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

Plant Cell, Tissue and Organ Culture

Volumn 124, Issue 2, 2016, Pages 377-391

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

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Alkali stress; Hydrogen peroxide; Polyamine; SlSAMS1; Tomato callus

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; DETOXIFICATION; ETHYLENE; FRUITS; OXIDATION; PEROXIDES;

ANTIOXIDANT SYSTEMS; BIOSYNTHESIS INHIBITORS; CROSS-LINKED NETWORKS; ETHYLENE BIOSYNTHESIS; POLYAMINES; S-ADENOSYLMETHIONINE SYNTHETASE; SLSAMS1; TOMATO CALLUS;

HYDROGEN PEROXIDE;

EID: 84955338550     PISSN: 01676857     EISSN: 15735044     Source Type: Journal    
DOI: 10.1007/s11240-015-0901-5     Document Type: Article

References (77)

1. 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
2. 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
3. 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
4. + homeostasis. Plant Cell Environ 36:1171–1191
5. 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
6. 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
7. 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
8. 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
9. 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
10. 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
11. 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
12. 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
13. 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
14. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18
15. 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
16. 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
17. 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
18. +-ATPase. Plant Cell Physiol 48:434–440
19. 3 stress on photosynthetic parameters, nutrient metabolism, and the antioxidant system in tomato leaves. Sci Hortic 157:1–12
20. 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
21. Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Bioch 48:540–546
22. 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
23. 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
24. 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
25. 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
26. 2 involvement in polyamine-induced cell death in tobacco leaf discs. J Plant Growth Regul 32:745–757
27. 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
28. 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
29. Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413
30. 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
31. 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
32. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381
33. 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
34. Liang Y, Strelkov E, Kav NNV (2009) Oxalic acid-mediated stress responses in Brassica napus L. Proteomics 9:3156–3173
35. 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
36. 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
37. 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
38. Mailloux RJ, Harper ME (2011) Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic Biol Med 51:1106–1115
39. 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
40. 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
41. 2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724
42. Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10:339–346
43. 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
44. Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395
45. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
46. + between plant organs. Plant Cell Environ 32:904–916
47. 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
48. 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
49. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
50. 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
51. 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
52. 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
53. 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
54. Roje S (2006) S-Adenosyl-l-methionine: beyond the universal methyl group donor. Phytochemistry 67:1686–1698
55. 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
56. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:1360–1385
57. 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
58. + efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999
59. +-ATPase. Plant Physiol 138:287–296
60. 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
61. 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
62. + homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tissue Organ 103:205–215
63. 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
64. 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
65. 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
66. 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
67. + ion homeostasis in plants. J Biol Chem 278:22453–22459
68. Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376:1–14
69. 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
70. Watson MB, Malmberg RL (1996) Regulation of Arabidopsis thaliana (L.) heynh arginine decarboxylase by potassium deficiency stress. Plant Physiol 111:1077–1084
71. Wimalasekera R, Tebartz F, Scherer GFE (2011) Polyamines; polyamine oxidases and nitric oxide in development; abiotic and biotic stresses. Plant Sci 181:593–603
72. 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
73. 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
74. + transport in roots under salt stress. Plant Signal Behav 3:401–403
75. 2-producing enzyme; accumulates in barley attacked by the powdery mildew fungus. Plant J 8:139–145
76. 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
77. + homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145:1061–1072