Abstract
The present study aimed to investigate the effect of exogenous spermidine (Spd) on cucumber (Cucumis sativus L. cv. Jinyou No. 4) growth and carbon–nitrogen balance under 80 mM Ca(NO3)2 stress. The result showed that leaf-applied Spd (1 mM) treatment alleviated the growth inhibition caused by Ca(NO3)2 stress by regulating the carbon–nitrogen balance in cucumber seedlings. The application of exogenous Spd effectively regulated the transcription levels and activities of major carbon–nitrogen metabolism enzymes, resulting in a significant decrease of NO3 − and NH4 + contents under Ca(NO3)2 stress. In addition, Spd treatment remarkably increased the accumulation of soluble carbohydrates (sucrose, fructose and glucose), thus protected enzyme activities related N metabolism and effectively promoted NO3 − assimilation under Ca(NO3)2 stress. Exogenous Spd also enhanced total amino acids, which serve as the building blocks of protein, and promoted the biosynthesis of soluble protein. In the presence of Spd, total C content and the C/N ratio increased significantly, while total N content decreased in response to Ca(NO3)2 stress. Based on our results, we suggested that exogenous Spd could effectively accelerate nitrate transformation into amino acids and improve the accumulation of carbon assimilation production, thereby enhancing the ability of the plants to maintain their C–N balance, and eventually promote the cucumber Ca(NO3)2 stress tolerance.
Similar content being viewed by others
Abbreviations
- GDH:
-
Glutamate dehydrogenase
- GOGAT:
-
Glutamate synthase
- GOT:
-
Glutamic-oxaloacetic transaminase
- GPT:
-
Glutamic-pyruvic transaminase
- GS:
-
Glutamine synthetase
- ICDH:
-
Isocitrate dehydrogenase
- NiR:
-
Nitrite reductase
- NR:
-
Nitrate reductase
- PAs:
-
Polyamines
- Put:
-
Putrescine
- Spd:
-
Spermidine
- Spm:
-
Spermine
References
Aarnes H, Eriksen AB, Petersen D, Rise F (2007) Accumulation of ammonium in Norway spruce (Picea abies) seedlings measured by in vivo 14 N-NMR. J Exp Bot 58(5):929–934
Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231(6):1237–1249
Alla MMN, Khedr AHA, Serag MM, Abu-Alnaga AZ, Nada RM (2012) Regulation of metabolomics in Atriplex halimus growth under salt and drought stress. Plant Growth Regul 67(3):281–304
Ashraf M, Foolad MA (2007) Improving plant abiotic-stress resistance by exogenous application of osmoprotectants glycine betaine and proline. Environ Exp Bot 59:206–216
Aubry S, Brown NJ, Hibberd JM (2011) The role of proteins in C3 plants prior to their recruitment into the C4 pathway. J Exp Bot 62:3049–3059
Aurisano N, Bertani A, Reggiani R (1995) Involvement of calcium and calmodulin in protein and amino acid metabolism in rice roots under anoxia. Plant Cell Physiol 36:1525–1529
Basu PS, Ali M, Chaturvedi SK (2007) Osmotic adjustment increases water uptake, remobilization of assimilates and maintains photosynthesis in chickpea under drought. Indian J Exp Biol 45(3):261–267
Bradford MM (1976) A rapid method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584
Buysse J, Merckx R (1993) An important colorimetric method to quantify sugar content of 307 plant tissue. J Exp Bot 44:1627–1629
Cataldo DA, Haroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6:71–80
Datta R, Sharma R (1999) Temporal and spatial regulation of nitrate reductase and nitrite reductase in greening maize leaves. Plant Sci 144:77–83
Foyer CH, Noctor G, Hodges M (2011) Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J Exp Bot 62:1467–1482
Gao H, Jia Y, Guo S, Lv G, Wang T, Juan L (2011) Exogenous calcium affects nitrogen metabolism in root-zone hypoxia-stressed muskmelon roots and enhances short-term hypoxia tolerance. J Plant Physiol 168:1217–1225
Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155(4):1566–1577
González EM, Aparicio-Tejo PM, Gordon AJ, Minchin FR, Royuela M, Arrese-Igor C (1998) Water-deficit effects on carbon and nitrogen metabolism of pea nodules. J Exp Bot 49(327):1705–1714
