Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Christou, Anastasis ^a,b   Filippou, Panagiota ^a   Manganaris, George A ^a   Fotopoulos, Vasileios ^a  

^a CYPRUS UNIVERSITY OF TECHNOLOGY   (Cyprus)

^b AGRICULTURAL RESEARCH INSTITUTE   (Cyprus)

Author keywords

Ascorbic acid; Fragaria x ananassa; Heat shock proteins; Hydrogen sulfide; Nitrosative stress; Oxidative stress; Priming; Thermotolerance

Indexed keywords

ANTIOXIDANT; AQUAPORIN; ASCORBIC ACID; GLUTATHIONE; HEAT SHOCK PROTEIN; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; SODIUM BISULFIDE; SULFIDE; SUPEROXIDE DISMUTASE; VEGETABLE PROTEIN;

ARTICLE; DRUG EFFECT; FRAGARIA; GENE EXPRESSION REGULATION; HEAT; METABOLISM;

ANTIOXIDANTS; AQUAPORINS; ASCORBIC ACID; FRAGARIA; GENE EXPRESSION REGULATION, PLANT; GLUTATHIONE; HEAT-SHOCK PROTEINS; HOT TEMPERATURE; HYDROGEN PEROXIDE; PLANT PROTEINS; SULFIDES; SUPEROXIDE DISMUTASE;

EID: 84893206208     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-42     Document Type: Article

References (76)

