Endogenous salicylic acid accumulation is required for chilling tolerance in cucumber (Cucumis sativus L.) seedlings

Planta

Volumn 240, Issue 4, 2014, Pages 687-700

  Dong, Chun Juan ^a   Li, Liang ^a   Shang, Qing Mao ^a   Liu, Xin Yan ^a   Zhang, Zhi Gang ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Chilling; Cucumis sativus; Hydrogen peroxide; Inhibitor; Salicylic acid

Indexed keywords

ALPHA-AMINOOXY-BETA-PHENYLPROPIONIC ACID; ANTIOXIDANT; CHLOROPHYLL; HYDROGEN PEROXIDE; PACLOBUTRAZOL; PHENYLALANINE; PHENYLALANINE AMMONIA LYASE; PHYTOHORMONE; SALICYLIC ACID; TRIAZOLE DERIVATIVE; VEGETABLE PROTEIN;

ANALOGS AND DERIVATIVES; COLD; CUCUMBER; DRUG EFFECTS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SEEDLING;

ANTIOXIDANTS; CHLOROPHYLL; COLD TEMPERATURE; CUCUMIS SATIVUS; HYDROGEN PEROXIDE; PHENYLALANINE; PHENYLALANINE AMMONIA-LYASE; PLANT GROWTH REGULATORS; PLANT PROTEINS; SALICYLIC ACID; SEEDLING; STRESS, PHYSIOLOGICAL; TRIAZOLES;

EID: 84907698567     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-014-2115-1     Document Type: Article

References (58)

