Abstract
Hydrogen peroxide (H2O2), an active oxygen species, is widely generated in many biological systems. The present study demonstrates that H2O2 was generated in seedling explants after the primary roots were removed, and it mediates the auxin response prior to adventitious root formation in cucumber (Cucumis sativus L. Ganfeng 8). When compared with the controls, treatment of cucumber seedling explants after primary roots removal with either 20–40 mM H2O2 or 10 μM IAA significantly increased the number of adventitious roots, and treatment with 10–50 mM H2O2 significantly increased the fresh weight of adventitious roots. The effects of H2O2 on promoting the formation and growth of adventitious roots were eliminated by 2 mM ascorbic acid, 100 U CAT or 1 μM DPI, and the effects of IAA were eliminated by 4 mM ascorbic acid, 100 U CAT or 5 μM DPI. Treatment with either 4 mM ascorbic acid or 1–5 μM DPI inhibited the formation and growth of adventitious roots, and these inhibitory effects were partly reversed by exogenous H2O2.Furthermore, a higher concentration of endogenous H2O2 was detected in seedling explants 3 h after the primary roots were removed. However, in 10 μM DPI-treated seedling explants, the concentration of endogenous H2O2 was markedly reduced by DPI. Results obtained suggest that H2O2 may function as a signaling molecule, involved in the formation and development of adventitious roots in cucumber.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- CAT:
-
Catalase
- DPI:
-
Diphenylene iodonium
- cGMP:
-
Cyclic guanosine monophosphate
- IAA:
-
Indole-3-acetic acid
- MAPK:
-
Mitogen-activated protein kinase
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate
References
Allan AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9:1559–1572
Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784
Berleth T, Sachs T (2001) Plant morphogenesis: long-distance coordination and local patterning. Curr Opin Plant Biol 4:57–62
Davies PJ (1995) The plant hormones: their nature, occurrence and function. In: Davies PJ (ed) Plant Hormones. Kluwer, Dordrecht, Netherlands, pp 1–12
DeKlerk GJ, Krieken WVD, Jong J (1999) The formation of adventitious roots: new concepts, new possibilities. In Vitro Cell Dev Biol 35:189–199
Desikan R, Hancock JT, Neill SJ (2003) Oxidative stress signaling. In: Hirt M, Shinozaki K (ed) Topics in current genetics. Springer-Verlag, UK, pp 121–150
Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cells. J Exp Bot 55:205–212
Doerner P (2000) Plant stem cells: the only constant thing is change. Curr Biol 10:201–203
Estelle M (1992) The plant hormone auxin: insight in sight. Bioessays 14:439–444
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and biology of ageing. Nature 408:239–247
Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 42:442–446
Grossmann K, Kwiatkowski J, Tresch S (2001) Auxin herbicides induce H2O2 overproduction and tissue damage in cleavers (Galium aparine L.). J Exp Bot 52:1811–1816
Houot V, Etienne P, Petitot AS, Barbier S, Blein JP, Suty L (2001) Hydrogen peroxide induces programmed cell death features in cultured tobacco BY-2 cells, in a dose-dependent manner. J Exp Bot 52:1721–1730
Larkindale J, Huang B (2005) Effects of abscisic acid, salicylic acid, ethylene and hydrogen peroxide in thermotolerance and recovery for creeping bentgrass. Plant Growth Regul 47:17–28
Lee S, Choi H, Suh S, Doo IS, Oh KY, Choi EJ, Taylor ATS, Low PS, Lee Y (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol 121:147–152
Levine A, Tenhaken R, Dixon RA, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive response. Cell 79:583–593
Matsubara C, Nishikawa Y, Yoshida Y, Takamura K (1983) A spectrophotometric method for the determination of free fatty acid in serum using acyl-coenzyme a synthetase and acyl-coenzyme a oxidase. Anal Biochem 130:128–133
Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1242
Neill SJ, Desikan R, Hancock JT (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395
Neuenschwander U, Vernooij B, Fredrich L, Uknes S, Kessmann H, Ryals J (1995) Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? Plant J 8:227–233
Noctor G, Foyer CH (1998) Ascorbate and glulathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
Orozco-Cardenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96:6553–6557
Orozco-Cardenas M, Narvaez-Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191
Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956
Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248
Pagnussat GC, Lanteri ML, Lombardo MC (2004) Nitric oxide mediates the indole acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286
Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492
Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GT, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic signaling in guard cells. Nature 406:731–734
Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol 119:849–858
Rentel M, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H (2004) OXI1 kinase is necessary for oxidative burst-mediated signaling in Arabidopsis. Nature 427:858–861
Romero-Puertas MC, Mccarthy I, Gomez M, Sandalio LM, Corpas FJ, Delrio LA, Palma JM (2004) Reactive oxygen species-mediated enzymatic systems involved in the oxidative action of 2,4-dichlorophenoxyacetic acid. Plant Cell Environ 27:1135–1148
Rout GR (2006) Effect of auxins on adventitious root development from single node cuttings of Camellia sinensis (L.) Kuntze. and associated with biochemical changes. Plant Growth Regul 48(2):111–117
Sheng YW, Jin W, Min ZY, Ya QW, Bo L, Qiong SL, Ping YL, Hua SW, Xin S (2004) Salicylic acid modulates aluminum-induced oxidative stress in roots of Cassiatora. Acta Bot Sin 46:819–828
Su GX, Zhang WH, Liu YL (2006) Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean. J Integr Plant Biol 48(4):426–432
Theologis A (1986) Rapid gene regulation by auxin. Annu Rev Plant Physiol 37:407–438
Walker L, Estelle M (1998) Molecular mechanisms of auxin action. Curr Opin Plant Biol 1:434–439
Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448
Acknowledgement
This work was supported by the National Natural Science Foundation of China (30625008 and 30570270) and the Chinese West Environmental and Ecological Science Funds (90302010). We are grateful for the editors and the anonymous reviewers for their valuable comments and help.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Li, S., Xue, L., Xu, S. et al. Hydrogen peroxide involvement in formation and development of adventitious roots in cucumber. Plant Growth Regul 52, 173–180 (2007). https://doi.org/10.1007/s10725-007-9188-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-007-9188-9