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Overexpression of S-adenosylmethionine synthetase 1 enhances tomato callus tolerance to alkali stress through polyamine and hydrogen peroxide cross-linked networks

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Abstract

S-adenosylmethionine synthetase is a member of the stress-induced family genes. Our previous research indicated that overexpression of SlSAMS1 confers alkali stress tolerance to tomato seedlings. However, information regarding the alkali stress tolerance mechanism of SlSAMS1 and the cross-linked network between SlSAMS1 and downstream signal has been limited. To study how SlSAMS1 improves alkali stress tolerance, we manipulated the SlSAMS1 transgenic calluses through a pharmacological approach and found that overexpression of SlSAMS1 was positively correlated with polyamine (PA) and hydrogen peroxide (H2O2) accumulation leading to improve alkali stress tolerance. Additionally, the accumulation of H2O2 in SlSAMS1 overexpression calluses depended on polyamine oxidase activity. The activities of antioxidant system, accumulation of organic acid, Na+ detoxification as well as alkali stress tolerance of the SlSAMS1 transgenic calluses were reversed by PA biosynthesis inhibitors, but not significantly influenced by ethylene biosynthesis inhibitors. These results suggest that overexpression of SlSAMS1 enhances alkali stress tolerance through PA and H2O2 cross-linked networks, which provide new insight into how SlSAMS1 functions as a stress mediatory element in regulating plants tolerance to alkali stress.

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References

  • Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645

    Article  CAS  PubMed  Google Scholar 

  • 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 231:1237–1249

    Article  PubMed  Google Scholar 

  • Anoop VM, Basu U, McCammon MT, McAlister-Henn L, Taylor GJ (2003) Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant Physiol 132:2205–2217

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Asina MJ, Villalta I, Aly MM, Olías R, Morales PÁD, Huertas R, Li J, Jaime-Pérez N, Haro R, Raga V, Carbonell EA, Belver A (2013) Two closely linked tomato HKT coding genes are positional candidates for the major tomato QTL involved in Na+/K+ homeostasis. Plant Cell Environ 36:1171–1191

    Article  Google Scholar 

  • Bhattacharjee S (2012) An inductive pulse of hydrogen peroxide pretreatment restores redox-homeostasis and oxidative membrane damage under extremes of temperature in two rice cultivars. Plant Growth Regul 68:395–410

    Article  CAS  Google Scholar 

  • Capone C, Cervelli M, Angelucci E, Colasanti M, Macone A, Mariottini P, Persichini T (2013) A role for spermine oxidase as a mediator of reactive oxygen species production in HIV-Tat-induced neuronal toxicity. Free Radic Biol Med 63:99–107

    Article  CAS  PubMed  Google Scholar 

  • Cessna SG, Sears VE, Dickman MB, Low PS (2000) Oxalic acid; a pathogenicity factor for Sclerotinia sclerotiorum; suppresses the oxidative burst of the host plant. Plant Cell 12:2191–2199

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chao YY, Hsu YT, Kao CH (2009) Involvement of glutathione in heat shock and hydrogen peroxide-induced cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Soil 318:37–45

    Article  CAS  Google Scholar 

  • Chen GH, Liu CP, Chen SCG, Wang LC (2012) Role of Arabidopsis A-fifteen in regulating leaf senescence involves response to reactive oxygen species and is dependent on ethylene insensitive 2. J Exp Bot 63:275–292

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88

    Article  CAS  PubMed  Google Scholar 

  • Confalonieri M, Balestrazzi A, Bisoffi S, Carbonera D (2003) In vitro culture and genetic engineering of Populus spp.: synergy for forest tree improvement. Plant Cell Tissue Organ 73:109–138

    Article  Google Scholar 

  • Delhaize E, Hebb DM, Ryan PR (2001) Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125:2059–2067

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Espartero J, Pintor-Toro JA, Pardo JM (1994) Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol Biol 25:217–227

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanism of acclamatory stress tolerance and signaling. Physiol Plant 100:241–254

    Article  CAS  Google Scholar 

  • Frendo P, Baldacci-Cresp F, Benyamina SM, Puppo A (2013) Glutathione and plant response to the biotic environment. Free Radic Biol Med 65:724–730

