitrogen assimilation in higher plants. Nature, 251, 614–616.
   PubMed Web of Science ®Google Scholar
• Lea PJ, Robinson SA, Stewart GR 1990: The enzymology and metabolism of glutamine, glutamate and asparagine. In The Biochemistry of Plants, Eds. Miflin BJ, Lea PJ, vol. 16, pp. 121–159. Academic Press, San Diego, CA.
   Google Scholar
• Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG 2007: Asparagine in plants. Ann. Appl. Biol., 150, 1–26.
   Web of Science ®Google Scholar
• Lehmann T, Skrok A, Dabert M 2010: Stress-induced changes in glutamate dehydrogenase activity imply its role in adaptation to C and N metabolism in lupine embryos. Physiol. Plant., 138, 35–47.
   PubMed Web of Science ®Google Scholar
• Limami AM, Glévarec G, Ricoult C, Cliquet JB, Planchet E 2008: Concerted modulation of alanine and glutamate metabolism in young Medicago truncatula seedling under hypoxic stress. J. Exp. Bot., 59, 2325–2335.
   PubMed Web of Science ®Google Scholar
• Maldonado JM, González-Fontes A, Rexach J 2010: Assimilation of nitrate and sulfate. In Agricultural Sciences: Topics in Modern Agriculture, Ed. González-Fontes A, Gárate A, Bonilla I, pp. 207–232. Studium Press, Houston, TX.
   Google Scholar
• Marschner H 1995: Mineral Nutrition of Higher Plants, 2nd edn, 379–396. Academic Press, San Diego, CA.
   Google Scholar
• Miflin BJ, Habash DZ 2002: The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J. Exp. Bot., 53, 979–987.
   PubMed Web of Science ®Google Scholar
• Miyashita Y, Good AG 2008: NAD(H)-dependent glutamate dehydrogenase is essential for the survival of Arabidopsis thaliana during dark-induced carbon starvation. J. Exp. Bot., 59, 667–680.
   PubMed Web of Science ®Google Scholar
• Nable RO, Bañuelos GS, Paull JG 1997: Boron toxicity. Plant Soil, 193, 181–198.
   Web of Science ®Google Scholar
• Oaks A, Ross DW 1984: Asparagine synthetase in Zea mays. Can. J. Bot., 62, 68–73.
   Google Scholar
• O´Neill MA, Ishii T, Albersheim P, Darvill AG 2004: Rhamnogalacturonan II: Structure and function of borate cross-linked cell wall pectic polysaccharide. Annu. Rev. Plant Biol., 55, 109–139.
   PubMed Web of Science ®Google Scholar
• Purnell MP, Skopelitis DS, Roubelakis-Angelakis KA, Botella JR 2005: Modulation of higher-plant NAD(H)-dependent glutamate dehydrogenase activity in transgenic tobacco via alteration of beta subunit levels. Planta, 222, 167–180.
   PubMed Web of Science ®Google Scholar
• Ramón AM, Carpena Ruíz RO, Gárate A 1989: In vitro stabilization and distribution of nitrate reductase in tomato plants. Incidence of boron deficiency. J. Plant Physiol., 135, 126–128.
   Web of Science ®Google Scholar
• Reid R 2007: Identification of boron transporter genes likely to be responsible for tolerance to boron toxicity in wheat and barley. Plant Cell Physiol., 48, 1673–1678.
   PubMed Web of Science ®Google Scholar
• Restivo FM 2004: Molecular cloning of glutamate dehydrogenase genes of Nicotiana plumbaginifolia: Structure analysis and regulation of their expression by physiological and stress conditions. Plant Sci., 166, 971–982.
   Web of Science ®Google Scholar
• Ruiz JM, Baghour M, Bretones G, Belakbir A, Romero L 1998: Nitrogen metabolism in tobacco plants (Nicotiana tabacum L.): role of boron as a possible regulatory factor. Int. J. Plant Sci., 159, 121–126.
   Web of Science ®Google Scholar
• Sakakibara H, Shimizu H, Hase T, Yamazaki Y, Takao T, Shimonoshi Y, Sugiyama T 1996: Molecular identification and characterization of cytosolic isoforms of glutamine synthetase in maize roots. J. Biol. Chem., 271, 29561–29568.
   PubMed Web of Science ®Google Scholar
• Scheible WR, González-Fontes A, Lauerer M, Müller-Röber B, Caboche M, Stitt M 1997a: Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell, 9, 783–798.
   PubMed Web of Science ®Google Scholar
• Scheible WR, Lauerer M, Schulze ED, Caboche M, Stitt M 1997b: Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J., 11, 671–691.
   Web of Science ®Google Scholar
• Schortemeyer M, Stamp P, Feil B 1997: Ammonium tolerance and carbohydrate status in maize cultivars. Ann. Bot., 79, 25–30.
   Web of Science ®Google Scholar
• Shen ZG, Liang YC, Shen K 1993: Effect of boron on nitrate reductase activity in oilseed rape plants. J. Plant Nutr., 16, 1229–1239.
   Web of Science ®Google Scholar
• Siddiqi MY, Malhotra B, Min XJ, Glass ADM 2002: Effects of ammonium and inorganic carbon enrichment on growth and yield of a hydroponic tomato crop. J. Plant Nutr. Soil Sci., 165, 191–197.
   Web of Science ®Google Scholar
• Sieciechowicz KA, Joy KW, Ireland RJ 1988: The metabolism of asparagine in plants. Phytochemistry, 27, 663–671.
   Web of Science ®Google Scholar
• Sivasankar S, Oaks A 1996: Nitrate assimilation in higher plants: the effect of metabolites and light. Plant Physiol. Biochem., 34, 609–620.
   Web of Science ®Google Scholar
• Stitt M, Lilley RM, Gerhardt R, Heldt HW 1989: Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol., 174, 518–552.
   Web of Science ®Google Scholar
• Teixeira J, Pereira S 2007: High salinity and drought act on an organ-dependent manner on potato glutamine synthetase expression and accumulation. Environ. Exp. Bot., 60, 121–126.
   Web of Science ®Google Scholar
• Todd J, Screen S, Crowley J, Peng J, Andersen S, Brown T, Qi Q, Fabbri B, Duff SMG 2008: Identification and characterization of four distinct asparagine synthetase (AsnS) genes in maize (Zea mays L.). Plant Sci., 175, 799–808.
   Web of Science ®Google Scholar
• Urquhart AA, Joy KW 1981: Use of phloem exudate technique in the study of amino acid transport in pea plants. Plant Physiol., 68, 750–754.
   PubMed Web of Science ®Google Scholar
• Wang H, Liu D, Sun J, Zhang A 2005: Asparagine synthetase gene TaASN1 from wheat is up-regulated by salt stress, osmotic stress and ABA. J. Plant Physiol., 162, 81–89.
   PubMed Web of Science ®Google Scholar
• Winichayakul S, Moyle RL, Coupe SA, Davies KM, Farnden KJF 2004: Analysis of the asparagus (Asparagus officinalis) asparagine synthetase gene promoter identifies evolutionarily conserved cis-regulatory elements that mediate Suc-repression. Funct. Plant Biol., 31, 63–72.
   PubMed Web of Science ®Google Scholar
• Wong HK, Chan HK, Coruzzi GM, Lam HM 2004: Correlation of ASN2 gene expression with ammonium metabolism in Arabidopsis. Plant Physiol., 134, 332–338.
   PubMed Web of Science ®Google Scholar