Biologia plantarum 61:675-684, 2017 | DOI: 10.1007/s10535-017-0722-y
Sulphur deficiency inhibits nitrogen assimilation and recycling in barley plants
- 1 Instituto de Investigaciones en Biociencias Agrícolas y Ambientales (INBA), CONICET - Universidad de Buenos Aires, Buenos Aires, Argentina
Sulphur (S) is incorporated into diverse primary and secondary metabolites that play important roles in proper growth and development of plants. In cereals, a fraction of the nitrogen (N) accumulated in developing grains is guaranteed by amino acid remobilization from vegetative tissues, a contribution that becomes critical when soil nutrients are deficient. Glutamine synthetase (GS) and amino acid transporters (AAT) are key components involved in N assimilation and recycling. The aim of the present study was to evaluate the effect of S availability on the expressions of HvGS and several selected HvAAT genes in barley plants and on the phloem exudation rate of amino acids. To this end, two independent experiments were designed to impose low S availability conditions to barley plants. Low S availability caused a decrease in the phloem exudation rate of amino acids as well as in the gene expression of all the HvGS genes and five of the six HvAAT genes analyzed. The strong correlation found between the phloem amino acid exudation rate and HvGS1-1, HvGS1-2, HvAAP7, and HvProT1 gene expression may indicate the participation of these genes in the regulation of amino acid remobilization through the phloem.
Keywords: amino acid transporters; glutamine synthetase; Hordeum vulgare; phloem amino acid exudation
Subjects: sulfur; nitrogen metabolism; amino acid transporters; glutamine synthetase; exudation; amino acids; nitrate; proteins; gene expression; barley
Received: July 14, 2016; Revised: November 16, 2016; Accepted: December 14, 2016; Published: December 1, 2017 Show citation
Supplementary files
| Download file | bpl-201704-0009_S1.pdf File size: 87.73 kB |
References
- Abdallah, M., Etienne, P., Ourry, A., Meuriot, F.: Do initial S reserves and mineral S availability alter leaf S-N mobilization and leaf senescence in oilseed rape? - Plant Sci. 180: 511-520, 2011.
Go to original source... - Avila-Ospina, L., Marmagne, A., Talbotec, J., Krupinska, K., Masclaux-Daubresse, C.: The identification of new cytosolic glutamine synthetase and asparagine synthetase genes in barley (Hordeum vulgare L.) and their expression during leaf senescence. - J. exp. Bot. 66: 213-226, 2015.
Go to original source... - Bazargani, M.M., Hajirezaei, M.-R., Salekdeh, G.H., Bushehri, A-A.S., Falahati-Anbaran, M., Moradi, F., Naghavi, M.-R., Ehdaie, B.: A view on the role of metabolites in enhanced stem reserves remobilization in wheat under drought during grain filling. - Aust. J. Crop Sci. 6: 1613-1623, 2012.
- Bernard, S.M., Habash D.Z.: The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. - New Phytol. 182: 608-620, 2009.
Go to original source... - Bradford, M.M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. - Anal. Biochem. 72: 248-254, 1976.
Go to original source... - Brugière, N., Dubois, F., Limami, A.M., Lelandais, M., Roux, Y., Sangwan, R.S., Hirel, B.: Glutamine synthetase in the phloem plays a major role in controlling proline production. - Plant Cell 11: 1995-2011, 1999.
Go to original source... - Buchanan-Wollaston, V., Earl, S., Harrison, E., Mathas, E., Navabpour, S., Page, T., Pink, D.: The molecular analysis of leaf senescence - a genomics approach. - Plant Biotech. J. 1: 3-22, 2003.
Go to original source... - Caputo, C., Barneix, A.J.: Export of amino acids to the phloem in relation to N supply in wheat. - Physiol. Plant. 101: 853-860, 1997.
Go to original source... - Caputo, C., Fatta, N., Barneix, A.J.: The amino acid export to the phloem is altered in wheat plants lacking the short arm of chromosome 7B. - J. exp. Bot. 52: 1761-1768, 2001.
