Photosynthetica, 2018 (vol. 56), issue 4

Photosynthetica 2018, 56(4):1237-1248 | DOI: 10.1007/s11099-018-0830-8

Hydrogen peroxide in regulation of plant metabolism: Signalling and its effect under abiotic stress

T.A. Khan1, M. Yusuf2, Q. Fariduddin3,*
1 College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, China
2 Department of Biology, College of Science, United Arab Emirates University, Al Ain, Abu Dhabi, UAE
3 Plant Physiology and Biochemistry Section, Department of Botany, Aligarh Muslim University, Aligarh, India

In plants, hydrogen peroxide (H2O2) acts as a signalling molecule that facilitates various biochemical and physiological processes. H2O2 is a versatile molecule, involved in several cellular processes both under stress and stress-free conditions. In regulating plant metabolism under stress conditions, exogenous application of H2O2 also plays a pivotal role which is manifested in improved growth, photosynthetic capacity, and antioxidant protection. Abiotic stress is an inevitable environmental factor that extensively affects and reduces growth, quality, yield, and productivity of plants. Several signalling pathways involved in H2O2-mediated stress and defense responses have been extensively studied and there is ample scope of additional research that could further clarify the mechanism and modulating factors which regulate these pathways. An attempt has been made to dissect the role of H2O2 under low temperature stress and how it affects plant growth and development, photosynthetic capacity, regulation of antioxidant system, and signalling.

Keywords: antioxidants; hydrogen peroxide; low temperature; photosynthesis; reactive oxygen species; signalling

Received: July 20, 2017; Accepted: March 9, 2018; Prepublished online: December 1, 2018; Published: November 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Khan, T.A., Yusuf, M., & Fariduddin, Q. (2018). Hydrogen peroxide in regulation of plant metabolism: Signalling and its effect under abiotic stress. Photosynthetica56(4), 1237-1248. doi: 10.1007/s11099-018-0830-8.
Download citation

References

  1. Abass S.M., Mohamed H.I.: Alleviation of adverse effects of drought stress on common bean (Phaseolus vulgaris L.) by exogenous application of hydrogen peroxide.-Bangladesh J. Bot. 41: 75-83, 2011.
  2. Ahmad P., Umar S., Sharma S.: Mechanism of free radical scavenging and role of phytohormones in plants under abiotic stresses.-In: Ashraf M., Ozturk M., Ahmad M.S.A. (ed.): Plant Adaptation and Phytoremediation. Pp. 99-118. Springer, Dordrecht-Heidelberg-London-New York, Springer 2010. Go to original source...
  3. Ahmad P.: Oxidative Damage to Plants-Antioxidant Networks and Signaling. Pp. 65-88. Academic Press, Elsevier Inc., New York 2014.
  4. Anjum N.A., Sofo A., Scopa A. et al.: Lipids and proteins-major targets of oxidative modifications in abiotic stressed plants.-Environ. Sci. Pollut. R. 22: 4099-4121, 2015. Go to original source...
  5. Alscher R.G., Erturk N., Heath L.S.: Role of superoxide dismutases (SODs) in controlling oxidative stress in plants.-J. Exp. Bot. 53: 1331-1341, 2002. Go to original source...
  6. Apel K., Hirt H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction.-Annu. Rev. Plant Biol. 55: 373-399, 2004. Go to original source...
  7. Apostol I., Heinstein P.F., Low P.S.: Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: role in defense and signal transduction.-Plant Physiol. 90: 109-116, 1989. Go to original source...
  8. Ashfaque F., Khan M.I.R., Khan N.A.: Exogenously applied H2O2 promotes proline accumulation, water relations, photosynthetic efficiency and growth of wheat (Triticum aestivum L.) under salt stress.-Ann. Res. Rev. Biol. 4: 105-120, 2014. Go to original source...
  9. Ashraf M., Foolad M.R.: Roles of glycine betaine and proline in improving plant abiotic stress resistance.-Environ. Exp. Bot. 59: 206-216, 2007. Go to original source...
  10. Ashraf M.A., Rasheed R., Hussain I. et al.: Hydrogen peroxide modulates antioxidant system and nutrient relation in maize (Zea mays L.) under water-deficit conditions.-Arch. Agron. Soil Sci. 61: 207-523, 2015.
  11. Azevedo-Neto A.D., Prisco J.T., Enéas-Filho J. et al.: Hydrogen peroxide pre-treatment induces salt stress acclimation in maize plants.-J. Plant Physiol. 162: 1114-1122, 2005. Go to original source...
