Skip to main content
SpringerLink
Log in

Elevated H2O2 production via overexpression of a chloroplastic Cu/ZnSOD gene of lily (Lilium oriental hybrid ‘Marco Polo’) triggers ethylene synthesis in transgenic potato

  • Cell Biology and Morphogenesis
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Transgenic potato plants (SS2 and SS4) that overexpressed a chloroplastic copper/zinc superoxide dismutase lily gene were utilized as an H2O2-inducible system in order to study the role of H2O2 as a signaling molecule in the biosynthesis of ethylene. SS2 and SS4 plants grown in vitro under sealed microenvironment (SME) conditions displayed anomalous phenotypes including reduction of stem elongation, radial stem growth, and promotion of root hair formation in the generated root, which were similar to ethylene-induced responses. In addition, SS4 plants showed severe vitrification in developing leaves and elevated ethylene production under SME conditions. After the ethylene action inhibitor AgNO3, 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase (ACO) inhibitor CoCl2, and ACC synthase inhibitor l-aminoethoxyvinylglycine were added to the growth media, the anomalous phenotypes in SS4 plants reverted to their normal phenotype with a concurrent decrease in ethylene production. Northern blot analysis showed that ACO transcripts in SS4 plants were constantly at high levels under normal and SME conditions, indicating that a high level of H2O2 in SS4 plants up-regulates ACO transcripts. Moreover, the direct treatment of H2O2 in potato plants confirmed the elevated expression of the ACO gene. Taken together, these data suggest that the high concentration of H2O2 in transgenic potato plants stimulates ethylene biosynthesis by activating ACO gene expression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Ausubel F, Brent R, Kingston R, Moore D, Seidman JG, Smith J, Struhl K (1987) Current protocols in molecular biology. Wiley, New York

    Google Scholar 

  • Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J 9:525–535

    Article  PubMed  CAS  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    Article  PubMed  CAS  Google Scholar 

  • Callahan AM, Morgens PH, Wright P, Nichols KE (1992) Comparison of Pch313 (pTOM13 homolog) RNA accumulation during fruit softening and wounding of two phenotypically different peach cultures. Plant Physiol 100:482–488

    PubMed  CAS  Google Scholar 

  • Chamnongpol S, Willekens H, Moeder W, Langebartels C, Sandermann H, Van Montagu M, Inzé D, Van Camp W (1998) Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc Natl Acad Sci USA 95:5818–5823

    Article  PubMed  CAS  Google Scholar 

  • Dai Q, Yan B, Huang S, Liu X, Peng S, Miranda MLM, Chavez AQ, Vegara BS, Olszyk D (1997) Response of oxidative stress defence systems in rice leaves with supplementary UV-B radiation. Physiol Plant 101:301–308

    Article  CAS  Google Scholar 

  • Drew MC, Jackson MB, Giffard S (1979) Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) may be adaptive response to flooding in Zea mays L. Planta 153:217–224

    Article  Google Scholar 

  • Guis M, Bouquin T, Zegzouti H, Ayub R, Ben Amor M, Lasserre E, Botondi R, Raynal J, Latché A, Bouzayen M, Balagué C, Pech JC (1997) Differential expression of ACC oxidase genes in melon and physiological characterization of fruit expressing an antisense ACC oxidase gene. In: Kanellis A, Chang C, Kender H, Grierson D (eds) Biology and biotechnology of the plant hormone ethylene. Kluwer Academic Publishers, Dordrecht, pp 327–338

    Google Scholar 

  • Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523

    Article  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51:2053–2066

    Article  PubMed  CAS  Google Scholar 

  • Jing HC, Schippers JHM, Hille J (2005) Ethylene-induced leaf senescence depends on age-related changes and OLD genes in Arabidopsis. J Exp Bot 56:2915–2923

    Article  PubMed  CAS  Google Scholar 

  • Johnson PR, Ecker JR (1998) The ethylene gas signal transduction pathway: a molecular perspective. Annu Rev Genet 32:227–254

    Article  PubMed  CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307

    Article  CAS  Google Scholar 

  • Kevers C, Gaspar T (1985) Vitrification of carnation in vitro: changes in ethylene production, ACC level and capacity to convert to ethylene. Plant Cell Tissue Organ Cult 4:215–223

    Article  CAS  Google Scholar 

  • Kim MS, Kim HS, Kim YS, Baek KH, Oh HW, Hahn KW, Bae RN, Lee IJ, Joung H, Jeon JH (2007) Superoxide anion regulates plant growth and tuber development of potato. Plant Cell Rep 26:1717–1725

    Article  PubMed  CAS  Google Scholar 

  • Lelievre JM, Tichit L, Dao P, Fillion L, Nam YW, Pech JC, Latche A (1997) Effects of chilling on the expression of ethylene biosynthetic genes in Passe-Crassane pear (Pyrus communis L.) fruits. Plant Mol Biol 33:847–855

    Article  PubMed  CAS  Google Scholar 

  • Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C, Kangasjärvi J (2002) Ethylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiol 130:1918–1926

    Article  PubMed  CAS  Google Scholar 

  • Mori IC, Schroeder JI (2004) Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol 135:702–708

    Article  PubMed  CAS  Google Scholar 

  • Murashige T (1978) The impact of plant tissue culture on agriculture. In: Thorpe TA (eds) Frontiers of plant tissue culture. University of Calgary, Calgary, pp 15–27