Go to original source... - Caputo, C., Criado, M.V., Roberts, I.N., Gelso, M.A., Barneix, A.J.: Regulation of glutamine synthetase 1 and amino acids transport in the phloem of young wheat plants. - Plant Physiol. Biochem. 47: 335-342, 2009.
Go to original source... - Cataldo, D.A., Haroon, M., Schrader, L.E., Youngs, V.L.: Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. - Commun. Soil Sci. Plant Anal. 6: 71-80, 1975.
Go to original source... - Chen, P., Wang, L.: Effects of sulfur deficiency on photosynthesis and chlorophyll fluorescence of Citrus sinensis Osbeck leaves. - Chin. J. Ecol. 05, 2006.
- Cren, M., Hirel, B.: Glutamine synthetase in higher plants: regulation of gene and protein expression from the organ to the cell. - Plant Cell Physiol. 40: 1187-1193, 1999.
Go to original source... - Dalling, M.J.: The physiological basis of nitrogen redistribution during grain filling in cereals - In: Harper, J.D, Schrader, L.E., Howell, R.W. (ed.): Exploitation of Physiological and Genetic Variability to Enhance Crop Productivity. Pp. 55-69. Waverly Press, Baltimore 1985.
- De Bona, F.D., Fedoseyenko, D., Von Wirén, N., Monteiro, F.A.: Nitrogen utilization by sulfur-deficient barley plants depends on the nitrogen form. - Environ. exp. Bot. 74: 237-244, 2011.
Go to original source... - Dubousset, L., Abdallah, M., Desfeux, A.S., Etienne, P., Meuriot, F., Hawkesford, M.J., Gombert, J., Ségura, R., Bataillé, M-P., Rezé, S., Bonnefoy, J., Ameline, A.F., Ourry, A., Le Dily, F., Avice, J.C.: Remobilization of leaf S compounds and senescence in response to restricted sulphate supply during the vegetative stage of oilseed rape are affected by mineral N availability. - J. exp. Bot. 60: 3239-3253, 2009.
Go to original source... - Edwards, J.W., Coruzzi, G.W.: Photorespiration and light act in concert to regulate the expression of the nuclear gene for chloroplast glutamine synthetase. - Plant Cell 1: 241-248, 1989.
Go to original source... - Goodall, A.J., Kumar, K., Tobin, A.K.: Identification and expression analyses of cytosolic glutamine synthetase genes in barley (Hordeum vulgare L.). - Plant Cell Physiol. 54: 492-505, 2013.
Go to original source... - Hesse, H., Nikiforova, V., Gakière, B., Hoefgen, R.: Molecular analysis and control of cysteine biosynthesis: integration of nitrogen and sulphur metabolism. - J. exp. Bot. 55: 1283-1292, 2004.
Go to original source... - Kohl, S., Hollmann, J., Blattner, F.R., Radchuk, V., Andersch, F., Steuernagel, B., Schmutzer, T., Scholz, U., Krupinska, K., Weber, H., Weschke, W.: A putative role for amino acid permeases in sink-source communication of barley tissues uncovered by RNA-seq. - BMC Plant Biol. 12: 154. doi: 10.1186/1471-2229-12-154, 2012.
Go to original source... - Larher, F., Aziz, A., Deleu, C., Lemesle, P., Ghaffar, A., Bouchard, F., Plasman, M.: Suppression of the osmoinduced proline response of rapeseed leaf discs by polyamines. - Physiol. Plant. 102: 139-147, 1998.
Go to original source... - Lewandowska, M., Sirko, A.: Recent advances in understanding plant response to sulfur-deficiency stress. - Acta biochim. polon. 55: 457-471, 2008.
Go to original source... - Lunde, C., Zygadlo, A., Simonsen, H.T., Nielsen, P.L., Blennow, A., Haldrup, A.: Sulfur starvation in rice: the effect on photosynthesis, carbohydrate metabolism, and oxidative stress protective pathways. - Physiol. Plant. 134: 508-521, 2008.
Go to original source... - Martin, A., Lee, J., Kichey, T., Gerentes, D., Zivy, M., Tatout, C., Dubois, F., Balliau, T., Valot, B., Davanture, M., Tercé-Laforgue, T., Quilleré, I., Coque, M., Gallais, A., Gonzales-Moro, M-B., Bethencourt, L., Habash, D.Z., Lea, P.J., Charcosset, A., Perez, P., Murigneux, A., Sakakibara, H., Edwards, K.J., Hirel, B.: Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. - Plant Cell. 18: 3252-3274, 2006.