  12. Baier M., Noctor G., Foyer C.H. et al.: Antisense suppression of 2-cys peroxiredoxin in Arabidopsis thaliana specifically enhances the activites and expression of enzymes associated with ascorbate metabolism, but not glutathione metabolism.-Plant Physiol. 124: 823-832, 2000. Go to original source...
  13. Banu N.A., Hoque A., Watanabe-Sugimoto M. et al.: Proline and glycinebetaine induce antioxidant defense gene expression and suppress cell death in cultured tobacco cells under salt stress.-J. Plant Physiol. 166: 146-156, 2009. Go to original source...
  14. Barba-Espin G., Diaz-Vivancos P., Clemente-Moreno M.J. et al.: Interaction between hydrogen peroxide and plant hormones during germination and the early growth of pea seedlings.-Plant Cell Environ. 33: 981-994, 2010. Go to original source...
  15. Becana M., Moran J., Iturbe-Ormaetxe I.: Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection.-Plant Soil 201: 137-147, 1998. Go to original source...
  16. Bhattacharjee S.: An inductive pulse of hydrogen peroxide pretreatment restores redox homeostasis and mitigates oxidative membrane damage under extremes of temperature in two rice cultivars (Oryza sativa L., cultivars Ratna and SR 26B).-Plant Growth Regul. 68: 395-410, 2012. Go to original source...
  17. Bhattacharyya S., Das B., Ghose T.K. et al.: Investigation on seed germination of Nyctanthes arbour-tristis (Oleraceae) in relation to the phenol content.-Seed Sci. Tech. 27: 321-327, 1999.
  18. Burdon R.H., Alliangana D., Gill V.: Hydrogen peroxide and the proliferation of BHK-21 cell.-Free Radic. Res. 23: 471-486, 1995. Go to original source...
  19. Cao Y.Y., Gao Y., Sun W.J. et al.: Role of hydrogen peroxide pretreatment in heat-induced alteration of DNA methylation in cucumber leaves.-Sci. Hortic.-Amsterdam 151: 173-183, 2013.
  20. Capone R., Tiwari B.S., Levine A.: Rapid transmission of oxidative and nitrosative stress signals from roots to shoots in Arabidopsis.-Plant Physiol. Bioch. 42: 425-428, 2004. Go to original source...
  21. Carol R.J., Dolan L.: The role of reactive oxygen species in cell growth: lessons from root hairs.-J. Exp. Bot. 57: 1829-1834, 2006.
  22. Çavusoglu K., Kabar K.: Effects of hydrogen peroxide on the germination and early seedling growth of barley under NaCl and high temperature stresses.-EurAsian J. Biol. Sci. 4: 70-79, 2010.
  23. Chien C.T., Lin T.P.: Mechanism of hydrogen peroxide in improving the germination of Cinnamonum camphora seed. -Seed Sci. Tech. 22: 231-236, 1994.
  24. Chen X.Y., Ding X., Xu S. et al.: Endogenous hydrogen peroxide plays a positive role in the upregulation of heme oxygenase and acclimation to oxidative stress in wheat seedling leaves.-J. Integr. Plant Biol. 51: 951-960, 2009. Go to original source...
  25. Cheng Y., Song C.: Hydrogen peroxide homeostasis and signaling in plant cells.-Sci. China C Life Sci. 49: 1-11, 2006.
  26. Cheng X.X., Yu M., Zhang N. et al.: Reactive oxygen species regulate programmed cell death progress of endosperm in winter wheat (Triticum aestivum L.) under waterlogging.-Protoplasma 253: 311-327, 2015.
  27. Das K., Roychoudhury A.: Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants.-Front. Environ. Sci. 2: 53, 2014.
  28. Deng X.P., Cheng Y.J., Wu X.B. et al.: Exogenous hydrogen peroxide positively influences root growth and exogenous hydrogen peroxide positively influences root growth and metabolism in leaves of sweet potato seedlings.-Aust. J Crop. Sci. 6: 1572-1578, 2012.
  29. Desikan R., Hancock J.T., Neill S.J.: Oxidative stress signalling.-In: Hirt H., Shinozaki K. (ed.): Plant Responses to Abiotic Stress. Topics in Current Genetics. Pp. 121-149, Springer, Berlin, Heidelberg, 2003.