    Article  CAS  PubMed  Google Scholar 

  • Gao ZX, Wehner TC, Chen H, Lin Y, Wang XF, Wei M, Yang FJ, Shi QH (2013) Deciphering the possible mechanism of exogenous NO alleviating alkali stress on cucumber leaves by transcriptomic analysis. Sci Hortic 150:377–386

    Article  CAS  Google Scholar 

  • Garufi A, Visconti S, Camoni L, Aducci P (2007) Polyamines as physiological regulators of 14-3-3 interaction with the plant plasma membrane H+-ATPase. Plant Cell Physiol 48:434–440

    Article  CAS  PubMed  Google Scholar 

  • Gong B, Wen D, VandenLangenberg K, Wei M, Yang F, Shi Q, Wang X (2013) Comparative effects of NaCl and NaHCO3 stress on photosynthetic parameters, nutrient metabolism, and the antioxidant system in tomato leaves. Sci Hortic 157:1–12

    Article  CAS  Google Scholar 

  • Gong B, Li X, VandenLangenberg KM, Wen D, Sun S, Wei M, Li Y, Yang F, Shi Q, Wang X (2014) Overexpression of S-adenosyl-l-methionine synthetase increased tomato tolerance to alkali stress through polyamine metabolism. Plant Biotechnol J 12:694–708

    Article  CAS  PubMed  Google Scholar 

  • Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Bioch 48:540–546

    Article  CAS  Google Scholar 

  • Harpaz-Saad S, Yoon GM, Mattoo AK, Kieber JJ (2012) The formation of ACC and competition between polyamines and ethylene for SAM. Ann Plant Rev 44:53–81

    CAS  Google Scholar 

  • Hsieh TH, Li CW, Su RC, Cheng CP, Tsai SYC, Chan MT (2010) A tomato bZIP transcription factor; SlAREB; is involved in water deficit and salt stress response. Planta 231:1459–1473

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Zhang Y, Shi Y, Zhang Z, Zou Z, Zhang H, Zhao J (2012) Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity–alkalinity mixed stress. Plant Physiol Biochem 57:200–209

    Article  CAS  PubMed  Google Scholar 

  • Hua Y, Zhang BX, Cai H, Li Y, Bai X, Ji W, Wang ZY, Zhu YM (2012) Stress-inducible expression of GsSAMS2 enhances salt tolerance in transgenic Medicago sativa. Afr J Biotechnol 11:4030–4038

    CAS  Google Scholar 

  • Iannone MF, Rosales EP, Groppa MD, Benavides MP (2013) H2O2 involvement in polyamine-induced cell death in tobacco leaf discs. J Plant Growth Regul 32:745–757

    Article  CAS  Google Scholar 

  • Ishibashi Y, Yamaguchi H, Yuasa T, Iwaya-Inoue M, Arima S, Zheng SH (2011) Hydrogen peroxide spraying alleviates drought stress in soybean plants. J Plant Physiol 168:1562–1567

    Article  CAS  PubMed  Google Scholar 

  • Jonak C, Okresz L, Bogre L, Hirt H (2002) Complexity; cross talk and integration of plant MAP kinase signaling. Curr Opin Plant Biol 5:415–424

    Article  CAS  PubMed  Google Scholar 

  • Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413

    Article  PubMed  Google Scholar 

  • Kawalleck P, Plcsch G, Hahlbrock K, Somssish I (1992) Induction by fungal elicitor of S-adenosyl-l-methiorrine synthase and S-adenosyl-l-homocysteine hydrolase mRNAs in cultured cells and leaves of Petroselinum crispum. PNAS 89:4713–4717

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Krishnamurthy K (1991) Amelioration of salinity effect in salt tolerant rice (Oryza sativa L.) by foliar application of putrescine. Plant Cell Physiol 32:699–703

    CAS  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    Article  CAS  PubMed  Google Scholar 

  • Li CZ, Jiao J, Wang GX (2004) The important roles of reactive oxygen species in the relationship between ethylene and polyamines in leaves of spring wheat seedlings under root osmotic stress. Plant Sci 166:303–315

    Article  CAS  Google Scholar 

  • Liang Y, Strelkov E, Kav NNV (2009) Oxalic acid-mediated stress responses in Brassica napus L. Proteomics 9:3156–3173