Go to original source... - Miflin, B.J., Habash, D.Z.: 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 (Inorganic Nitrogen Assimilation Special Issue): 979-987, 2002.
Go to original source... - Nikiforova, V.J., Gakiére, B., Kempa, S., Adamik, M., Willmitzer, L., Hesse, H., Hoefgen, R.: Towards dissecting nutrient metabolism in plants: a systems biology case study on sulphur metabolism. - J. exp. Bot. 55 (Sulphur Metabolism in Plants Special Issue): 1861-1870, 2004.
Go to original source... - Nikiforova, V.J., Kopka, J., Tolstikov, V., Fiehn, O., Hopkins, L., Hawkesford, M.J., Hesse, H., Hoefgen, R.: Systems rebalacing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidospsis plants. - Plant Physiol. 138: 304-318, 2005.
Go to original source... - Pratelli, R., Pilot, G.: Regulation of amino acid metabolic enzymes and transporters in plants. - J. exp. Bot. 65: 5535-5556, 2014.
Go to original source... - Scherer, H.W.: Sulphur in crop production. - Eur. J. Agron. 14: 81-111, 2001.
Go to original source... - Sorin, E., Etienne, P., Maillard, A., Zamarreño, A-M., Garcia-Mina, J-M., Arkoun, M., Jamois, F., Cruz, F., Yvin, J-C., Ourry, A.: Effect of sulphur deprivation on osmotic potential components and nitrogen metabolism in oilseed rape leaves: identification of a new early indicator. - J. exp. Bot. 66: 6175-6189, 2015.
Go to original source... - Tabuchi, M., Sugiyama, K., Ishiyama, K., Inoue, E., Sato, T., Takahashi, H., Yamaya, T.: Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1; 1, a cytosolic glutamine synthetase1; 1. - Plant J. 42: 641-651, 2005.
Go to original source... - Tegeder, M., Rentsch, D.: Uptake and partitioning of amino acids and peptide. - Mol. Plant. 3: 997-1011, 2010.
Go to original source... - Tegeder, M.: Transporters for amino acids in plant cells: some functions and many unknowns. - Curr. Opin. Plant Biol. 15: 315-321, 2012.
Go to original source... - Veliz, C.G., Criado, M.V., Roberts, I.N., Echeverria, M., Prystupa, P., Prieto, P., Gutierrez Boem, F.H., Caputo, C.: Phloem sugars and amino acids as potential regulators of hordein expression in field grown malting barley (Hordeum vulgare L.). - J. Cereal Sci. 60: 433-439, 2014.
Go to original source... - Wallsgrove, R.M., Turner, J.C., Hal, N.P., Kendall, A.C., Bright, S.W.: Barley mutants lacking chloroplast glutamine synthetase - biochemical and genetic analysis. - Plant Physiol. 83: 155-158, 1987.
Go to original source... - Weibull, J., Ronquist, F., Brishammar, S.: Free amino acid composition of leaf exudates and phloem sap: a comparative study in oats and barley. - Plant Physiol. 92: 222-226, 1990.
Go to original source... - Winter, H., Lohaus, G., Heldt, H.W.: Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. - Plant Physiol. 99: 996-1004, 1992.
Go to original source... - Yamaya, T., Kusano, M.: Evidence supporting distinct functions of three cytosolic glutamine synthetases and two NADH-glutamate synthases in rice. - J. exp. Bot. 65: 5519-5525, 2014.
Go to original source... - Yemm, E.W., Cocking, E.C.: The determination of amino acids with ninhydrin. - Analyst 80: 209-214, 1955.
Go to original source... - Zhao, F.J., Fortune, S., Barbosa, V.L., McGrath, S.P., Stobart, R., Bilsborrow, P.E., Booth, E.J., Brown, A., Robson, P.: Effects of sulphur on yield and malting quality of barley. - J. Cereal Sci. 43: 369-377, 2006.
Go to original source...



