Abstract
Key message
Polyamines can regulate the expression of antioxidant enzymes and impart plants tolerance to abiotic stresses.
Abstract
A comparative analysis of polyamines, their biosynthetic enzymes at kinetic and at transcriptional level, and their role in regulating the induction of antioxidant defense enzymes under salt stress condition in two foxtail millet (Setaria italica L.) cultivars, namely Prasad, a salt-tolerant, and Lepakshi, a salt-sensitive cultivar was conducted. Salt stress resulted in elevation of free polyamines due to increase in the activity of spermidine synthase and S-adenosyl methionine decarboxylase enzymes in cultivar Prasad compared to cultivar Lepakshi under different levels of NaCl stress. These enzyme activities were further confirmed at the transcript level via qRT-PCR analysis. The cultivar Prasad showed a greater decrease in diamine oxidase and polyamine oxidase activity, which results in the accumulation of polyamine pools over cultivar Lepakshi. Generation of free radicals, such as O ·−2 and H2O2, was also analyzed quantitatively. A significant increase in O ·−2 and H2O2 in the cultivar Lepakshi compared with cultivar Prasad was recorded in overall pool sizes. Further, histochemical staining showed lesser accumulation of O ·−2 and of H2O2 in the leaves of cultivar Prasad than cultivar Lepakshi. Our results also suggest the ability of polyamine oxidation in regulating the induction of antioxidative defense enzymes, which involve in the elimination of toxic levels of O ·−2 and H2O2, such as Mn-superoxide dismutase, catalase and ascorbate peroxidase. The contribution of polyamines in modulating antioxidative defense mechanism in NaCl stress tolerance is discussed.
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References
Arbona V, Gomez-Cadenas A (2008) Hormonal modulation of citrus responses to flooding. J Plant Growth Regul 27:241–250
Aronova EE, Shevyakova NI, Sretsenko LA, Kuznetsov VIV (2005) Cadaverine-induced induction of superoxide dismutase gene expression in Mesembryanthemum crystallinum L. Dokklady Biol Sci 403:1–3
Bagni N, Ruiz Carrasco, Franceschetti M, Fornale S, Fornasiero RB, Tassoni A (2006) Polyamine metabolism and biosynthetic gene expression in Arabidopsis thaliana under salt stress. Plant Physiol Biochem 44:776–786. doi:10.1016/j.plaphy.2006.10.011
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140
Bose J, Pottosin I, Shabala SS, Palmgren M, Shabala S (2011) Calcium efflux systems in stress signaling and adaptation in plants. Front Plant Sci 2:85. doi:10.3389/fpls.2011.00085
Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental changes: recent developments. Plant Sci 140:103–125
Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathways in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909–9914. doi:10.1073/pnas.0306974101
Dobrovinskaya OR, Muniz J, Pottosin II (1999) Inhibition of vacuolar ion channels by polyamines. J Membr Biol 167:127–140
Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophtora infestans and the hyphal wall components. Physiol Plant Pathol 23:345–357
Gao C, Hu J, Zhang S, Zheng Y, Knapp A (2009) Association of polyamines in governing the chilling sensitivity of maize genotypes. Plant Growth Regul 57:31–38. doi:10.1007/s10725-008-9315-2
Gerard-Monnier D, Erdelmeier I, Regnard K, Moze-Henry N, Yadan JC, Chaudiere JC (1998) Reactions of 1-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Analytical applications to a colorimetric assay of lipid peroxidation. Chem Res Toxicol 11:1176–1183. doi:10.1021/tx9701790