Gupta K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35(7):2015–2036
Hayashi F, Ichino T, Osanai M, Wada K (2000) Oscillation and regulation of proline content by P5Cs and ProDH gene expressions in the light/dark cycles in Arabidopsis thaliana L. Plant Cell Physiol 41:1096–1101
He FF, Chen Q, Jiang RF, Chen XP, Zhang FS (2007) Yield and nitrogen balance of greenhouse tomato (Lycopersium esculentum Mill.) with conventional and site-specific nitrogen management in northern China. Nutr Cycl Agroecosyst 77:1–14
Hodges M (2002) Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J Exp Bot 53(370):905–916
Hussain SS, Ali M, Ahmad M, Siddique KH (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29(3):300–311
Hussin S, Geissler N, Koyro HW (2013) Effect of NaCl salinity on Atriplex nummularia (L.) with special emphasis on carbon and nitrogen metabolism. Acta Physiol Plant 35:1025–1038
Kaiser WM, Huber SC (2001) Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J Exp Bot 52(363):1981–1989
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. J Exp Bot 53:875–882
Kamiab F, Talaie A, Khezri M, Javanshah A (2014) Exogenous application of free polyamines enhance salt tolerance of pistachio (Pistacia vera L.) seedlings. Plant Growth Regul 72(3):257–268
Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45(6):712–722
Koyro HW, Ahmad P, Geissler N (2012) Abiotic stress responses in plants: an overview, Chap. 1. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, Berlin, pp 1–28
Krapp A, Truong HN (2005) Regulation of C/N interaction in model plant species. In: Goyal S, Tischner R, Basra A (eds) Enhancing the efficiency of nitrogen utilization in plants. Haworth Press, New York, pp 127–173
Kronzucker HJ, Britto DT, Davenport RJ, Tester M (2001) Ammonium toxicity and the real cost of transport. Trends Plant Sci 6:335–337
Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 53(370):773–787
Legocka J, Kluk A (2005) Effect of salt and osmotic stress on changes in polyamine content and arginine decarboxylase activity in Lupinus luteus seedlings. J Plant Physiol 162:662–668
Li D, Wu Z, Liang C, Chen L (2004) Characteristics and regulation of greenhouse soil environment. Chin J Ecol 23:192–197
Lin CC, Kao CH (1996) Disturbed ammonium assimilation is associated with growth inhibition of roots in rice seedlings caused by NaCl. Plant Growth Regul 18:233–238
Liu C, Wang Y, Pan K, Zhu T, Li W, Zhang L (2014) Carbon and nitrogen metabolism in leaves and roots of dwarf bamboo (Fargesia denudata Yi) subjected to drought for two consecutive years during sprouting period. J Plant Growth Regul 33:243–255
Lòpez-Millàn AF, Morales F, Andaluz S, Gogorcena Y, Abadìa A, De Las Rivas J, Abadìa J (2000) Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use. Plant Physiol 124:885–897
Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43:491–500
Mattoo AK, Sobolev AP, Neelam A, Goyal RK, Handa AK, Segre AL (2006) Nuclear magnetic resonance spectroscopy-based metabolite profiling of transgenic tomato fruit engineered to accumulate spermidine and spermine reveals enhanced anabolic and nitrogen–carbon interactions. Plant Physiol 142:1759–1770
Mishra P, Dubey RS (2011) Nickel and Al-excess inhibit nitrate reductase but upregulate activities of aminating glutamate dehydrogenase and aminotransferases in growing rice seedlings. Plant Growth Regul 64(3):251–261
Misra N, Gupta AK (2005) Effect of salt stress on proline metabolism in two high yielding genotypes of green gram. Plant Sci 169:331–339
Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon–nitrogen interactions. Mol Plant 3:973–996
Qiao X, Wang P, Shi G, Yang H (2015) Zinc conferred cadmium tolerance in Lemna minor L. via modulating polyamines and proline metabolism. Plant Growth Regul 77(1):1–9
Reda M, Migocka M, Klobus G (2011) Effect of short-term salinity on the nitrate reductase activity in cucumber roots. Plant Sci 180:783–788
