Abstract
Nitrogen (N) deficiency is one of the critical environmental factors that induce leaf senescence, and its occurrence may cause the shorten leaf photosynthetic period and markedly lowered grain yield. However, the physiological metabolism underlying N deficiency-induced leaf senescence and its relationship with the abscisic acid (ABA) concentration and reactive oxygen species (ROS) burst in leaf tissues are not well understood. In this paper, the effect of N supply on several senescence-related physiological parameters and its relation to the temporal patterns of ABA concentration and ROS accumulation during leaf senescence were investigated using the premature senescence of flag leaf mutant rice (psf) and its wild type under three N treatments. The results showed that N deficiency hastened the initiation and progression of leaf senescence, and this occurrence was closely associated with the upregulated expression of 9-cis-epoxycarotenoiddioxygenase genes (NCEDs) and with the downregulated expression of two ABA 8′-hydroxylase isoform genes (ABA8ox2 and ABA8ox3) under LN treatment. Contrarily, HN supply delayed the initiation and progression of leaf senescence, concurrently with the suppressed ABA biosynthesis and relatively lower level of ABA concentration in leaf tissues. Exogenous ABA incubation enhanced ROS generation and MDA accumulation in a dose-dependent manner, but it decreased the activities of glutamine synthetase (GS) and glutamate dehydrogenase (GDH) in detached leaf. These results suggested that the participation of ABA in the regulation of ROS generation and N assimilating/remobilizing metabolism in rice leaves was strongly responsible for induction of leaf senescence by N deficiency.
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References
Agüera E, Cabello P, de la Haba P (2010) Induction of leaf senescence by low nitrogen nutrition in sunflower (Helianthus annuus) plants. Physiol Plantarum 138:256–267
Asad MAU, Zakari SA, Zhao Q, Zhou L, Ye Y, Cheng F (2019) Abiotic stresses intervene with ABA signaling to induce destructive metabolic pathways leading to death: premature leaf senescence in plants. Int J Mol Sci 20:256–265
Balotf S, Kavoosi G, Kholdebarin B (2016) Nitrate reductase, nitrite reductase, glutamine synthetase, and glutamate synthase expression and activity in response to different nitrogen sources in nitrogen-starved wheat seedlings. Biotechnol Appl Biochem 63:220–229
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cabello P, Aguera E, de la Haba P (2006) Metabolic changes during natural ageing in sunflower (Helianthus annuus) leaves: expression and activity of glutamine synthetase isoforms are regulated differently during senescence. Physiol Plantarum 128:175–185
Distelfeld A, Avni R, Fischer AM (2014) Senescence, nutrient remobilization, and yield in wheat and barley. J Exp Bot 65:3783–3798
Gan S, Amasino RM (1997) Making sense of senescence-molecular genetic regulation and manipulation of leaf senescence. Plant Physiol 113:313–319
Havé M, Marmagne A, Chardon F, Masclaux-Daubresse C (2016) Nitrogen remobilisation during leaf senescence: lessons from Arabidopsis to crops. J Exp Bot 365:2513–2529
Hilary R, Sergi M (2016) Production and scavenging of reactive oxygen species and redox signaling during leaf and flower senescence: similar but different. Plant Physiol 171:1560–1568
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
Hung KT, Kao CH (2004) Hydrogen peroxide is necessary for abscisic acid-induced senescence of rice leaves. J Plant Physiol 161:1347–1357
Ji Y, Li Q, Liu G, Selvaraj G, Zheng Z, Zou J, Wei Y (2019) Roles of cytosolic glutamine synthetases in Arabidopsis development and stress responses. Plant Cell Physiol 60:657–671
Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273
Kichey T, Heumez E, Pocholle D, Pageau K, Vanacker H, Dubois F, Legouis J, Hirel B (2006) Combined agronomic and physiological aspects of nitrogen management in wheat highlight a central role for glutamine synthetase. New Phytol 169:265–278
Kojima M, Kamada-Nobusada T, Komatsu H, Takei K, Kuroha T, Mizutani M, Ashikari M, Ueguchi-Tanaka M, Matsuoka M, Suzuki K, Sakakibara H (2009) Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant Cell Physiol 50:1201–1214
Kraepiel Y, Rousselin P, Sotta B, Kerhoas L, Einhorn J, Caboche M, Miginiac E (1994) Analysis of phytochrome and ABA-deficient mutants suggests that ABA degradation is controlled by light in Nicotiana plumbaginifolia. Plant J 6:665–672
Li J, Li Y, Yin Z, Jiang J, Zhang M, Guo X, Ye Z, Zhao Y, Xiong H, Zhang Z, Shao Y, Jiang C, Zhang H, An G, Paek N-C, Ali J, Zichao L (2017) OsASR5 enhances drought tolerance through a stomatal closure pathway associated with ABA and H 2O2 signalling in rice. Plant Biotechnol J 15:183–196
Liang C, Chen L, Wang Y, Liu J, Xu G, Li T (2011) High temperature at grain-filling stage affects nitrogen metabolism enzyme activities in grains and grain nutritional quality in rice. Rice Sci 18:210–216
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Douce R, Packer L (eds) Methods in enzymology. Academic Press, New York, pp 350–382
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136
Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, Tan M, Dong W, Jiang M (2009) Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J Exp Bot 60:3221–3238