  30. Desikan R.S., Mackerness A.H., Hancock J.T. et al.: Regulation of the Arabidopsis transcriptome by oxidative stress.-Plant Physiol. 127: 159-172, 2001. Go to original source...
  31. Dietz K.J., Mittler R., Noctor G.: Recent progress in understanding the role of reactive oxygen species in plant cell signaling.-Plant Physiol. 171: 1535-1539, 2016. Go to original source...
  32. Dunand C., Crevecoeur M., Penel C.: Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases.-New Phytol. 174: 332-341, 2007. Go to original source...
  33. Fan Y., Huang Y.: The effective peroxidase-like activity of chitosan-functionalized CoFe2O4 nanoparticles for chmiluminescence sensing of hydrogen peroxide and glucose.-Analyst 137: 1225-1231, 2012. Go to original source...
  34. Fariduddin Q., Khan T.A., Yusuf M.: Hydrogen peroxide mediated tolerance to copper stress in the presence of 28-homobrassinolide in Vigna radiata.-Acta Physiol. Plant. 36: 2767-2778, 2014.
  35. Fontaine O., Huault C., Pavis N. et al.: Dormancy breakage of Hordeum vulgare seeds: Effect of hydrogen peroxide and stratification on glutathione level and glutathione reductase activity.-Plant Physiol. Bioch. 32: 677-683, 1994.
  36. Foyer C.H., Noctor G.: Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria.-Physiol. Plantarum 119: 355-364, 2003 Go to original source...
  37. Foyer C.H., Noctor G.: Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context.-Plant Cell Environ. 28: 1056-1071, 2005. Go to original source...
  38. Foyer C.H., Souriau N., Perret S. et al.: Over-expression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and improved photosynthesis in poplar (Populus tremula× P. alba) trees.-Plant Physiol. 109: 1047-1057, 1995. Go to original source...
  39. Fukao T., Bailey-Serres J.: Plant responses to hypoxia-is survival a balancing act.-Trends Plant Sci. 9: 449-456, 2004. Go to original source...
  40. Gao Y., Guo Y.K., Lin S.H. et al.: Hydrogen peroxide pretreatment alters the activity of antioxidant enzymes and protects chloroplast ultrastructure in heat stressed cucumber leaves.-Sci. Hortic.-Amsterdam 126: 20-26, 2010.
  41. Ge X.M., Cai H.L., Lei X. et al.: Heterotrimeric G protein mediates ethylene-induced stomatal closure via hydrogen peroxide synthesis in Arabidopsis.-Plant J. 82: 138-150, 2015. Go to original source...
  42. Gechev T., Gadjev I., van Breusegem F. et al.: Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes.-Cell Mol. Life Sci. 59: 708-714, 2002. Go to original source...
  43. Gechev T.S., Hille J.: Hydrogen peroxide as a signal controlling plant programmed cell death.-J. Cell Biol. 8: 17-20, 2005. Go to original source...
  44. Gill S.S., Tuteja N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.-Plant Physiol. Bioch. 48: 909-930, 2010. Go to original source...
  45. Gondim F.A., Gomes-Filho E., Costa J.H. et al.: Catalase plays a key role in salt stress acclimation induced by hydrogen peroxide pretreatment in maize.-Plant Physiol. Bioch. 56: 62-71, 2012. Go to original source...
  46. Gondim F.A., Miranda R.S., Gomes-Filho E. et al.: Enhanced salt tolerance in maize plants induced by H2O2 leaf spraying is associated with improved gas exchange rather than with nonenzymatic antioxidant system.-Theor. Exp. Plant Physiol. 25: 251-260, 2013. Go to original source...
  47. Gong M., Chen B., Li Z.G. et al.: Heat-shock-induced cross adaptation to heat, chilling, drought and salt stress in maize seedlings and involvement of H2O2.-J. Plant Physiol. 158: 1125-1130, 2001. Go to original source...
  48. González A., de los Ángeles Cabrera M., Henríquez M.J. et al.: Cross talk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess.-Plant Physiol. 158: 1451-1462, 2012. Go to original source...
  49. Grant J.J., Yun B.W., Loake G.J.: Oxidative burst and cognate redox signaling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity.-Plant J. 24: 569-582, 2000. Go to original source...
  50. Guzel S., Terzi R.: Exogenous hydrogen peroxide increases dry matter production, mineral content and level of osmotic solutes in young maize leaves and alleviates deleterious effects of copper stress.-Bot. Stud. 54: 26, 2013. Go to original source...