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. doi:10.1016/j.plaphy.2010.08.016
Goyal M, Asthir B (2010) Polyamine catabolism influences antioxidative defense mechanism in shoots and roots of five wheat genotypes under high temperature stress. Plant Growth Regul 60:13–25. doi:10.1007/s10725-009-9414-8
Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45. doi:10.1007/s00726-007-0501-8
Ha HC, Woster PW, Yager JD, Casero RA (1997) The role of polyamine catabolism in analogue-induced programmed cell death. Proc Natl Acad Sci USA 94:11557–11562
Hiraga H, Ito H, Yamakawa H, Ohtsubo N, Seo S, Mitsuhara I, Matsui H, Honma M, Ohashi Y (2000) An HR-induced tobacco peroxidase gene is responsive to spermine, but not to salicylate, methyl jasmonate, and ethephone. Mol Plant Microbe Interact 13:210–216
Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573. doi:10.1104/pp.104.041699
Ioannidis NE, Kotzabasis K (2007) Effects of polyamines on the functionality of photosynthetic membrane in vivo and in vitro. Biochim Biophys Acta 1767:1372–1382. doi:10.1016/j.bbabio.2007.10.002
Ioannidis NE, Sfichi L, Kotzabasis K (2006) Putrescine stimulates chemiosmotic ATP synthesis. Biochim Biophys Acta Bioenerg 1757:821–828. doi:10.1016/j.bbabio.2007.10.002
Jaleel CA, Riadh K, Gopi R, Manivannan P, Ines J, Al-Juburi HJ, Zhao CX, Shao HB, Panneerselvam R (2009) Antioxidant defense response: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436. doi:10.1007/s11738-009-0275-6
Johnston JW, Horne S, Harding K, Benson EE (2008) Evaluation of the 1-methyl-2-phenylindole colorimetric assay for aldehydic lipid peroxidation products in plants: malondialdehyde and 4-hydroxynonenal. Plant Physiol Biochem 45:108–112. doi:10.1016/j.plaphy.2007.01.011
Katerova ZI, Todorova D (2009) Endogenous polyamines lessen membrane damages in pea plants provoked by enhanced ultraviolet-C radiation. Plant Growth Regul 57:145–152. doi:10.1007/s10725-008-9330-3
Kubis J (2008) Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves. J Plant Physiol 165:397–406. doi:10.1016/j.jplph.2007.02.005
Kuznetsov VIV, Shevyakova NI (1999) Proline under stress: biological role, metabolism, and regulation. Russ J Plant Physiol 46:274–289
Kuznetsov VIV, Shevyakova NI (2007) Polyamines and stress tolerance of plants. Plant Stress 1:50–71. doi:10.1016/j.biotechadv.2011.01.003
Larher F, Aziz A, Deleu C, Lemesle P, Ghaffa A, Bouchard F, Plasman M (1998) Suppression of the osmoinduced proline response of rapeseed leaf discs by polyamines. Physiol Plant 102:139–147. doi:10.1034/j.1399-3054.1998.1020118.x
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. doi:10.1016/j.jplph.2004.08.009
Liu J, Liu YL (2004) The relations between polyamine types and forms and polyamine oxidase activities in barley seedlings under salt stress. J Plant Physiol Mol Biol 30:141–146
Liu JH, Moriguchi T (2007) Changes in free polyamine titers and expression of polyamine biosynthetic genes during growth of peach in vitro callus. Plant Cell Rep 26:125–131. doi:10.1007/s00299-006-0223-5
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Lowry OH, Rosebrough NJ, Farr AL, Randall RL (1951) Protein measurement with the folin-phenol reagent. J Biol Chem 193:265–275
Messner B, Boll M (1994) Cell suspension cultures of spruce (Picea abies): inactivation of extra cellular enzymes by fungal elicitor-induced transient release of hydrogen peroxide. Plant Cell Tissue Organ Cult 39:69–78
Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175. doi:10.3389/fpls.2014.00175
