Nitrogen metabolism in durum wheat under salinity: Accumulation of proline and glycine betaine

Functional Plant Biology

Volumn 35, Issue 5, 2008, Pages 412-426

  Carillo, Petronia ^a   Mastrolonardo, Gabriella ^a   Nacca, Francesco ^a   Parisi, Danila ^a   Verlotta, Angelo ^a,b   Fuggi, Amodio ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b Ist Sperim per la Cerealicoltura   (Italy)

Author keywords

Compatible solutes; Glutamate synthase; Nitrate reductase; Nitrogen metabolism; Salt stress

Indexed keywords

AGRICULTURAL PRODUCTS; AMINES; AMINO ACIDS; ARSENIC COMPOUNDS; BIOCHEMISTRY; HEALTH; HISTOLOGY; NITRATES; NITROGEN; ORGANIC ACIDS; SALINITY MEASUREMENT;

COMPATIBLE SOLUTES; CYTOPLASMIC COMPARTMENTS; DURUM WHEATS; GLUTAMATE SYNTHASE; GLYCINE BETAINE (GB); NITRATE REDUCTASE (NR); NITROGEN METABOLISM; NITROGEN NUTRITION; NITROGEN SUPPLY; OSMOTIC ADJUSTMENT (OA); PROLINE (PRO); SALT STRESSES;

NONMETALS;

AMINO ACID; BIOACCUMULATION; CHEMICAL COMPOUND; ENZYME ACTIVITY; METABOLISM; NITROGEN; OSMOSIS; SALINITY; WHEAT;

TRITICUM AESTIVUM; TRITICUM TURGIDUM SUBSP. DURUM;

EID: 47349129436     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP08108     Document Type: Article

References (69)

