Overexpression of S-adenosylmethionine synthetase 1 enhances tomato callus tolerance to alkali stress through polyamine and hydrogen peroxide cross-linked networks
详细信息 查看全文
- 作者：Biao Gong ; Xiufeng Wang ; Min Wei…
- 关键词：Alkali stress ; Hydrogen peroxide ; Polyamine ; Tomato callus ; SlSAMS1
- 刊名：Plant Cell, Tissue and Organ Culture
- 出版年：2016
- 出版时间：February 2016
- 年：2016
- 卷：124
- 期：2
- 页码：377-391
- 全文大小：1,093 KB
- 参考文献：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 281:37636–37645CrossRef PubMed
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 231:1237–1249CrossRef PubMed
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 132:2205–2217PubMedCentral CrossRef PubMed
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 36:1171–1191CrossRef
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 68:395–410CrossRef
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 63:99–107CrossRef PubMed
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 12:2191–2199PubMedCentral CrossRef PubMed
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 318:37–45CrossRef
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 63:275–292PubMedCentral CrossRef PubMed
Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88CrossRef PubMed
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 73:109–138CrossRef
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 125:2059–2067PubMedCentral CrossRef PubMed
Espartero J, Pintor-Toro JA, Pardo JM (1994) Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol Biol 25:217–227CrossRef PubMed
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18PubMedCentral CrossRef PubMed
Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanism of acclamatory stress tolerance and signaling. Physiol Plant 100:241–254CrossRef
Frendo P, Baldacci-Cresp F, Benyamina SM, Puppo A (2013) Glutathione and plant response to the biotic environment. Free Radic Biol Med 65:724–730CrossRef PubMed
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 150:377–386CrossRef
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 48:434–440CrossRef PubMed
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 157:1–12CrossRef
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 12:694–708CrossRef PubMed
Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Bioch 48:540–546CrossRef
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
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 231:1459–1473CrossRef PubMed
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 57:200–209CrossRef PubMed
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
Iannone MF, Rosales EP, Groppa MD, Benavides MP (2013) H2O2 involvement in polyamine-induced cell death in tobacco leaf discs. J Plant Growth Regul 32:745–757CrossRef
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 168:1562–1567CrossRef PubMed
Jonak C, Okresz L, Bogre L, Hirt H (2002) Complexity; cross talk and integration of plant MAP kinase signaling. Curr Opin Plant Biol 5:415–424CrossRef PubMed
Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413CrossRef PubMed
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 89:4713–4717PubMedCentral CrossRef PubMed
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
Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381CrossRef PubMed
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 166:303–315CrossRef
Liang Y, Strelkov E, Kav NNV (2009) Oxalic acid-mediated stress responses in Brassica napus L. Proteomics 9:3156–3173CrossRef PubMed
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 58:6–15CrossRef PubMed
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 124:1315–1326PubMedCentral CrossRef PubMed
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 53:107–112CrossRef
Mailloux RJ, Harper ME (2011) Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic Biol Med 51:1106–1115CrossRef PubMed
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 20:613–618CrossRef PubMed
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 24:55–64CrossRef PubMed
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 20:1708–1724PubMedCentral CrossRef PubMed
Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10:339–346CrossRef PubMed
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 48:51–63CrossRef
Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395CrossRef PubMed
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279CrossRef PubMed
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 32:904–916CrossRef PubMed
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 33:2191–2280CrossRef PubMed
Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot 57:1181–1199CrossRef PubMed
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45PubMedCentral CrossRef PubMed
Poduslo JF, Curran GL (1996) Increased permeability of superoxide dismutase at the blood-nerve and blood
ain barriers with retained enzymatic activity after covalent modification with the naturally occurring polyamine, putrescine. J Neurochem 67:734–741CrossRef PubMed
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 32:263–269CrossRef
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 61:2719–2733PubMedCentral CrossRef PubMed
Rodríguez AA, Maiale SJ, Menèndez AB, Ruiz OA (2009) Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress. J Exp Bot 60:4249–4262CrossRef PubMed
Roje S (2006) S-Adenosyl-l -methionine: beyond the universal methyl group donor. Phytochemistry 67:1686–1698CrossRef PubMed
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 164:895–903CrossRef PubMed
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:1360–1385CrossRef
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 220:278–285CrossRef PubMed
Shabala S, Cuin TA, Pottosin II (2007) Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999CrossRef PubMed
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 138:287–296PubMedCentral CrossRef PubMed
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 146:285–296CrossRef PubMed
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 63:209–216CrossRef PubMed
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 103:205–215CrossRef
Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270CrossRef PubMed
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 35:1599–1607CrossRef PubMed
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 388:427–433PubMedCentral CrossRef PubMed
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 127:1836–1844PubMedCentral CrossRef PubMed
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 278:22453–22459CrossRef PubMed
Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376:1–14PubMedCentral CrossRef PubMed
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 51:1754–1765CrossRef PubMed
Watson MB, Malmberg RL (1996) Regulation of Arabidopsis thaliana (L.) heynh arginine decarboxylase by potassium deficiency stress. Plant Physiol 111:1077–1084PubMedCentral CrossRef PubMed
Wimalasekera R, Tebartz F, Scherer GFE (2011) Polyamines; polyamine oxidases and nitric oxide in development; abiotic and biotic stresses. Plant Sci 181:593–603CrossRef PubMed
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 294:263–276CrossRef
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 49:257–264CrossRef PubMed
Zepeda-Jazo I, Shabala S, Chen Z, Pottosin II (2008) Na+–K+ transport in roots under salt stress. Plant Signal Behav 3:401–403PubMedCentral CrossRef PubMed
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 8:139–145CrossRef
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 122:200–208CrossRef
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 145:1061–1072PubMedCentral CrossRef PubMed - 作者单位：Biao Gong (1) (2) (3)
Xiufeng Wang (1) (2) (3)
Min Wei (1) (2) (3)
Fengjuan Yang (1) (2) (3)
Yan Li (1) (2) (3)
Qinghua Shi (1) (2) (3)
1. State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, 271018, People’s Republic of China
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
3. College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, 271018, People’s Republic of China - 刊物类别：Biomedical and Life Sciences
- 刊物主题：Life Sciences
Plant Sciences
Plant Physiology - 出版者：Springer Netherlands
- ISSN：1573-5044
文摘
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.