Moschou PN, Wu J, Tavladoraki P, Angelini R, Roubelakis-Angelakis KA (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J Exp Bot 63:5003–5015. doi:10.1093/jxb/ers202
Naik BL, Goswami RG, Srivastava SK (1981) A rapid and sensitive colorimetric assay of amine oxidase. Anal Biochem 111:146–148
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Panagiotis NM, Paschalidis KA, Roubelakis-Angelakis KA (2008) Plant polyamine catabolism. Plant Signal Behav 3:1061–1066
Panicot M, Minguet EG, Ferrando A, Alcazar R, Blasquez MA, Carbonell J, Altabella T, Koncz C, Tiburcio AF (2002) A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell 14:2539–2551. doi:10.1105/tpc.004077
Paola F, Panagiotis NM, Valentina S, Raffaela T, Riccardo A, Rodolfo F, Roubelakis-Angelakis Kalliopi A, Paraskevi T (2011) Functional diversity inside the Arabidopsis polyamine oxidase gene family. J Exp Bot 62:1155–1168. doi:10.1093/jxb/erq341
Paschalidis K, Moschou PN, Toumi I, Roubelakis-Angelakis KA (2009) Polyamine anabolic/catabolic regulation along the woody grapevine plant axis. J Plant Physiol 166:1508–1519. doi:10.1016/j.jplph.2009.03.013
Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O (2014) Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot 65:1271–1283. doi:10.1093/jxb/ert423
Rea G, de Pinto MC, Tavazza R, Biondi S, Gobbi V, Ferrante P, De Gara L, Federico R, Angelini R, Tavladorak P (2004) Ectopic expression of maize polyamine oxidase and pea popper amine oxidase in the cell wall of tobacco plants. Plant Physiol 134:1414–1426. doi:10.1104/pp.103.036764
Rodriguez AA, Maiale SJ, Menendez AB, Ruiz OA (2009) Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress. J Exp Bot 60:4249–4262. doi:10.1093/jxb/erp256
Romero-Puertas CM, Rodríguez-Serrano FJ, Corpas M, Gomez LA, Del Rio L, Sandalio M (2004) Cadmium induced subcellular accumulation of O2 − and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134. doi:10.1111/j.1365-3040.2004.01217.x
Seiler N, Knodgen B (1979) Determination of the naturally occurring monoacetyl derivatives of di- and polyamines. J Chromatogr 164:155–168
Shabala S, Cuin TC, Pottosin II (2007) Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999. doi:10.1016/j.febslet.2007.04.032
Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922. doi:10.1093/treephys/tpq030
Shi H, Ye T, Chen F, Cheng Z, Wang Y, Yang P, Zhang Y, Chan Z (2013) Manipulation of arginase expression modulates abiotic stress tolerance in Arabidopsis: effect on arginine metabolism and ROS accumulation. J Exp Bot 64:1367–1379. doi:10.1093/jxb/ers400
Smith TA, Best GR (1977) Polyamines in barley seedlings. Phytochem 16:841–843
Sreenivasulu N, Ramanjulu S, Ramachandra K, Prakash SH, Sekhar Shetty H, Savithri HS, Sudhakar C (1999) Total peroxidase activity and peroxidase isoforms as modified by salt stress in two cultivars of fox-tail millet with differential salt tolerance. Plant Sci 141:1–9
Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6. doi:10.1093/aob/mcp259
Tavladoraki P, Cona A, Federico R, Tempera G, Viceconte N, Saccoccio S, Battaglia V, Toninello A, Agostinelli E (2012) Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants. Amino Acids 42:411–426. doi:10.1007/s00726-011-1012-1
Tisi A, Federico R, Moreno S, Lucretti S, Panagiotis NM, Kalliopi A, Roubelakis-Angelakis KA, Angelini R, Cona A (2011) Perturbation of polyamine catabolism can strongly affect root development and xylem differentiation. Plant Physiol 157:200–215. doi:10.1104/pp.111.173153