  51. Hasan S.A., Irfan M., Masrahi Y.S. et al.: Growth, photosynthesis, and antioxidant response of Vigna unguiculata L. treated with hydrogen peroxide.-Cogent Food Agri. 2: 1155331, 2016. Go to original source...
  52. He L., Gao Z., Li R.: Pretreatment of seed with H2O2 enhances drought tolerance of wheat (Triticum aestivum L.) seedlings.-Afr. J. Biotech. 8: 6151-6157, 2009.
  53. Hernández J.A., Ferrer M.A., Jiménez A. et al.: Antioxidant systems and O2-/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins.-Plant Physiol. 127: 817-831, 2001. Go to original source...
  54. Hernández-Barrera A., Velarde-Buendía A., Zepeda I. et al.: Hyper, a hydrogen peroxide sensor, indicates the sensitivity of the Arabidopsis root elongation zone to aluminum treatment.-Sensors 15: 855-867, 2015. Go to original source...
  55. Hippeli S., Elstner E.F.: Mechanisms of oxygen activation during plant stress: biochemical effects of air pollutants.-J. Plant Physiol. 148: 249-257, 1996. Go to original source...
  56. Holländer-Czytko J., Grabowski I., Sandorf K. et al.: Tocopherol content and activities of tyrosine aminotransferase and cystine lyase in Arabidopsis under stress conditions.-J. Plant Physiol. 162: 767-770, 2005. Go to original source...
  57. Holmberg N., Bülow L.: Improving stress tolerance in plants by gene transfer.-Trends Plant Sci. 3: 61-66, 1998. Go to original source...
  58. Horling F., Lamkemeyer P., König J. et al.: Divergent light-, ascorbate-and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis.-Plant Physiol. 131: 317-325, 2003. Go to original source...
  59. Hossain M.A., Fujita M.: Hydrogen peroxide priming stimulates drought tolerance in mustard (Brassica juncea L.) seedlings.-Plant Gene Trait. 4: 109-123, 2013.
  60. Hossain M.A., Bhattacharjee S., Armin S.M. et al.: Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging.-Front. Plant Sci. 6: 420, 2015. Go to original source...
  61. Hu Y., Ge Y., Zhang C. et al.: Cadmium toxicity and translocation in rice seedlings are reduced by hydrogen peroxide pretreatment.-Plant Growth Regul. 59: 51-61, 2009. Go to original source...
  62. Hung S.H., Wang C.C., Ivanov S.V. et al.: Repetition of hydrogen peroxide treatment induces a chilling tolerance comparable to cold acclimation in mung bean.-J. Am. Soc. Hortic. Sci. 132: 770-776, 2007. Go to original source...
  63. Hung S.H., Yu C.W., Lin C.H.: Hydrogen peroxide functions as a stress signal in plants.-Bot. Bull. Acad. Sci. 46: 1-10, 2005.
  64. Iseri O.D., Körpe D.A., Sahin F.I. et al.: Hydrogen peroxide pretreatment of roots enhanced oxidative stress response of tomato under cold stress.-Acta Physiol. Plant. 35: 1905-1913, 2013.
  65. Ishibashi Y., Yamaguchi H., Yuasa T. et al.: Hydrogen peroxide spraying alleviates drought stress in soybean plants.-J. Plant Physiol. 168: 1562-1567, 2011. Go to original source...
  66. Jahan A.A., Anis M.: Changes in antioxidative enzymatic responses during acclimatization of in vitro raised plantlets of Cardiospermum halicacabum L. against oxidative stress.-J. Plant Physiol. Pathol. 4: 2, 2014. Go to original source...
  67. Jiang Y., Cheng F., Zhou Y. et al.: Hydrogen peroxide functions as a secondary messenger for brassinosteroids-induced CO2 assimilation and carbohydrate metabolism in Cucumis sativus.-J. Zhejiang Univ.-Sci. B 13: 811-823, 2012.
  68. Kamal-Eldin L.A., Appelqvist.: The chemistry and antioxidant properties of tocopherols and tocotrienols.-Lipids 31: 671-701, 1996. Go to original source...
  69. Kapoor D., Sharma R., Handa N. et al.: Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols.-Front. Environ. Sci. 3: 13, 2015. Go to original source...
  70. Karpinski S., Reynolds H., Karpinska B. et al.: Systemic signaling in response to excess excitation energy in Arabidopsis.-Science 284: 654-657, 1999. Go to original source...