1. Wahid A, Gelani S, Ashraf M, Foolad MR. Heat tolerance in plants: an overview. Environ Exp Bot 2007, 61:199-223.
2. Schöffl F, Prändl R, Reindl A. Regulation of the heat-shock response. Plant Physiol 1998, 117:1135-1141.
3. Allakhverdiev S, Kreslavski V, Klimov V, Los D, Carpentier R, Mohanty P. Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 2008, 98:541-550.
4. Wahid A, Close T. Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol Plantarum 2007, 51:104-109.
5. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI. Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 2007, 1767:414-421.
6. Zhang J-H, Huang W-D, Liu Y-P, Pan Q-H. Effects of temperature acclimation pretreatment on the ultrastructure of mesophyll cells in young grape plants (Vitis vinifera L. cv. Jingxiu) under cross-temperature stresses. J Integr Plant Biol 2005, 47:959-970.
7. Tan W, Meng QW, Brestic M, Olsovska K, Yang X. Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. J Plant Physiol 2011, 168:2063-2071.
8. Horvath I, Glatz A, Varvasovszki V, Balogh G, Kovacs E. Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a " fluidity gene" Proc Natl Acad Sci U S A 1998, 95:3513-3518.
9. Vinocur B, Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 2005, 16:123-132.
10. Saidi Y, Finka A, Goloubinoff P. Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol 2011, 190:556-565.
11. von Koskull-Doring P, Scharf K-D, Nover L. The diversity of plant heat stress transcription factors. Trends Plant Sci 2007, 12:452-457.
12. Ahn Y-J, Claussen K, Lynn Zimmerman J. Genotypic differences in the heat-shock response and thermotolerance in four potato cultivars. Plant Sci 2004, 166:901-911.
13. Howarth CJ. Genetic improvements of tolerance to high temperature. Abiotic Stresses: Plant Resistance Through Breeding and Molecular Approaches 2005, 277-300. New York: Howarth Press Inc, Ashraf M, Harris PJC.
14. Sung D-Y, Kaplan F, Lee KJ, Guy CL. Acquired tolerance to temperature extremes. Trends Plant Sci 2003, 8:179-187.
15. Kumar S, Kaur R, Kaur N, Bhandhari K, Kaushal N, Gupta K, Bains TS, Nayyar H. Heat-stress induced inhibition in growth and chlorosis in mungbean (Phaseolus aureus Roxb.) is partly mitigated by ascorbic acid application and is related to reduction in oxidative stress. Acta Physiol Plant 2011, 33:2091-2101.
16. Larkindale J, Huang B. Effects of abscisic acid, salicylic acid, ethylene and hydrogen peroxide in thermotolerance and recovery for creeping bentgrass. Plant Growth Regul 2005, 47:17-28.
17. Wang L-J, Fan L, Loescher W, Duan W, Liu G-J, Cheng J-S, Luo H-B, Li S-H. Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biol 2010, 10:34.
18. Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 2002, 163:515-523.
19. Wahid A, Perveen M, Gelani S, Basra SMA. Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol 2007, 164:283-294.
20. Rausch T, Wachter A. Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 2005, 10:503-509.
21. Fotopoulos V, Christou A, Manganaris GA. Hydrogen sulfide as a potent regulator of plant responses to abiotic stress factors. In Molecular Approaches in Plant Abiotic Stress 2013, 353-373. UK: CRC Press, Gaur RK, Sharma P.
22. Li Z-G. Hydrogen sulfide: a multifunctional gaseous molecule in plants. Rus J Plant Phys 2013, 60:733-740.
23. Zhang H, Tan Z-Q, Hu L-Y, Wang S-H, Luo J-P, Jones RL. Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 2010, 52:556-567.
24. Wang B-L, Shi L, Li Y-X, Zhang WH. Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 2010, 231:1301-1309.
25. Ali S, Farooq MA, Hussain S, Yasmeen T, Abbasi GH, Zhang G. Alleviation of chromium toxicity by hydrogen sulfide in barley. Environ Toxicol Chem 2013, 32:2234-2239.
26. Zhang H, Ye Y-K, Wang S-H, Luo J-P, Tang J, Ma D-F. Hydrogen sulfide counteracts chlorophyll loss in sweetpotato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 2009, 58:243-250.
27. Zhang H, Jiao H, Jiang C-X, Wang S-H, Wei Z-J, Luo J-P, Jones R. Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol Plant 2010, 32:849-857.
28. Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V. Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 2013, 64:1953-1966.
29. Zhang H, Tang J, Liu X-P, Wang Y, Yu W, Peng W-Y, Fang F, Ma D-F, Wei Z-J, Hu L-Y. Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 2009, 51:1086-1094.
30. García-Mata C, Lamattina L. Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 2010, 188:977-984.
31. Li Z-G, Gong M, Xie H, Yang L, Li J. Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 2012, 185-186:185-189.
32. Li Z-G, Yang S-Z, Long W-B, Yang G-X, Shen Z-Z. Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 2013, 36:1564-1572.
33. Li Z-G, Ding X-J, Du P-F. Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Phys 2013, 170:741-747.
34. Kadir S, Sidhu G, Al-Khatib K. Strawberry (Fragaria x ananassa Duch.) growth and productivity as affected by temperature. HortSci 2006, 41:1423-1430.
35. Rowland JG, Pang X, Suzuki I, Murata N, Simon WJ, Slabas AR. Identification of components associated with thermal acclimation of photosystem II in Synechocystis sp. PCC6803. PLoS One 2010, 5:e10511.
36. Song L, Chow WS, Sun L, Li C, Peng C. Acclimation of photosystem II to high temperature in two Wedelia species from different geographical origins: implications for biological invasions upon global warming. J Exp Bot 2010, 61:4087-4096.
37. Banti V, Mafessoni F, Loreti E, Alpi A, Perata P. The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 2010, 152:1471-1483.
38. Volkov R, Panchuk I, Mullineaux P, Schöffl F. Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 2006, 61:733-746.
39. Li L, Wang Y, Shen W. Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. BioMetals 2012, 25:617-631.
40. Wang Y, Li L, Cui W, Xu S, Shen W, Wang R. Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 2012, 351:107-119.