1. Abd-El Baki GK, Siefritz F, Man HM, Weiner H, Kaldenhoff R, Kaiser WM (2000) Nitrate reductase in Zea mays L. under salinity. Plant, Cell and Environment 23, 515-521. doi: 10.1046/j.1365-3040.2000.00568.x
2. Abenavoli MR, Muscolo A, Panuccio R, Fuggi A (1993) Isoforme della glutammina sintetasi espresso durante la germinazione del grano duro (Triticum durum Desf., cv. Simeto). Atti del XI Convegno Società Italiana di Chimica Agraria Cremona, 21-24 Settembre 1993, Pàtron Editore.
3. Armengaud P, Thiery L, Buhot N, Grenier-De March G, Savoure A (2004) Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiologia Plantarum 120(3), 442-450. doi: 10.1111/j.0031-9317.2004.00251.x
4. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59, 206-216. doi: 10.1016/j.envexpbot. 2005.12.006
5. 2: The MAPLE results'. (Eds A Raschi, FP Vaccari, F Miglietta) pp. 117-132. (Office for Official Publications of the European Communities: Luxembourg)
6. Berteli F, Corrales E, Guerrero C, Ariza MJ, Pilego F, Valpuesta L (1995) Salt stress increases ferredoxin-dependent glutamate synthase activity and protein level in the leaves of tomato. Physiologia Plantarum 93, 259-264. doi: 10.1111/j.1399-3054.1995.tb02226.x
7. Bessieres MA, Gibon Y, Lefeuvre JC, Larher F (1999) A single-step purification for glycine betaine determination in plant extracts by isocratic HPLC. Journal of Agricultural and Food Chemistry 47, 3718-3722. doi: 10.1021/jf990031h
8. Bowsher CG, Tobin AK (2001) Compartmentation of metabolism within mitochondria and plastids. Journal of Experimental Botany 52(356), 513-527. doi: 10.1093/jexbot/52.356.513
9. Bradford MM (1976) A rapid and sensitive method for the quantification of microrganism quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 72, 248-254. doi: 10.1016/0003-2697(76)90527-3
10. Brugnoli E, Lauteri M (1991) Effects of salinity on stomatal conductance, photosynthetic capacity and carbon isotope discrimination of salt-tolerant (Gossypium hirsutum L.) and salt-sensitive (Phaseolus vulgaris L.) C3 non-halophytes. Plant Physiology 95, 628-635.
11. Carillo P, Mastrolonardo G, Nacca F, Fuggi A (2005) Nitrate reductase in durum wheat seedlings as affected by nitrate nutrition and salinity. Functional Plant Biology 32(3), 209-219. doi: 10.1071/FP04184
12. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156-159. doi: 10.1016/0003-2697(87)90021-2
13. Colmer TD, Epstein E, Dvorak J (1995) Differential solute regulation in leaf blades of various ages in salt-sensitive wheat and a salt-tolerant wheat x Lophopyrum elongatum (Host) A. Love Amphiploid. Plant Physiology 108, 1715-1724.
14. Davenport R, James RA, Zakrisson-Plogander A, Tester M, Munns R (2005) Control of sodium transport in durum wheat. Plant Physiology 137, 807-818. doi: 10.1104/pp.104.057307
15. de-Lacerda CF, Cambraia J, Oliva MA, Ruiz HA, Prisco JT (2003) Solute accumulation and distribution during shoot and leaf development in two sorghum genotypes under salt stress. Environmental and Experimental Botany 49, 107-120. doi: 10.1016/S0098-8472(02)00064-3
16. Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. The New Phytologist 158, 455-463. doi: 10.1046/j.1469-8137.2003.00770.x
17. FAO (2005) Food and Agriculture Organization of the United Nations. Data available online at http://www.fao.org/ag/agl/aglw/aquastat/main/index.stm [verified 11 May 2008].
18. Ferrario-Méry S, Valadier MH, Foyer CH (1998) Overexpression of nitrate reductase in tobacco delays drought-induced decreases in nitrate reductase activity and mRNA. Plant Physiology 117, 293-302. doi: 10.1104/pp.117.1.293
19. Flagella Z, Trono D, Pompa M, Di Fonzo N, Pastore D (2006) Seawater stress applied at germination affects mitochondrial function in durum wheat (Triticum durum) early seedlings. Functional Plant Biology 33(4), 357-366. doi: 10.1071/FP05244
20. Forde BG (2002) The role of long-distance signalling in plant responses to nitrate and other nutrients. Journal of Experimental Botany 53(366), 39-43. doi: 10.1093/jexbot/53.366.39
21. Foyer CH, Valadier MH, Migge A, Becker TW (1998) Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiology 117, 283-292. doi: 10.1104/pp.117.1.283
22. Gibon Y, Bessieres MA, Larher F (1997) Is glycine betaine a noncompatible solute in higher plants that do not accumulate it? Plant, Cell and Environment 20, 329-340. doi: 10.1046/j.1365-3040.1997.d01-82.x