  71. Karuppanapandian T., Moon J.C., Kim C. et al.: Reactive oxygen species in plants: their generation signal transduction, and scavenging mechanisms.-Aust. J. Crop Sci. 5: 709, 2011.
  72. Katzman, L.S., Taylor A.G., Langhans R.W.: Seed enhancements to improve spinach germination.-HortScience 36: 979-981, 2001. Go to original source...
  73. Khan T.A., Yusuf M., Fariduddin Q.: Seed treatment with H2O2 modifies net photosynthetic rate and antioxidant system in mung bean (Vigna radiata L. Wilczek) plants.-Israel J. Plant Sci. 62: 167-175, 2015.
  74. Khan M.I.R., Khan N.A., Masood A. et al.: Hydrogen peroxide alleviates nickel-inhibited photosynthetic responses through increase in use-efficiency of nitrogen and sulfur, and glutathione production in mustard.-Front. Plant Sci. 7: 44, 2016. Go to original source...
  75. Khandaker M.M., Boyce A.N., Osman N.: The influence of hydrogen peroxide on the growth, development and quality of wax apple (Syzygium samarangense, [Blume] Merrill & L.M. Perry var. jambu madu) fruits.-Plant Physiol. Bioch. 53: 101-110, 2012. Go to original source...
  76. Knight H., Trewavas A.J., Knight M.R.: Cold calcium signalling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation.-Plant Cell 8: 489-503, 1996. Go to original source...
  77. Knight M.R., Campbell A.K., Smith S.M. et al.: Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium.-Nature 352: 524-526, 1991. Go to original source...
  78. Kovtun Y., Chiu W.L., Tena G. et al.: Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants.-P. Natl. Acad. Sci. USA 97: 2940-2945, 2000. Go to original source...
  79. Krifka S., Hiller K.A., Spagnuolo G. et al.: The influence of glutathione on redox regulation by antioxidant proteins and apoptosis in macrophages exposed to 2-hydroxyethyl methacrylate (HEMA).-Biomaterials 33: 5177-5186, 2012. Go to original source...
  80. Kubis J., Floryszak-Wieczorek J., Arasimowicz-Jelonek M.: Polyamines induce adaptive responses in water deficit stressed cucumber roots.-J. Plant Res. 127: 151-158, 2014. Go to original source...
  81. Lamb C., Dixon R.A.: The oxidative burst in plant disease resistance.-Annu. Rev. Plant Phys. 48: 251-275, 1997. Go to original source...
  82. Larkindale J., Huang B.: Thermo tolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene.-J. Plant Physiol. 161: 405-413, 2004. Go to original source...
  83. Leshem Y., Wills R.B.H., Ku V.: Evidence for the function of the free radical gas-nitric oxide (NO) as an endogenous maturation and senescence regulating factor in higher plants.-Plant Physiol. Bioch. 36: 825-833, 1998. Go to original source...
  84. Lewis B.D., Karlin-Neumann G., Davis R.W. et al.: Ca2+-activated anion channels and membrane depolarizations induced by blue light and cold in Arabidopsis seedlings.-Plant Physiol. 114: 1327-1334, 1997. Go to original source...
  85. Li J.T., Qiu Z.B., Zhang X.W. et al.: Exogenous hydrogen peroxide can enhance tolerance of wheat seedlings to salt stress.-Acta Physiol. Plant. 33: 835-842, 2011.
  86. Liao W.B., Huang G.B., Yu J.H. et al.: Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development.-Plant Physiol. Bioch. 58: 6-15, 2012. Go to original source...
  87. Lin Q., Chen Y., Wang Z. et al.: Study on the possibility of hydrogen peroxide pretreatment and plant system to remediate soil pollution.-Chemosphere 57: 1439-1447, 2004.
  88. Liu X., Xing D., Li L. et al.: Rapid determination of seed vigor based on the level of superoxide generation during early imbibitions.-Photoch. Photobio. Sci. 6: 767-774, 2007. Go to original source...
  89. Liu X.M., Kim K.E., Kim K.C. et al.: Cadmium activates Arabidopsis MPK3 and MPK6 via accumulation of reactive oxygen species.-Phytochemistry 71: 614-618, 2010. Go to original source...
  90. Lum H.K., Butt Y.K.C., Lo S.C.L.: Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus).-Nitric Oxide 6: 205-213, 2002. Go to original source...
  91. Ma F., Wang L.J., Li J.L. et al.: Interaction between HY1 and H2O2 in auxin-induced lateral root formation in Arabidopsis.-Plant Mol. Biol. 85: 49-61. 2014. Go to original source...