Tonon G, Kevers C, FaivreRampant O, Graziani M, Gaspar T (2004) Effect of NaCl and mannitol iso-osmotic stresses on proline and free polyamine levels in embryonic Fraxinus angustifolia callus. J Plant Physiol 161:701–708
Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579:1557–15564. doi:10.1016/j.febslet.2005.01.048
Veeranagamallaiah G, Chanadraobulreddy P, Jyothsnakumari G, Sudhakar C (2007) Glutamine synthetase expression and pyrroline-5-carboxylate reductase activity influence proline accumulation in two cultivars of foxtail millet (Setaria italica L.) with differential salt sensitivity. Environ Exp Bot 60:239–244. doi:10.1016/j.envexpbot.2006.10.012
Velarde-Buendía AM, Shabala S, Cultivarikrova M, Dobrovinskaya O, Pottosin I (2012) Salt-sensitive and salt-tolerant barley varieties differ in the extent of potentiation of the ROS-induced K+ efflux by polyamines. Plant Physiol Biochem 61:18–23. doi:10.1016/j.plaphy.2012.09.002
Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 162:669–677. doi:10.1016/j.jplph.2004.08.008
Walters D (2003) Resistance to plant pathogens: possible roles for free polyamines and polyamines catabolism. New Phytol 159:109–115. doi:10.1046/j.1469-8137.2003.00802.x
Wang X, Shi G, Xu Q, Hu J (2007) Exogenous polyamines enhance copper tolerance of Nymphoides peltatum. J Plant Physiol 164:1062–1070. doi:10.1016/j.jplph.2006.06.003
Wang BQ, Zhang QF, Liu JH, Li GH (2011) Overexpression of PtADC confers enhanced dehydration and drought tolerance in transgenic tobacco and tomato: effect on ROS elimination. Biochem Biophys Res Commun 413:10–16. doi:10.1016/j.bbrc.2011.08.015
Wen XP, Ban Y, Inoue H, Matsuda N, Moriguchi T (2009) Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic European pear by exerting antioxidant activities. Transgenic Res 19:91–103. doi:10.1007/s11248-009-9296-6
Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:486–490. doi:10.1016/j.bbrc.2006.11.041
Yiu JC, Liu CW, Fang DYT, Lai YS (2009) Water logging tolerance of Welsh onion (Allium fistulosum L.) enhanced by exogenous spermidine and spermine. Plant Physiol Biochem 47:710–716. doi:10.1016/j.plaphy.2009.03.007
Yoon SO, Lee YS, Lee SH, Cho YD (2000) Polyamine synthesis in plants: isolation and characterization of spermidine synthase from soybean (Glycine max) axes. Biochem Biophys Acta 1475:17–26
Zapata PJ, Serrano M, Pretel MT, Amoros A, Botella MA (2004) Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci 167:781–788. doi:10.1016/j.plantsci.2004.05.014
Zepeda-Jazo I, Velarde-Buendía AM, Enríquez-Figueroa R, Jayakumar B, Shabala S, Muñiz J et al (2011) Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Physiol 157:2167–2180. doi:10.1104/pp.111.179671
Zhao H, Yang H (2008) Exogenous polyamines alleviate the lipid peroxidation induced by cadmium chloride stress in Malus hupehensis. Rehd Sci Horti 116:442–444
Acknowledgments
We acknowledge the DST (SR/SO/PS/001/2011 and CSIR-(38/1305/11/EMR-II), GoI, New Delhi for financial assistance in the form of research grants to CS. We thank Professor T. J. Flowers, University of Sussex, Brighton, UK, for reading the manuscript and his valuable comments.
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Communicated by Manoj Prasad.
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Sudhakar, C., Veeranagamallaiah, G., Nareshkumar, A. et al. Polyamine metabolism influences antioxidant defense mechanism in foxtail millet (Setaria italica L.) cultivars with different salinity tolerance. Plant Cell Rep 34, 141–156 (2015). https://doi.org/10.1007/s00299-014-1695-3
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DOI: https://doi.org/10.1007/s00299-014-1695-3