Liu J, Sun X, Xu F, Zhang Y, Zhang Q, Miao R, Zhang J, Liang J, Xu W (2018) Suppression of OsMDHAR4 enhances heat tolerance by mediating H2O2-induced stomatal closure in rice plants. Rice 11:38–46
Lu Y, Sasaki Y, Li X, Mori IC, Matsuura T, Hirayama T, Sato T, Yamaguchi J (2015) ABI1 regulates carbon/nitrogen-nutrient signal transduction independent of ABA biosynthesis and canonical ABA signalling pathways in Arabidopsis. J Exp Bot 66:2763–2771
Masclaux C, Valadier M-H, Brugière N, Morot-Gaudry JF, Hirel B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211:510–518
Masclaux-Daubresse C, Carrayol E, Valadier M-H (2005) The two nitrogen mobilisation and senescence-associated GS1 and GDH genes are controlled by C and N metabolites. Planta 221:580–588
Mega R, Meguro-Maoka A, Endo A, Shimosaka E, Murayama S, Nambara E, Seo M, Kanno Y, Abrams SR, Sato Y (2015) Sustained low abscisic acid levels increase seedling vigor under cold stress in rice. Sci Rep 5:13819
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185
Oka M, Shimoda Y, Sato N, Inoue J, Yamazaki T, Shimomura N, Fujiyama H (2012) Abscisic acid substantially inhibits senescence of cucumber plants grown under low nitrogen conditions. J Plant Physiol 169:789–796
Oliver SN, Dennis ES, Dolferus R (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol 48:1319–1330
Overmyer K, Brosché M, Kangasjarvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342
Quirino BF, Yoosun N, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282
Ronald WW, Lawrence VG, Bo L, Suzanne RA, Bruce EE (1994) Effects of abscisic acid (ABA) and ABA analogs on freezing tolerance, low-temperature growth, and flowering in rapeseed. J Plant Growth Regul 13:235–241
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101
Seger M, Gebril S, Tabilona J, Peel A, Sengupta-Gopalan C (2015) Impact of concurrent overexpression of cytosolic glutamine synthetase (GS1) and sucrose phosphate synthase (SPS) on growth and development in transgenic tobacco. Planta 24:69–81
Seiler C, Harshavardhan VT, Rajesh K, Reddy PS, Strickert M, Rolletschek H, Scholz U, Wobus U, Sreenivasulu N (2011) ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions. J Exp Bot 62:2615–2632
Shah JM, Asgher Z, Zeng J, Quan X, Ali E, Shamsi IH, Zhang G (2017) Growth and physiological characterization of low nitrogen responses in Tibetan wild barley (Hordeum spontaneum) and cultivated barley (Hordeum vulgare). J Plant Nutr 40:861–868
Teng K, Li J, Liu L, Han Y, Du Y, Zhang J, Sun H, Zhao Q (2014) Exogenous ABA induces drought tolerance in upland rice: the role of chloroplast and ABA biosynthesis-related gene expression on photosystem II during PEG stress. Acta Physiol Plant 36:2219–2227
Thiago BG, Danilo FADO, Cristiane ECDM, Eduardo LV (2017) Modulation of reserve mobilization by sucrose, glutamine, and abscisic acid during seedling establishment in sunflower. J Plant Growth Regul 36:11–21
Thompson AJ, Andrews J, Mulholland BJ, McKee JM, Hilton HW, Horridge JS, Farquhar GD, Smeeton RC, Smillie IR, Black CR, Taylor IB (2007) Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiol 143:1905–1917
Wang F, Liu J, Zhou L, Pan G, Li Z, Zaidi SHR, Cheng F (2016a) Senescence-specific change in ROS scavenging enzyme activities and regulation of various SOD isozymes to ROS levels in psf mutant rice leaves. Plant Physiol Biochem 109:248–261
Wang F, Liu J, Chen M, Zhou L, Li Z, Zhao Q, Pan G, Zaidi SHR, Cheng F (2016b) Involvement of abscisic acid in PSII photodamage and D1 protein turnover for light-induced premature senescence of rice flag leaves. PLoS ONE 11:e0161203
Xing Y, Jia WS, Zhang JH (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 produced via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440–451
Xing X, Zhou Q, Xing H, Jiang H, Wang S (2016) Early abscisic acid accumulation regulates ascorbate and glutathione metabolism in soybean leaves under progressive water stress. J Plant Growth Regul 35:865–876
Yang J, Zhang J, Wang Z, Wang Z, Zhu Q, Liu L (2003) Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling. Plant Cell Environ 26:1621–1631
Ye N, Zhu G, Liu Y, Li Y, Zhang J (2011) ABA controls H2O2 accumulation through the induction of osCATb in rice leaves under water stress. Plant Cell Physiol 52:689–698
Yoshida S (2003) Molecular regulation of leaf senescence. Curr Opin Plant Biol 6:79–84
Zhang FP, Sussmilch F, Nichols DS, Cardoso AA, Brodribb TJ, McAdam SAM (2018) Leaves, not roots or floral tissue, are the main site of rapid, external pressure-induced ABA biosynthesis in angiosperms. J Exp Bot 69:1261–1267
Zhang Z, Xiong S, Wei Y, Meng X, Wang X, Ma X (2017) The role of glutamine synthetase isozymes in enhancing nitrogen use efficiency of N-efficient winter wheat. Sci Rep 7:1000–1012
Acknowledgements
The authors are deeply indebted to National Key Research and Development Plan of China (No 2016YFD0300502) and National Natural Science Foundation of China (No. 31571602 and No. 31871566) for its financial support to this research project.
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Zakari, S.A., Asad, MAU., Han, Z. et al. Relationship of Nitrogen Deficiency-Induced Leaf Senescence with ROS Generation and ABA Concentration in Rice Flag Leaves. J Plant Growth Regul 39, 1503–1517 (2020). https://doi.org/10.1007/s00344-020-10128-x
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DOI: https://doi.org/10.1007/s00344-020-10128-x