  92. May M.J., Vernoux T., Leaver C. et al.: Glutathione homeostasis in plants: implications for environmental sensing and plant development.-J. Exp. Bot. 49: 649-667, 1998. Go to original source...
  93. Mittler R., Vanderauwera S., Gollery M. et al.: Reactive oxygen gene network of plants.-Trends Plant Sci. 9: 490-498, 2004. Go to original source...
  94. Mittler R.: Oxidative stress, antioxidants and stress tolerance.-Trends Plant Sci. 7: 405-410, 2002. Go to original source...
  95. Mittler R., Vanderauwera S., Suzuki N. et al.: ROS signaling: the new wave?-Trends Plant Sci. 16: 300-309, 2011. Go to original source...
  96. Mittler R.: Abiotic stress, the field environment and stress combination.-Trends Plant Sci. 11: 15-19, 2006. Go to original source...
  97. Monroy A.F., Dhindsa R.S.: Low temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25ºC.-Plant Cell 7: 321-331, 1995.
  98. Morita S., Kaminaka H., Masumura T. et al.: Induction of rice cytosolic ascorbate peroxidase mRNA by oxidative stress: the involvement of hydrogen peroxide in oxidative stress signalling.-Plant Cell Physiol. 40: 417-422, 1999. Go to original source...
  99. Mostofa M.G., Seraj Z.I., Fujita M.: Exogenous sodium nitroprusside and glutathione alleviate copper toxicity by reducing copper uptake and oxidative damage in rice (Oryza sativa L.) seedlings.-Protoplasma 251: 1373-1386, 2014. Go to original source...
  100. Müller K., Linkies A., Vreeburg R.A.M. et al.: In vivo cell wall loosening by hydroxyl radicals during cross seed germination and elongation growth.-Plant Physiol. 150: 1855-1865, 2009. Go to original source...
  101. Nahar K., Hasanuzzaman M., Alam M.M. et al.: Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system.-Environ. Exp. Bot. 112: 44-54, 2015. Go to original source...
  102. Neill S.J., Desikan R., Clarke A. et al.: Hydrogen peroxide and nitric oxide as signalling molecules in plants.-J. Exp. Bot. 53: 1237-1247, 2002. Go to original source...
  103. Neill S.J., Desikan R., Hancock J.: Hydrogen peroxide signaling.-Curr. Opin. Plant Biol. 5: 388-395, 2002.
  104. Noctor G., Foyer C.: Ascorbate and GSH: keeping active oxygen under control.-Annu. Rev. Plant Phys. 49: 249-279, 1998. Go to original source...
  105. Noctor G., Mhamdi A., Foyer C.H.: The roles of reactive oxygen metabolism in drought: not so cut and dried.-Plant Physiol. 164: 1636-1648, 2014. Go to original source...
  106. Nogues S., Baker N.R.: Effects of drought on photosynthesis in Mediterranean plants grown under enhanced UV-B radiation.-J. Exp. Bot. 51: 1309-1317, 2000. Go to original source...
  107. Ogawa K., Iwabuchi M.: A mechanism for promoting the germination of Zinnia elegans seeds by hydrogen peroxide.-Plant Cell Physiol. 42: 286-291, 2001. Go to original source...
  108. Okuda T., Matsuda Y., Yamanaka A. et al.: Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment.-Plant Physiol. 97: 1265-1267, 1991. Go to original source...
  109. Orabi S.A., Dawood M.G., Salman S.R.: Comparative study between the physiological role of hydrogen peroxide and salicylic acid in alleviating the harmful effect of low temperature on tomato plants grown under sand-ponic culture.-Sci. Agri. 9: 49-59, 2015.
  110. Oracz K., El-Maarouf-Bouteau H., Kranner I. et al.: The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signalling during germination.-Plant Physiol. 150: 494-505, 2009.
  111. Pastori G.M., Foyer C.: Common components, networks and pathways of cross-tolerance to stress. The central role of 'redox' and abscisic acid-mediated controls.-Plant Physiol. 129: 460-468, 2002. Go to original source...
  112. Payton P., Webb R., Kornyeyev D. et al.: Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activity.-J. Exp. Bot. 52: 2345-2354, 2001. Go to original source...
  113. Pei Z.M., Murata Y., Benning G. et al.: Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.-Nature 406: 731-734, 2000. Go to original source...
