Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine
Petronia Carillo A C , Gabriella Mastrolonardo A , Francesco Nacca A , Danila Parisi A , Angelo Verlotta A B and Amodio Fuggi AA Dipartimento di Scienze della Vita, Seconda Università degli Studi di Napoli, Via Vivaldi 43, 81100 Caserta, Italy.
B Istituto Sperimentale per la Cerealicoltura C. R. A., SS 16 Km 675, 71100 Foggia, Italy.
C Corresponding author. Email: petronia.carillo@unina2.it
Functional Plant Biology 35(5) 412-426 https://doi.org/10.1071/FP08108
Submitted: 3 March 2008 Accepted: 29 April 2008 Published: 11 July 2008
Abstract
We studied the effect of salinity on amino acid, proline and glycine betaine accumulation in leaves of different stages of development in durum wheat under high and low nitrogen supply. Our results suggest that protective compounds against salt stress are accumulated in all leaves. The major metabolites are glycine betaine, which preferentially accumulates in younger tissues, and proline, which is found predominantly in older tissues. Proline tended to accumulate early, at the onset of the stress, while glycine betaine accumulation was observed during prolonged stress. Nitrate reductase (NR) and glutamate synthase (GOGAT) are positively correlated with these compatible solutes: proline is associated with NR in the oldest leaves of high-nitrate plants and glycine betaine is associated with GOGAT in the youngest leaves of both low- and high-nitrate plants. In high-nitrate conditions proline accounts for more than 39% of the osmotic adjustment in the cytoplasmic compartments of old leaves. Its nitrogen-dependent accumulation may offer an important advantage in that it can be metabolised to allow reallocation of energy, carbon and nitrogen from the older leaves to the younger tissues. The contribution of glycine betaine is higher in young leaves and is independent of nitrogen nutrition.
Additional keywords: compatible solutes, glutamate synthase, nitrate reductase, nitrogen metabolism, salt stress.
Acknowledgements
The research was supported by ‘Ministero dell’Istruzione, dell’Università e della Ricerca’ and ‘Seconda Universitá di Napoli (Fondi di Ateneo)’. We gratefully acknowledge the kind gift of the rabbit antiserum raised against purified GOGAT from Dr Brian Forde (Department of Biological Science, Lancaster University, UK). We gratefully acknowledge Dr Ronan Sulpice and Dr John E. Lunn (Max Planck Institute of Molecular Plant Physiology, Golm, Germany) for advice during the course of this work and Dr Gareth S. Catchpole (Max Planck Institute of Molecular Plant Physiology, Golm, Germany) for his critical and constructive review of the manuscript.
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.
| Crossref | GoogleScholarGoogle Scholar |
[verified 11 May 2008].
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gibon Y,
Bessieres MA, Larher F
(1997) Is glycine betaine a non-compatible solute in higher plants that do not accumulate it? Plant, Cell and Environment 20, 329–340.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hare PD,
Cress WA, Van Staden J
(1998) Dissecting the roles of osmolyte accumulation during stress. Plant, Cell & Environment 21, 535–553.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kavi Kishor PB,
Sangam S,
Amrutha RN,
Sri Laxmi P,
Naidu KR,
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.
Kleczkowski LA, Givan CV
(1988) Serine formation in leaves by mechanisms other than the glycolate pathway. Journal of Plant Physiology 132(6), 641–652.
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.
| Crossref | GoogleScholarGoogle 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. Annual Review of Plant Physiology and Plant Molecular Biology 47, 569–593.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lancien M,
Martin M,
Hsieh M-H,
Leustek T,
Goodman H, Coruzzi GM
(2002) Arabidopsis glt1-T mutant defines a role for NADH-GOGAT in the non-photorespiratory ammonium assimilatory pathway. The Plant Journal 29(3), 347–358.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lutts S,
Majerus V, Kinet J-M
(1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedling. Physiologia Plantarum 105, 450–458.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Mansour MMF
(2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biologia Plantarum 43, 491–500.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle 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. Journal of Experimental Botany 53, 979–987.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Munns R
(2002) Comparative physiology of salt and water stress. Plant, Cell and Environment 25, 239–250.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Papageorgiou GC,
Fujimura Y, Murat N
(1991) Protection of the oxygen-evolving photosystem II complex by glycinebetaine. Biochimica et Biophysica Acta 1057, 361–366.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Rao KR, Gnanam A
(1990) Inhibition of nitrate and nitrite reductase activities by salinity stress in Sorghum vulgare. Phytochemistry 29, 1047–1049.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| PubMed |
Sairam RK, Tyagi A
(2004) Physiology and molecular biology of salinity stress tolerance in plants. Current Science 86, 407–421.
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sulpice R,
Gibon Y,
Bouchereau A, Larher F
(1998) Exogenously supplied glycine betaine in spinach and rapeseed leaf discs: compatibility or non-compatibility? Plant, Cell and Environment 21, 1285–1292.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Suzuki A, Rothstein S
(1997) Structure and regulation of ferredoxin-dependent 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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Temple SJ,
Vance CP, Gantt JS
(1998) Glutamate synthase and nitrogen assimilation. Trends in Plant Science 3, 51–56.
| Crossref | GoogleScholarGoogle Scholar |
Tester M, Davenport RJ
(2003) Na+ transport and Na+ tolerance in higher plants. Annals of Botany 91, 503–527.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tischner R
(2000) Nitrate uptake and reduction in higher and lower plants. Plant, Cell and Environment 23, 1005–1024.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Van Quy L,
Foyer C, Champigny M-L
(1991) Effect of light and NO3
− on wheat leaf phosphoenolpyruvate carboxylase activity. Evidence for covalent modulation of the C3 enzyme. Plant Physiology 97(4), 1476–1482.
| PubMed |
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.
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.
| Crossref | GoogleScholarGoogle Scholar |
Yang X, Lu C
(2005) Photosynthesis is improved by exogenous glycine betaine in salt-stressed maize plants. Physiologia Plantarum 124, 343–352.
| Crossref | GoogleScholarGoogle Scholar |
Zelitch I
(1992) Control of plant productivity by regulation of photorespiration. Bioscience 42, 510–520.
| Crossref | GoogleScholarGoogle Scholar |