    Google Scholar 

  • Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118:1295–1305

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917

    Article  PubMed  CAS  Google Scholar 

  • Oetiker JH, Olson DC, Shiu OY, Yang SF (1997) Differential induction of seven 1-aminocyclopropane-1-carboxylate synthase genes by elicitor in suspension cultures of tomato (Lycopersicon esculentum). Plant Mol Biol 34:275–286

    Article  PubMed  CAS  Google Scholar 

  • Olson DC, Oetiker JH, Yang SF (1995) Analysis of LE-ACS3, a 1-aminocyclopropane-1-carboxylic acid synthase gene expressed during flooding in the roots of tomato plants. J Biol Chem 270:14056–14061

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Park SW, Jeon JH, Kim HS, Park YM, Aswath C, Joung H (2004) Effect of sealed and vented gaseous microenvironment on hyperhydricity of potato shoots in vitro. Sci Hortic 99:199–205

    Article  Google Scholar 

  • Park JY, Kim HS, Youm JW, Kim MS, Kim KS, Joung H, Jeon JH (2006) Cloning of superoxide dismutase (SOD) gene of lily ‘Marcopolo’ and expression in transgenic potatoes. Agric Chem Biotechnol 49:1–7

    CAS  Google Scholar 

  • Pellinen R, Palva T, Kangasjärvi J (1999) Short communication: subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. Plant J 20:349–356

    Article  PubMed  CAS  Google Scholar 

  • Saab IN, Sachs MM (1996) A flooding-induced xyloglucan endo-transglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma. Plant Physiol 112:385–391

    Article  PubMed  CAS  Google Scholar 

  • Schaller GE, Kieber JJ (2002) Ethylene. In: Somerville C, Meyerowitz E (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville, pp 1579–1597

    Google Scholar 

  • Schlagnhaufer C, Arteca R, Pell E (1997) Sequential expression of two 1-aminocyclopropane-1-carboxylate synthase gene in response to biotic and abiotic stresses in potato (Solanum tuberosum L.) leaves. Plant Mol Biol 35:683–688

    Article  PubMed  CAS  Google Scholar 

  • Surplus SL, Jordan BR, Murphy AM, Carr JP, Thomas B, Mackerness SAH (1998) Ultraviolet-B-induced responses in Arabidopsis thaliana: role of salicylic acid and reactive oxygen species in the regulation of transcripts encoding photosynthetic and acidic pathogenesis-related proteins. Plant Cell Environ 21:685–694

    Article  CAS  Google Scholar 

  • Taiz L, Zerger E (2002) Plant physiology, 3rd edn. Sinauer Associates, Inc. Publishers, Sunderland

    Google Scholar 

  • Tuomainen J, Betz C, Kangasjärvi J, Ernst D, Yin ZH, Langebartels C, Sandermann H Jr (1997) Ozone induction of ethylene emission in tomato plants: regulation by differential transcript accumulation for the biosynthetic enzymes. Plant J 12:1151–1162

    Article  CAS  Google Scholar 

  • Vahala J, Schlagnhaufer CD, Pell EJ (1998) Induction of an ACC synthase cDNA by ozone in light grown Arabidopsis thaliana leaves. Physiol Plant 103:45–50

    Article  CAS  Google Scholar 

  • Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T, Morsa S, Rottiers P, Slooten L, Van Montagu M, Zabeau M, Inzé D, Van Breusegem F (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc Natl Acad Sci USA 100:16113–16118

    Article  PubMed  CAS  Google Scholar 

  • Wang CY, Adams DO (1982) Chilling-induced ethylene production in cucumbers (Cucumis sativus L.). Plant Physiol 69:424–427

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Sakai S (1998) Effects of active oxygen species and methyl jasmonate on expression of the gene for a wound-inducible 1-aminocyclopropane-1-carboxylate synthase in winter squash (Cucurbita maxima). Planta 206:570–576

    Article  CAS  Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189

    Article  CAS  Google Scholar 

  • Zarembinski TI, Theologis A (1994) Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26:1579–1597

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by grants from the KRIBB Research Initiative Program and the Plant Diversity Research Center of the 21st Century Frontier Research Program, funded by the Ministry of Science and Technology of the Korean government.

Author information

Authors and Affiliations

  1. Plant Genome Research Center, KRIBB, Yuseong, Daejeon, 305-806, South Korea

    Yoon-Sik Kim, Hyun-Soon Kim, Yong-Hwa Lee, Mi-Sun Kim, Hyouk Joung & Jae-Heung Jeon

  2. Insect Resources Research Center, KRIBB, Daejeon, 305-806, South Korea

    Hyun-Woo Oh

  3. Department of Biological Sciences, Hannam University, Daejeon, 306-791, South Korea

    Kyu-Woong Hahn

Authors
  1. Yoon-Sik Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hyun-Soon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yong-Hwa Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mi-Sun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hyun-Woo Oh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kyu-Woong Hahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hyouk Joung
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jae-Heung Jeon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jae-Heung Jeon.

Additional information

Communicated by J.R. Liu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, YS., Kim, HS., Lee, YH. et al. Elevated H2O2 production via overexpression of a chloroplastic Cu/ZnSOD gene of lily (Lilium oriental hybrid ‘Marco Polo’) triggers ethylene synthesis in transgenic potato. Plant Cell Rep 27, 973–983 (2008). https://doi.org/10.1007/s00299-008-0515-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-008-0515-z

Keywords

Search

Navigation