  114. Peng L.T., Jiang Y.M., Yang S.Z. et al.: Accelerated senescence of fresh-cut Chinese water chestnut tissues in relation to hydrogen peroxide accumulation.-J. Plant Phys. Mol. Biol. 31: 527-532, 2005.
  115. Pinhero R., Rao M., Paliyath G. et al.: Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings.-Plant Physiol. 114: 695-704, 1997. Go to original source...
  116. Polisensky D.H., Braam J.: Cold-shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels.-Plant Physiol. 111: 1271-1279, 1996. Go to original source...
  117. Prasad T., Anderson M., Martin B. et al.: Evidence for chillinginduced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide.-Plant Cell 6: 65-74, 1994a. Go to original source...
  118. Prasad T., Anderson M., Stewart C.: Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings.-Plant Physiol. 105: 619-627, 1994b. Go to original source...
  119. Ranganayakulu G.S., Veeranagamallaiah G., Sudhakar C.: Effect of salt stress on osmolyte accumulation in two groundnut cultivars (Arachis hypogaea L.) with contrasting salt tolerance.-Afr. J. Plant Sci. 12: 586-592, 2013.
  120. Ren C.G., Li X., Liu X.L. et al.: Hydrogen peroxide regulated photosynthesis in C4-pepc transgenic rice.-Plant Physiol. Bioch.-74: 218-229, 2014. Go to original source...
  121. Rizhsky L., Davletova S., Liang H., Mittler R.: The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis.-J. Biol. Chem. 279: 11736-11743, 2004. Go to original source...
  122. Roxas V.P., Smith R.K., Allen E.R. et al.: Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress.-Nat. Biotechnol. 15: 988-991, 1997. Go to original source...
  123. Roxas V.P., Lodhi S.A., Garrett D.K. et al.: Stress tolerance in transgenic tobacco seedlings that overexpress glutathione Stransferase/glutathione peroxidase.-Plant Cell Physiol. 41: 1229-1234, 2000. Go to original source...
  124. Sakamoto H., Maruyama K., Sakuma Y. et al.: Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions.-Plant Physiol. 136: 2734-2746, 2004. Go to original source...
  125. Sanders D., Brownlee C., Harper J.F.: Communicating with calcium.-Plant Cell 11: 691-706, 1999. Go to original source...
  126. Sanders D., Pelloux J., Brownlee C. et al.: Calcium at the crossroads of signalling.-Plant Cell 14: S401-S417, 2002. Go to original source...
  127. Sarath G., Hou G., Hou L.M. et al.: Reactive oxygen species, ABA and nitric oxide interactions on the germination of warmseason C4-grasses.-Planta 226: 697-708, 2007. Go to original source...
  128. Sharma P., Jha A.B., Dubey R.S. et al.: Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions.-J. Bot. 2012: 217037, 2012. Go to original source...
  129. Shi H., Wang X., Ye T. et al.: The Cysteine2/Histidine2-type transcription factor ZINC FINGER OF Arabidopsis thaliana 6 modulates biotic and abiotic stress responses by activating salicylic acid-related genes and C-REPEAT-BINDING FACTOR genes in Arabidopsis.-Plant Physiol. 165: 1367-1379, 2014. Go to original source...
  130. Sofo A., Scopa A., Nuzzaci M. et al.: Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses.-Int. J. Mol. Sci. 16: 13561-13578, 2015. Go to original source...
  131. Tanou G., Job C., Rajjou L. et al.: Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity.-Plant J. 60: 795-804, 2009. Go to original source...
  132. Tao K.L.J., Buta J.G.: Differential effects of camptothecin and interaction with plant hormones on seed germination and seedling growth.-Plant Growth Regul. 4: 219-226, 1986. Go to original source...
  133. Terzi R., Kadioglu A., Kalaycioglu E. et al.: Hydrogen peroxide pretreatment induces osmotic stress tolerance by influencing osmolyte and abscisic acid levels in maize leaves.-J. Plant Interact. 9: 559-565, 2014. Go to original source...
  134. Türkan I., Demiral T.: Recent developments in understanding salinity tolerance.-Environ. Exp. Bot. 67: 2-9, 2009. Go to original source...
  135. Uchida A., Jagendorf A.T., Hibino T. et al.: Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice.-Plant Sci. 163: 515-523, 2002. Go to original source...
  136. van Breusegem F., Dat J.F.: Reactive oxygen species in plant cell death.-Plant Physiol. 141: 384-390, 2006. Go to original source...