Repčák M, Pal’ove-Balang P, Dučaiová Z, Sajko M, Bendek F (2014) High nitrogen supply affects the metabolism of Matricaria chamomilla leaves. Plant Growth Regul 73(2):147–153
Rosales EP, Iannone MF, Groppa MD, Benavides MP (2012) Polyamines modulate nitrate reductase activity in wheat leaves: involvement of nitric oxide. Amino Acids 42:857–865
Schlüter U, Mascher M, Colmsee C, Scholz U, Bräutigam A, Fahnenstich H, Sonnewald U (2012) Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Physiol 160:1384–1406
Seebauer JR, Moose SP, Fabbri BJ, Crossland LD, Below FE (2004) Amino acid metabolism in maize ear shoots: implications for assimilate preconditioning and nitrogen signaling. Plant Physiol 136:4326–4334
Sharma S, Dietz K (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726
Shi H, Ye T, Chan Z (2013a) Comparative proteomic and physiological analyses reveal the protective effect of exogenous polyamines in the bermuda grass (Cynodon dactylon) response to salt and drought stresses. J Proteome Res 12:4807–4829
Shi H, Ye T, Chen F, Cheng Z, Wang Y, Yang P, Zhang Y, Chan Z (2013b) Manipulation of arginase expression modulates abiotic stress tolerance in Arabidopsis: Effect on arginine metabolism and ROS accumulation. J Exp Bot 64:1367–1379
Simon-Sarkadi L, Kocsy G, Várhegyi Á, Galiba G, De Ronde JA (2006) Stress-induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Plant Biol 50:793–796
Singh RP, Srivastava HS (1983) Regulation of glutamate dehydrogenase activity by amino acids in maize seedlings. Physiol Plant 57:549–554
Skopelitis DS, Paranychianakis NV, Paschalidis KA, Pliakonis ED, Delis ID, Yakoumakis DI, Kouvarakis A, Papadakis AK, Stephanou EG, Roubelakis-Angelakis KA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18(10):2767–2781
Solorzano L (1969) Determination of ammonia in natural waters by the phenolhy pochlorite method. Limnol Oceanogr 14:799–801
Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5:199–206
Sun W, Huang A, Sang Y, Fu Y, Yang Z (2013) Carbon–nitrogen interaction modulates plant growth and expression of metabolic genes in rice. J Plant Growth Regul 32:575–584
Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6
Tang ZC (1999) Experimental guide of modern plant physiology. Science Press, Shanghai, pp 138–139, 154–157
Todorova D, Sergiev I, Alexieva V, Karanov E, Smith A, Hall M (2007) Polyamine content in Arabidopsis thaliana (L.) Heynh during recovery after low and high temperature treatments. Plant Growth Regul 51:185–191
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759
Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotech 16:1–10
Yu H, Li T, Zhou J (2005) Secondary salinization of greenhouse soil and its effects on soil properties. Soils 37:581–586
Yuan L, Yuan Y, Du J, Sun J, Guo S (2012) Effects of 24-epibrassinolide on nitrogen metabolism in cucumber seedlings under Ca(NO3)2 stress. Plant Physiol Bioch 61:29–35
Zhang YH, Zhang G, Liu LY, Zhao K, Wu LS, Hu CX, Di HJ (2011) The role of calcium in regulating alginate-derived oligosaccharides in nitrogen metabolism of Brassica campestris L. var. Tsen et Lee. Plant Growth Regul 64(2):193–202
Zhang Y, Hu XH, Shi Y, Zou ZR, Yan F, Zhao YY, Zhang H, Zhao JZ (2013) Beneficial role of exogenous spermidine on nitrogen metabolism in tomato seedlings exposed to saline-alkaline stress. J Amer Soc Hort Sci 138(1):28–49
Acknowledgments
This work was financially supported by the National Natural Science Foundation of China (No. 31471869, No. 31272209 and No. 31401919), the National Key Technology R&D Program (2013BAD20B05), the Jiangsu Province Scientific and Technological Achievements into Special Fund (BA2014147), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Du, J., Shu, S., An, Y. et al. Influence of exogenous spermidine on carbon–nitrogen metabolism under Ca(NO3)2 stress in cucumber root. Plant Growth Regul 81, 103–115 (2017). https://doi.org/10.1007/s10725-016-0193-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-016-0193-8