1. Adams-Phillips L, Briggs AG, Bent AF (2010) Distribution of poly(ADP-ribosyl) action mechanisms alters responses of Arabidopsis to biotic stress. Plant Physiol 152:267–280
2. Bandurska H, Stroiński A (2005) The effect of salicylic acid on barley response to water deficit. Acta Physiol Plant 27:379–386
3. 3 and 2S, 3S paclobutrazol. J Exp Bot 41:715–722
4. Dat JF, Foyer CH, Scott IM (1998) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118:1455–1461
5. Dean JV, Mohammed LA, Fitzpatrick T (2005) The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta 221:287–296
6. Dempsey DMA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156
7. Ding CK, Wang CY, Gross KC, Smith DL (2002) Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 214:895–901
8. Durrant WE, Dong XN (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
9. Gémes K, Poór P, Horváth E, Kolbert Z, Szopko D, Szepesi A, Tari I (2011) Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiol Plant 142:179–192
10. Ghai N, Setia RC, Setia N (2002) Effects of paclobutrazol and salicylic acid on chlorophyll content, hill activity and yield components in Brassica napus L. (cv. GSL-1). Phytomorphol 52:83–87
11. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865
12. Hu S, Jiang H, Li Y (2013) Effects of PAL and ICS on the production of total flavonoids, daidzein and puerarin in Pueraria thomsonii Benth. suspension cultures under low light stress. J Plant Biochem. doi:10.1007/s13562-013-0233-7
13. Jakab G, Ton J, Flors V, Zimmerli L, Métraux JP, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267–274
14. Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180
15. Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576
16. Kawai-Yamada M, Ohori Y, Uchimiya H (2004) Dissection of Arabidopsis Bax Inhibitor-1 suppressing bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell 16:21–32
17. Kim Y, Park S, Gilmour SJ, Thomashow MF (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low temperature transcriptome and freezing tolerance of Arabidopsis. Plant J 75:364–376
18. Kosova K, Prasil IT, Vitamvas P, Dobrev P, Motyka V, Flokova K, Novak O, Tureckova V, Rolcik J, Pesek B, Travnickova A, Gaudinova A, Galiba G, Janda T, Vlasakova E, Prasilova P, vankova R (2012) Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol 169:567–576
19. Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak SS, Bressan RA, Haseqawa PM, Yun DJ (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90
20. Lee S, Kim SG, Park CM (2010) Salicylic acid promotes seed germination under high salinity by modulating antioxidant activity in Arabidopsis. New Phytol 188:626–637
21. León J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108:1673–1678
22. Li J, Besseau S, Toronen P, Siparit N, Kollist H, Holm L, Palva ET (2013) Defense-related transcription factors WRKY70 and WRKY54 modulate osmotic stress tolerance by regulating stomatal aperture in Arabidopsis. New Phytol 200:457–472
23. Liu HT, Liu YY, Pan QH, Yang HR, Zhan JC, Huang WD (2006) Novel interrelationship between salicylic acid, abscisic acid, and PIP2-specific phospholipase C in heat acclimation-induced thermotolerance in pea leaves. J Exp Bot 57:3337–3347
24. Martinez CA, Loureiro ME, Oliva MA, Maestri M (2001) Differential responses of superoxide dismutase in freezing resistant Solanum curtilobum and freezing sensitive Solanum tuberosum subjected to oxidative and water stress. Plant Sci 160:505–515
25. Min YK, Asami T, Fujioka S, Murofushi N, Yamaguchi I, Yoshida S (1999) New lead compounds for brassinosteroids biosynthesis inhibitors. Bioorg Med Chem Lett 9:425–430
26. Miura K, Ohta M (2010) SIZ1, a small ubiquitin-related modifier ligase, controls cold signaling through regulation of salicylic acid accumulation. J Plant Physiol 167:555–560
27. Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:4
28. Miura K, Jin JB, Lee Y, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19:1403–1414
29. Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J 49:79–90
30. Munné-Bosch S, Penuelas J (2003) Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta 217:758–766
31. Pál M, Horváth E, Janda T, Páldi E, Szalai G (2005) Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays) plants. Physoil Plant 125:356–364
32. Pál M, Szalai G, Kovács V, Gondor OK, Janda T (2013) Salicylic acid-mediated abiotic stress tolerance. In: Ahmad A, Alyemeni MN, Hayat S (eds) Salicylic acid. Springer, Netherlands, pp 183–247
33. Pan Q, Zhan J, Liu H, Zhang J, Chen J, Wen P, Huang W (2006) Salicylic acid synthesized by benzoic acid 2-hydroxylase participates in the development of thermotolerance in pea plants. Plant Sci 171:226–233
34. Pan H, Wang Y, Zhang Y, Zhou T, Fang C, Nan P, Wang X, Li X, Wei Y, Chen J (2008) Phenylalanine ammonia lyase functions as a switch directly controlling the accumulation of calycosin and calycosin-7-O-beta-d-glucoside in Astragalus membranaceus var. mongholicus plants. J Exp Bot 59:3027–3037
35. Petrov VD, Van Breusegem F (2012) Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants 2012:pls014
36. Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT (1999) The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell 11:1695–1708
37. Ren CG, Dai CC (2012) Jasmonic acid is involved in the signaling pathway for fungal endophyte-induced volatile oil accumulation of Atractylodes lancea plantlets. BMC Plant Biol 12:128
38. Sawada H, Shim I-S, Usui K (2006) Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis: modulation by salt stress in rice seedlings. Plant Sci 171:263–270
39. Scott IM, Clarke SM, Wood JE, Mur LAJ (2004) Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 135:1040–1049
40. Senaratna T, Touchell D, Bunn E, Dixon K (2000) Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:157–161
41. Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physoil 151:275–289
42. Shang QM, Li L, Dong CJ (2012) Multiple tandem duplication of the phenylalanine ammonia-lyase genes in Cucumis sativus L. Planta 236:1093–1105
43. Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51
44. Tasgin E, Atici O, Nalbantoglu B (2003) Effects of salicylic acid and cold on freezing tolerance in winter wheat leaves. Plant Growth Regul 41:231–236
45. Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105
46. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194
47. Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M, Epple P, Kuhns C, Sureshkumar S, Schwartz C, Lanz C, Laitinen RA, Huang Y, Chory J, Lipka V, Borevitz JO, Dangl JL, Bergelson J, Nordborg M, Weigel D (2010) Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465:632–636
48. Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant-environment interaction. Arabidopsis Book 8:e0140
49. Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206
50. Wan SB, Tian L, Tian RR, Pan QH, Zhan JC, Wen PF, Chen JY, Zhang P, Wang W, Huang WD (2009) Involvement of phospholipase D in the low temperature acclimation-induced thermotolerance in grape berry. Plant Physiol Biochem 47:504–510
51. Wang LJ, Li SH (2006) Thermotolerance and related antioxidant enzyme activities induced by heat acclimation and salicylic acid in grape (Vitis vinifera L.) leaves. Plant Growth Regul 48:137–144
52. Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14
53. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–571
54. Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in Brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814
55. Yang Y, Qi M, Mei C (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919
56. Yuasa T, Ichimura K, Mizoguchi T, Shinozaki K (2001) Oxidative stress activates ATMPK6, an Arabidosis homologue of MAP kinase. Plant Cell Physiol 42:1012–1016
57. Zhang WP, Jiang B, Lou LN, Lu MH, Yang M, Chen JF (2011) Impact of salicylic acid on the antioxidant enzyme system and hydrogen peroxide production in Cucumis sativus under chilling stress. Z Naturforsch C 66:413–422
58. Zhou X, Zhong JJ (2011) Intracellular salicylic acid is involved in signal cascade regulating low ammonium-induced taxoid biosynthesis in suspension cultures of Taxus chinensis. Appl Microbiol Biotechnol 90:1027–1036