  137. van Camp W.: Yield enhancement genes: seeds for growth.-Curr. Opin. Biotechnol. 16: 147-153, 2005. Go to original source...
  138. Vavilala S.L., Gawde K.K., Sinha M. et al.: Programmed cell death is induced by hydrogen peroxide but not by excessive ionic stress of sodium chloride in the unicellular green alga Chlamydomonas reinhardtii.-Eur. J. Phycol. 50: 422-438, 2015. Go to original source...
  139. Verma K., Mehta S.K., Shekhawat G.S.: Nitric oxide (NO) counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species (ROS) in Brassica juncea: cross-talk between ROS, NO and antioxidant responses.-Biometals 26: 255-269, 2013. Go to original source...
  140. Wahid A., Perveen M., Gelani S. et al.: Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins.-J. Plant Physiol. 164: 283-294, 2007. Go to original source...
  141. Wahid A., Noreen A., Basra S.M.A. et al.: Priming-induced metabolic changes in sunflower (Helianthus annuus) achenes improve germination and seedling growth.-Bot. Stud. 49: 343-350, 2008.
  142. Wang C., Croft K.P.C., Järlfors U. et al.: Subcellular localization studies indicate that lipoxygenases 1 to 6 are not involved in lipid mobilization during soybean germination.-Plant Physiol. 120: 227-236, 1999. Go to original source...
  143. Wang Y., Feng H., Qu Y. et al.: The relationship between reactive oxygen species and nitric oxide in ultraviolet-Binduced ethylene production in leaves of maize seedlings.-Environ. Exp. Bot. 57: 51-61, 2006. Go to original source...
  144. Wang Y., Li J., Wang J. et al.: Exogenous H2O2 improves the chilling tolerance of manila grass and mascarene grass by activating the antioxidative system.-Plant Growth Regul. 61: 195-204, 2010. Go to original source...
  145. Wang Y., Zhang J., Li J. et al.: Exogenous hydrogen peroxide enhanced the thermotolerance of Festuca arundinacea and Lolium perenne by increasing the antioxidative capacity.-Acta Physiol. Plant. 36: 2915-2924, 2014.
  146. White P.J.: Calcium channels in higher plants.-BBABiomembranes 1465: 171-189, 2000. Go to original source...
  147. Wingate V.P.M., Lawton M.A., Lamb C.J.: Glutathione causes a massive and selective induction of plant defense genes.-Plant Physiol. 87: 206-210, 1998.
  148. Wojtyla L., Lechowska K., Kubala S. et al.: Different modes of hydrogen peroxide action during seed germination.-Front. Plant Sci. 7: 66, 2016.
  149. Xia X.J., Wang Y.J., Zhou Y.H. et al.: Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber.-Plant Physiol. 150: 801-814, 2009. Go to original source...
  150. Xing T., Higgins V.J., Blumwald E.: Race-specific elicitors of Cladosporium fulvum promote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells.-Plant Cell 9: 249-259, 1997. Go to original source...
  151. Xing Y., Jia W., Zhang J.: AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signalling in Arabidopsis.-Plant J. 54: 440-451, 2008. Go to original source...
  152. Xu F.J., Jin C.W., Liu W.J. et al.: Pretreatment with H2O2 alleviates aluminum-induced oxidative stress in wheat seedlings.-J. Integr. Plant Biol. 53: 44-53, 2011.
  153. Yang T., Poovaiah B.W.: Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin.-P. Natl. Acad. Sci. USA 99: 4097-4102, 2002. Go to original source...
  154. Yu C.W., Murphy T.M., Lin C.H.: Hydrogen peroxide-induced chilling tolerance in mung beans mediated through ABAindependent glutathione accumulation.-Funct. Plant Biol. 30: 955-963, 2003.
  155. Zeinalabedini M., Majourhat K., Hernández J.A. et al.: Breaking seed dormancy in long-term stored seeds from Iranian wild almond species.-Seed Sci. Tech. 37: 267-275, 2009. Go to original source...
  156. Zhang A., Jiang M., Zhang J. et al.: Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants.-Plant Physiol. 141: 475-487, 2006. Go to original source...
  157. Zhang J., Cui S., Li J. et al.: Protoplasmic factors, antioxidant responses, and chilling resistance in maize.-Plant Physiol. Bioch. 33: 567-575, 1995.
  158. Zhou J., Wang J., Shi K. et al.: Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants.-Plant Physiol. Bioch. 60: 141-149, 2012. Go to original source...