    Article  CAS  PubMed  Google Scholar 

  • Liao WB, Huang GB, Yu JH, Zhang ML (2012) Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development. Plant Physiol Biochem 58:6–15

    Article  CAS  PubMed  Google Scholar 

  • Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1326

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Y, Shi Y, Song Y, Wang T, Li Y (2010) Characterization of a stress-induced NADP-isocitrate dehydrogenase gene in maize confers salt tolerance in Arabidopsis. J Plant Biol 53:107–112

    Article  CAS  Google Scholar 

  • Mailloux RJ, Harper ME (2011) Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic Biol Med 51:1106–1115

    Article  CAS  PubMed  Google Scholar 

  • Mehta RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life. Nat Biotechnol 20:613–618

    Article  CAS  PubMed  Google Scholar 

  • Minocha R, Long S (2004) Effects of aluminum on organic acid metabolism and secretion by red spruce cell suspension cultures and the reversal of Al effects on growth and polyamine metabolism by exogenous organic acids. Tree Physiol 24:55–64

    Article  CAS  PubMed  Google Scholar 

  • Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10:339–346

    Article  CAS  PubMed  Google Scholar 

  • Ndayiragije A, Lutts S (2006) Exogenous putrescine reduces sodium and chloride accumulation in NaCl-treated calli of the salt-sensitive rice cultivar I Kong Pao. Plant Growth Regul 48:51–63

    Article  CAS  Google Scholar 

  • Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Olías R, Eljakaoui Z, Li J, Morales PAD, Marín-Manzano MC, Pardo JM, Belver A (2009) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ 32:904–916

    Article  PubMed  Google Scholar 

  • Orellana S, Yañez M, Espinoza A, Verdugo I, González E, Ruiz-Lara S, Casaretto JA (2010) The transcription factor SlAREB1 confers drought; salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant Cell Environ 33:2191–2280

    Article  CAS  PubMed  Google Scholar 

  • Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot 57:1181–1199

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Poduslo JF, Curran GL (1996) Increased permeability of superoxide dismutase at the blood-nerve and blood-brain barriers with retained enzymatic activity after covalent modification with the naturally occurring polyamine, putrescine. J Neurochem 67:734–741

    Article  CAS  PubMed  Google Scholar 

  • Qi YC, Wang FF, Zhang H, Liu WQ (2010) Overexpression of Suadea salsa S-adenosylmethionine synthetase gene promotes salt tolerance in transgenic tobacco. Acta Physiol Plant 32:263–269

    Article  CAS  Google Scholar 

  • Quinet M, Ndayiragije A, Lefèvre I, Lambillote B, Dupont-Gillain CC, Lutts S (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61:2719–2733

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rodríguez AA, Maiale SJ, Menèndez AB, Ruiz OA (2009) Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress. J Exp Bot 60:4249–4262

    Article  PubMed  Google Scholar 

  • Roje S (2006) S-Adenosyl-l-methionine: beyond the universal methyl group donor. Phytochemistry 67:1686–1698

    Article  CAS  PubMed  Google Scholar 

  • Roussos PA, Pontikis CA (2007) Changes of free; soluble conjugated and bound polyamine titers of jojoba explants under sodium chloride salinity in vitro. J Plant Physiol 164:895–903

    Article  CAS  PubMed  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:1360–1385

    Article  Google Scholar 

  • Sánchez-Aguayo I, Rodríguez-Galán JM, García R, Torreblanca J, Pardo JM (2004) Salt stress enhances xylem development and expression of S-adenosyl-l-methionine synthase in lignifying tissues of tomato plants. Planta 220:278–285

    Article  PubMed  Google Scholar 

  • Shabala S, Cuin TA, Pottosin II (2007) Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999

    Article  CAS  PubMed  Google Scholar 

  • Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription; translation; and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shu S, Guo SR, Sun J, Yuan LY (2012) Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine. Physiol Plant 146:285–296

    Article  CAS  PubMed  Google Scholar 

  • Shu S, Yuan LY, Guo SR, Sun J, Yuan YH (2013) Effects of exogenous spermine on chlorophyll fluorescence; antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiol Biochem 63:209–216

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Li L, Liu M, Wang M, Ding M, Deng S, Lu C, Zhou X, Shen X, Zheng X, Chen S (2010) Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tissue Organ 103:205–215