23. Gibon Y, Sulpice R, Larher F (2000) Proline accumulation in canola leaf discs subjected to osmotic stress is related to the loss of chlorophylls and to the decrease of mitochondrial activity. Physiologia Plantarum 110, 469-476. doi: 10.1111/j.1399-3054.2000.1100407.x
24. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Hoehne M, Hendriks JHM, Palacios-Rojas N, Cross J, Selbig J, Stitt M (2004) A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and prolonged darkness. The Plant Cell 16, 3304-3325. doi: 10.1105/tpc.104.025973
25. Gibon Y, Usadel B, Blaesing OE, Kamlage B, Hoehne M, Trethewey R, Stitt M (2006) Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biology 7, R76. doi: 10.1186/gb-2006-7-8-r76
26. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant, Cell & Environment 21, 535-553. doi: 10.1046/j.1365-3040.1998.00309.x
27. Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463-499. doi: 10.1146/annurev.arplant.51. 1.463
28. Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Molecular Biology 43, 103-111. doi: 10.1023/A:1006408712416
29. Iglesias-Bartolomé R, González CA, Kenis JD (2004) Nitrate reductase dephosphorylation is induced by sugars and sugar-phosphates in corn leaf segments. Physiologia Plantarum 122, 62-67. doi: 10.1111/j.1399-3054.2004.00375.x
30. Ireland RJ, Lea PJ (1999) The enzymes of glutamine, glutamate, asparagine and aspartate metabolism. In 'Plant amino acids, biochemistry and biotechnology'. (Ed. BK Singh) pp. 49-109. (Marcel Dekker: New York)
31. Kaiser WM, Weiner H, Wuber SC (1999) Nitrate reductase in higher plants: a case for transduction of environmental stimuli into control of catalytic activity. Plant Physiology 100, 773-779.
32. Kaiser WM, Weiner H, Kandlbinder A, Tsai CB, Rockel P, Sonoda M, Planchet E (2002) Modulation of nitrate reductase: some new insights, an unusual case and a potentially important side reaction. Journal of Experimental Botany 53, 875-882. doi: 10.1093/jexbot/53.370.875
33. Kavi Kishor PB, Sangam S, Amrutha RN, Sri Laxmi P, NaiduKR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Current Science 88, 424-438.
34. Kleczkowski LA, Givan CV (1988) Serine formation in leavesby mechanisms other than the glycolate pathway. Journal of Plant Physiology 132(6), 641-652.
35. Kuznetsov VV, Shevyakova NI (1997) Stress response in tobacco cells to high temperature and salinity. Proline accumulation and phosphorylation of polypeptides. Physiologia Plantarum 100, 320-326. doi: 10.1111/j.1399-3054.1997.tb04789.x
36. Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 569-593. doi: 10.1146/annurev.arplant.47.1.569
37. Lancien M, Gadal P, Hodges M (2000) Enzyme redundancy and the importance of 2-oxoglutarate in higher plant ammonium assimilation. Plant Physiology 123, 817-824. doi: 10.1104/pp.123.3.817
38. Lancien M, Martin M, Hsieh M-H, Leustek T, Goodman H, Coruzzi GM (2002) Arabidopsis glt1-T mutant defines a role for NADH-GOGATin the non-photorespiratory ammonium assimilatory pathway. The Plant Journal 29(3), 347-358. doi: 10.1046/j.1365-313X.2002.01218.x
39. Larher F, Rotival GN, Lemesle P, Plasman M, Bouchereau A (1996) The glycine betaine inhibitory effect on the osmoinduced proline response of rape leaf discs. Plant Science 113, 21-31. doi: 10.1016/0168-9452(95) 04277-6
40. Lillo C, Meyer C, Lea US, Provan F, Oltedal S (2004) Mechanism and importance of post-translational regulation of nitrate reductase. Journal of Experimental Botany 55, 1275-1282. doi: 10.1093/jxb/erh132
41. Lutts S, Majerus V, Kinet J-M (1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedling. Physiologia Plantarum 105, 450-458. doi: 10.1034/j.1399-3054.1999.105309.x
42. Mäkelä P, Peltonen-Sainio P, Jokinen K, Pehu E, Setälä H, Hinkkanen R, Somersalo S (1996) Uptake and translocation of foliar-applied glycine betaine in crop plants. Plant Science 121(2), 221-230. doi: 10.1016/S0168-9452(96)04527-X
43. Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biologia Plantarum 43, 491-500. doi: 10.1023/A:1002873531707
44. Mattioni C, Lacerenza NG, Troccoli A, De Leonardis AM, Di Fonzo N (1997) Water and salt stress-induced alterations in proline metabolism of Triticum durum seedlings. Physiologia Plantarum 101, 787-792. doi: 10.1111/j.1399-3054.1997.tb01064.x
45. 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. Journal of Experimental Botany 53, 979-987. doi: 10.1093/jexbot/53.370.979
46. Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell and Environment 25, 239-250. doi: 10.1046/j.0016-8025.2001. 00808.x
47. Nuccio ML, McNeil SD, Ziemak MJ, Hanson AD, Jain RK, Selvaraj G (2000) Choline import into chloroplasts limits glycine betaine synthesis in tobacco: analysis of plants engineered with a chloroplastic or a cytosolic pathway. Metabolic Engineering 2(4), 300-311. doi: 10.1006/mben.2000.0158
48. Papageorgiou GC, Fujimura Y, Murat N (1991) Protection of the oxygen-evolving photosystem II complex by glycinebetaine. Biochimica et Biophysica Acta 1057, 361-366. doi: 10.1016/S0005-2728(05)80148-3
49. Rana G, Katerji N (2000) Measurement and estimation of actual evapotranspiration in the field under Mediterranean climate: a review. European Journal of Agronomy 13, 125-153. doi: 10.1016/S1161-0301(00)00070-8
50. Rao KR, Gnanam A (1990) Inhibition of nitrate and nitrite reductase activities by salinity stress in Sorghum vulgare. Phytochemistry 29, 1047-1049. doi: 10.1016/0031-9422(90)400-A
51. Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 44, 357-383. doi: 10.1146/annurev.pp.44.060193. 002041
52. Robinson SA, Stewart GR, Phillips R (1992) Regulation of glutamate dehydrogenase activity in relation to carbon limitation and protein catabolism in carrot cell suspension cultures. Plant Physiology 98, 1190-1195.
53. Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Current Science 86, 407-421.
54. Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant, Cell and Environment 25, 163-171. doi: 10.1046/j.0016-8025.2001.00790.x
55. Silveira JAG, Melo ARB, Viégas RA, Oliveira JTA (2001) Salinity-induced effects on nitrogen assimilation related to growth in cowpea plants. Environmental and Experimental Botany 46, 171-179. doi: 10.1016/S0098-8472(01)00095-8
56. Speer M, Kaiser WM (1991) Ion relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity. Plant Physiology 97, 990-997.
57. Stitt M, Müller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible WR, Krapp A(2002) Steps towards an integrated view of nitrogen metabolism. Journal of Experimental Botany 53, 959-970. doi: 10.1093/jexbot/53.370.959
58. Sulpice R, Gibon Y, Bouchereau A, Larher F (1998) Exogenously supplied glycine betaine in spinach and rapeseed leaf discs: compatibility or noncompatibility? Plant, Cell and Environment 21, 1285-1292. doi: 10.1046/j.1365-3040.1998.00362.x
59. Sulpice R, Gibon Y, Cornic G, Larher FR (2002) Interaction between exogenous glycine betaine and the photorespiratory pathway in canola leaf discs. Physiologia Plantarum 116, 460-467. doi: 10.1034/j.1399-3054. 2002.1160404.x
60. Suzuki A, Rothstein S (1997) Structure and regulation of ferredox-independent glutamate synthase from Arabidopsis thaliana. Cloning of cDNA expression in different tissues of wild-type and gltS mutant strains, and light induction. European Journal of Biochemistry 243, 708-718. doi: 10.1111/j.1432-1033.1997.00708.x
61. Temple SJ, Vance CP, Gantt JS (1998) Glutamate synthase and nitrogen assimilation. Trends in Plant Science 3, 51-56. doi: 10.1016/S1360-1385(97)01159-X
62. + tolerance in higher plants. Annals of Botany 91, 503-527. doi: 10.1093/aob/mcg058
63. Tischner R (2000) Nitrate uptake and reduction in higher and lower plants. Plant, Cell and Environment 23, 1005-1024. doi: 10.1046/j.1365-3040.2000.00595.x
64. Turano FJ, Muhitch MJ (1999) Differential accumulation of ferredoxin and NADH-dependent glutamate synthase activities, peptides, and transcripts in developing soybean seedlings in response to light, nitrogen and nodulation. Physiologia Plantarum 107, 407-418. doi: 10.1034/j.1399-3054.1999. 100406.x
65. - on wheat leaf phosphoenolpyruvate carboxylase activity. Evidence for covalent modulation of the C3 enzyme. Plant Physiology 97(4), 1476-1482.
66. Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Plant Physiology 144, 307-313.
67. Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philosophical Transactions of the Royal Society B. Biological Sciences 355, 1517-1529. doi: 10.1098/rstb.2000.0712
68. Yang X, Lu C (2005) Photosynthesis is improved by exogenous glycine betaine in salt-stressed maize plants. Physiologia Plantarum 124, 343-352. doi: 10.1111/j.1399-3054.2005.00518.x
69. Zelitch I (1992) Control of plant productivity by regulation of photorespiration. Bioscience 42, 510-520. doi: 10.2307/1311881