41. Filippou P, Antoniou C, Fotopoulos V. Effect of drought and rewatering on the cellular status and antioxidant response of Medicago truncatula plants. Plant Signal Behav 2011, 6:270-277.
42. Mur LAJ, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJM, Hebelstrup KH, Gupta KJ. Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 2013, 5:052.
43. Arasimowicz M, Floryszak-Wieczorek J. Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci 2007, 172:876-887.
44. Molassiotis A, Fotopoulos V. Oxidative and nitrosative signaling in plants: two branches in the same tree?. Plant Signal Behav 2011, 6:210-214.
45. Filippou P, Bouchagier P, Skotti E, Fotopoulos V. Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ Exp Bot 2014, 97:1-10.
46. Antoniou C, Filippou P, Mylona P, Fasoula D, Ioannides I, Polidoros A, Fotopoulos V. Developmental stage and concentration-specific sodium nitroprusside application results in nitrate reductase regulation and the modification of nitrate metabolism in leaves of Medicago truncatula plants. Plant Signal Behav 2013, 8:e25479.
47. Shapiro AD. Nitric oxide signaling in plants. Vitam Horm 2005, 72:339-398.
48. Xuan Y, Zhou S, Wang L, Cheng Y, Zhao L. Nitric oxide functions as a signal and acts upstream of AtCaM3 in thermotolerance in Arabidopsis seedlings. Plant Physiol 2010, 153:1895-1906.
49. Fotopoulos V, Ziogas V, Tanou G, Molassiotis A. Involvement of AsA/DHA and GSH/GSSG Ratios in Gene and Protein Expression and in the Activation of Defence Mechanisms Under Abiotic Stress Conditions. Ascorbate-Glutathione Pathway and Stress Tolerance in Plants 2010, 265-302. Netherlands: Springer, Anjum NA, Chan M-T, Umar S.
50. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 2010, 48:909-930.
51. Potters G, Horemans N, Jansen MAK. The cellular redox state in plant stress biology - a charging concept. Plant Physiol Biochem 2010, 48:292-300.
52. Szalai G, Kello{double acute}s T, Galiba G, Kocsy G. Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 2009, 28:66-80.
53. Shan C-J, Zhang S-L, Li D-F, Zhao Y-Z, Tian X-L, Zhao X-L, Wu Y-X, Wei X-Y, Liu R-Q. Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress. Acta Physiol Plant 2011, 33:2533-2540.
54. Shan C, Dai H, Sun Y. Hydrogen sulfide protects wheat seedlings against copper stress by regulating the ascorbate and glutathione metabolism in leaves. Aust J Crop Sci 2012, 6:248-254.
55. Wang W, Vinocur B, Shoseyov O, Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 2004, 9:244-252.
56. Yang KA, Lim CJ, Hong JK, Park CY, Cheong YH, Chung WS, Lee KO, Lee SY, Cho MJ, Lim CO. Identification of cell wall genes modified by a permissive high temperature in Chinese cabbage. Plant Sci 2006, 171:175-182.
57. Rampino P, Mita G, Pataleo S, De Pascali M, Di Fonzo N, Perrotta C. Acquisition of thermotolerance and HSP gene expression in durum wheat (Triticum durum Desf.) cultivars. Environ Exp Bot 2009, 66:257-264.
58. Xu C, Huang B. Root proteomic responses to heat stress in two Agrostis grass species contrasting in heat tolerance. J Exp Bot 2008, 59:4183-4194.
59. Zhang J-X, Wang C, Yang C-Y, Wang J-Y, Chen L, Bao X-M, Zhao Y-X, Zhang H, Liu J. The role of Arabidopsis AtFes1A in cytosolic Hsp70 stability and abiotic stress tolerance. Plant J 2010, 62:539-548.
60. Huerta C, Freire M, Cardemil L. Expression of hsp70, hsp100 and ubiquitin in Aloe barbadensis Miller under direct heat stress and under temperature acclimation conditions. Plant Cell Rep 2013, 32:293-307.
61. Luu D-T, Maurel C. Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 2005, 28:85-96.
62. Ayadi M, Cavez D, Miled N, Chaumont F, Masmoudi K. Identification and characterization of two plasma membrane aquaporins in durum wheat (Triticum turgidum L. subsp. durum) and their role in abiotic stress tolerance. Plant Physiol Biochem 2011, 49:1029-1039.
63. Johansson I, Karlsson M, Johanson U, Larsson C, Kjellbom P. The role of aquaporins in cellular and whole plant water balance. Biomembranes 2000, 1465:324-342.
64. Iglesias-Acosta M, Martínez-Ballesta MC, Teruel JA, Carvajal M. The response of broccoli plants to high temperature and possible role of root aquaporins. Environ Exp Bot 2010, 68:83-90.
65. Chen K, Arora R. Understanding the cellular mechanism of recovery from freeze-thaw injury in spinach: possible role of aquaporins, heat shock proteins, dehydrin and antioxidant system. Physiol Plant (in press), DOI: 10.1111/ppl.12090.
66. Chen J, Wu F-H, Wang W-H, Zheng C-J, Lin G-H, Dong X-J, He J-X, Pei Z-M, Zheng H-L. Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 2011, 62:4481-4493.
67. Hou Z, Wang L, Liu J, Hou L, Liu X. Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. J Integr Plant Biol 2013, 55:277-289.
68. Heath R, Packer L. Photooxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 1968, 125:189-198.
69. Zhou B, Guo Z, Xing J, Huang B. Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 2005, 56:3223-3228.
70. Loreto F, Velikova V. Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 2001, 127:1781-1787.
71. Nashef AS, Osuga DT, Feeney RE. Determination of hydrogen sulfide with 5,5β'-dithiobis-(2-nitrobenzoic acid), N-ethylmaleimide, and parachloromercuribenzoate. Anal Biochem 1977, 79:394-405.
72. Foyer C, Rowell J, Walker D. Measurement of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 1983, 157:239-244.
73. Griffith O. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 1980, 106:207-212.
74. Christou A, Georgiadou E, Filippou P, Manganaris GA, Fotopoulos V. Establishment of a rapid, inexpensive protocol for the extraction of high quality RNA from small amounts of strawberry plant tissues and other recalcitrant fruit crops. Gene 2014, 537:169-173.
75. Bustamante CA, Rosli HG, Añón MC, Civello PM, Martinez GA. β-xylosidase in strawberry fruit: isolation of a full-length gene and analysis of its expression and enzymatic activity in cultivars with contrasting firmness. Plant Sci 2006, 171:497-504.
76. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.