    Article  CAS  Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    Article  CAS  PubMed  Google Scholar 

  • Taubert D, Breitenbach T, Lazar A, Censarek P, Harlfinger S, Berkels R, Klaus W, Roesen R (2003) Reaction rate constants of superoxide scavenging by plant antioxidants. Free Radic Biol Med 35:1599–1607

    Article  CAS  PubMed  Google Scholar 

  • Terui Y, Ohnuma M, Hiraga K, Kawashima E, Oshima T (2005) Stabilization of nucleic acids by unusual polyamines produced by an extreme thermophile, Thermus thermophilus. Biochem J 388:427–433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tesfaye M, Temple SJ, Allan DL, Vance CP, Samac DA (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiol 127:1836–1844

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Venema K, Belver A, Marín-Manzano MC, Rodríguez-Rosales MP, Donaire JP (2003) A novel intracellular K+/H+ antiporter related to Na+/H+ antiporters is important for K+ ion homeostasis in plants. J Biol Chem 278:22453–22459

    Article  CAS  PubMed  Google Scholar 

  • Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376:1–14

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang H, Liang X, Huang J, Zhang D, Lu H, Liu Z, Bi Y (2010) Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. Plant Cell Physiol 51:1754–1765

    Article  CAS  PubMed  Google Scholar 

  • Watson MB, Malmberg RL (1996) Regulation of Arabidopsis thaliana (L.) heynh arginine decarboxylase by potassium deficiency stress. Plant Physiol 111:1077–1084

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wimalasekera R, Tebartz F, Scherer GFE (2011) Polyamines; polyamine oxidases and nitric oxide in development; abiotic and biotic stresses. Plant Sci 181:593–603

    Article  CAS  PubMed  Google Scholar 

  • Yang CW, Chong JN, Kim CM, Li CY, Shi DC, Wang DL (2007) Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294:263–276

    Article  CAS  Google Scholar 

  • Yao YX, Dong QL, Zhai H, You CX, Hao YJ (2011) The functions of an apple cytosolic malate dehydrogenase gene in growth and tolerance to cold and salt stresses. Plant Physiol Biochem 49:257–264

    Article  CAS  PubMed  Google Scholar 

  • Zepeda-Jazo I, Shabala S, Chen Z, Pottosin II (2008) Na+–K+ transport in roots under salt stress. Plant Signal Behav 3:401–403

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang Z, Collinge DB, Thordal-Christensen H (1995) Germin-like oxalate oxidase; a H2O2-producing enzyme; accumulates in barley attacked by the powdery mildew fungus. Plant J 8:139–145

    Article  CAS  Google Scholar 

  • Zhang WP, Jiang BA, Li WG, Song H, Yu YS, Chen JF (2009) Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. Sci Hortic 122:200–208

    Article  CAS  Google Scholar 

  • Zhao FG, Song CP, He JQ, Zhu H (2007) Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145:1061–1072

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31372059); the Excellent Young Scientist Foundation of Shandong Province (No. BS2014NY005); and the Agricultural Biology Resource Innovation Project, Breeding Program of Shandong Province, China (PTBR2013).

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Authors and Affiliations

  1. State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, 271018, People’s Republic of China

    Biao Gong, Xiufeng Wang, Min Wei, Fengjuan Yang, Yan Li & Qinghua Shi

  2. Scientific Observing and Experimental Station of Environment Controlled Agricultural Engineering in Huang-Huai-Hai Region, Ministry of Agriculture, Shandong Agricultural University, Tai’an, 271018, People’s Republic of China

    Biao Gong, Xiufeng Wang, Min Wei, Fengjuan Yang, Yan Li & Qinghua Shi

  3. College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, 271018, People’s Republic of China

    Biao Gong, Xiufeng Wang, Min Wei, Fengjuan Yang, Yan Li & Qinghua Shi

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  1. Biao Gong
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Correspondence to Qinghua Shi.

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Gong, B., Wang, X., Wei, M. et al. Overexpression of S-adenosylmethionine synthetase 1 enhances tomato callus tolerance to alkali stress through polyamine and hydrogen peroxide cross-linked networks. Plant Cell Tiss Organ Cult 124, 377–391 (2016). https://doi.org/10.1007/s11240-015-0901-5

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