Skip to main content
SpringerLink
Log in

Heme oxygenase up-regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Ultraviolet-B (UV-B) radiation has a negative impact on plant cells, and leads to the generation of reactive oxygen species (ROS). Heme oxygenase (HO, EC 1.14.99.3) plays a protective role against oxidative stress in mammals, but little is known about this issue in plants. Here, we report for the first time the response of HO in leaves of soybean (Glycine max L.) plants subjected to UV-B radiation. Under 7.5 and 15 kJ m−2 UV-B doses, HO, catalase (CAT, EC 1.11.1.6) and ascorbate peroxidase (APX, EC 1.11.1.11) activities were increased and the production of thiobarbituric acid reactive substances (TBARS) regain control values after 4 h of plant recuperation. Treatment with 30 kJ m−2 UV-B provoked a decrease in these antioxidant enzyme activities. Immunoblot analysis showed a 4.3 and 3.7-fold increase in HO-1 protein expression after irradiation with 7.5 and 15 kJ m−2, respectively. HO-1 transcript levels were enhanced (up to 77%) at these doses, as assessed by semi-quantitative RT-PCR. These data demonstrated that increased HO activity was associated with augmented protein expression and transcript levels. Plants pre-treated with the antioxidant ascorbic acid did not show the UV-B-induced up-regulation of HO-1 mRNA, but hydrogen peroxide treatment could mimic this reaction. Our results indicate that HO is up-regulated in a dose-depending manner as a mechanism of cell protection against oxidative damage and that such response occurred as a consequence of HO-1 mRNA enhancement involving ROS.

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

Similar content being viewed by others

Abbreviations

APX:

Ascorbate peroxidase

AsA:

Ascorbic acid

BV:

Biliverdin IXα

CAT:

Catalase

CPDs:

Cyclobutane pyridimine dimers

HO:

Heme oxygenase

ROS:

Reactive oxygen species

TBARS:

Thiobarbituric acid reactive substances

UV-B:

Ultraviolet-B

References

  • A-H-Mackerness S, Thomas B, Jordan BR (1997) The effect of supplementary ultraviolet-B radiation on mRNA transcripts, translation and stability of chloroplast proteins and pigment formation in Pisum sativum L. J Exp Bot 48:729–738

    Article  Google Scholar 

  • A-H-Mackerness S, Surplus SL, Blake P, John CF, Buchanan-Wollaston V, Jordan BR, Thomas B (1999) Ultraviolet-B-induced stress and changes in gene expression in Arabidopsis thaliana: role of signalling pathways controlled by jasmonic acid, ethylene and reactive oxygen species. Plant Cell Environ 22:1413–1423

    Article  Google Scholar 

  • Allen DJ, McKee IF, Farage PK, Baker NR (1997) Analysis of the limitation to CO2 assimilation on the exposure of leaves of two Brassica napus cultivars to UV-B. Plant Cell Environ 20:633–640

    Article  CAS  Google Scholar 

  • Arnott T, Murphy TM (1991) A comparison of the effects of a fungal elicitor and ultraviolet radiation on ion transport and hydrogen peroxide synthesis by rose cells. Environ Exp Bot 31:209–216

    Article  Google Scholar 

  • Asada K (1992) Ascorbate peroxidase—a hydrogen peroxide scavenging enzyme in plants. Physiol Plant 85:235–241

    Article  CAS  Google Scholar 

  • Baker NR, Nogues S, Allen DJ (1997) Photosynthesis and photoinhibition. In: Lumsden PJ (ed) Plants and UV-B: responses to environmental change. Cambridge University Press, Cambridge, pp 113–134

    Google Scholar 

  • Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2005) Involvement of heme oxygenase as antioxidant defense in soybean nodules. Free Radic Res 39:145–151

    Article  PubMed  CAS  Google Scholar 

  • Baudouin E, Frendo P, Le Gleuher M, Puppo A (2004) A Medicago sativa haem oxygenase gene is preferentially expressed in root nodules. J Exp Bot 55:43–47

    Article  PubMed  CAS  Google Scholar 

  • Beligni MV, Lamattina L (1999) Nitric oxide protects against cellular damage produced by methyl viologen herbicides in potato. Nitric Oxide 3:199–208

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Britt AB, May GD (2003) Re-engineering plant gene target. Trends Plant Sci 8:90–95

    Article  PubMed  CAS  Google Scholar 

  • Caldwell MM (1971) Solar UV irradiation and the growth and development of higher plants. In: Giese AC (ed) Photophysiology, Academic, New York, pp 131–177

    Google Scholar 

  • Casati P, Walbot V (2003) Gene expression profiling in response to ultraviolet radiation in maize genotypes with varying flavonoid content. Plant Physiol 132:1739–1754

    Article  PubMed  CAS  Google Scholar 

  • Casati P, Walbot V (2004) Rapid transcriptome responses of maize (Zea mays) to UV-B in irradiated and shielded tissues. Genome Biol 5:R16

    Article  PubMed  Google Scholar 

  • Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605

    PubMed  CAS  Google Scholar 

  • Chen K, Feng H, Zhang M, Wang X (2003) Nitric oxide alleviates oxidative damage in the green alga Chlorella pyrenoidosa caused by UV-B radiation. Folia Microbiol 48:389–393

    CAS  Google Scholar 

  • Corpas FJ, Palma JM, Sandalio LM, Lopez-Huertas E, Romero-Puertas MC, Barroso JB, Del Rio LA (1999) Purification of catalase from pea leaf peroxisomes: identification of five different isoforms. Free Radic Res 31:235–241

    Article  Google Scholar 

  • Dai Q, Yan B, Huang S, Liu X, Peng S, Miranda ML, Chavez AQ, Vergara BS, Olszyk DM (1997) Response of oxidative stress defense systems in rice (Oryza sativa) leaves with supplemental UV-B radiation. Physiol Plant 101:301–308

    Article  CAS  Google Scholar 

  • Davies KJ (1986) Intracellular proteolytic systems may function as secondary antioxidant defenses: a hypothesis. Free Radic Biol Med 2:155–173

    Article  CAS  Google Scholar 

  • Davis SJ, Kurepa J, Vierstra RD (1999) The Arabidopsis thaliana HY1 locus, required for phytochrome-chromophore biosynthesis, encodes a protein related to heme oxygenases. Proc Natl Acad Sci USA 96:6541–6546

    Article  PubMed  CAS  Google Scholar 

  • Davis SJ, Hee Bhoo S, Durski AM, Walker JM, Vierstra RD (2001) The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol 126:656–669

    Article  PubMed  CAS  Google Scholar 

  • Erario MA, Gonzales S, Noriega GO, Tomaro ML (2002) Bilirubin and ferritin as protectors against hemin-induced oxidative stress in rat liver. Cell Mol Biol 48:877–884

    PubMed  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts I Kineties and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Calif Agricultural Exp Station Circular 347:1–32

    Google Scholar 

  • Izaguirre MM, Scopel AL, Baldwin IT, Ballare CL (2003) Convergent responses to stress. Solar ultraviolet-B radiation and Manduca sexta herbivory elicit overlapping transcriptional responses in field-grown plants of Nicotiana longiflora. Plant Physiol 132:1755–1767

    Article  PubMed  CAS  Google Scholar 

  • Jansen MAK, Gaba V, Greenberg BM (1998) Higher plants and UV-B radiation: balancing damage, repair and acclimatization. Trends Plant Sci 3:131–135

    Article  Google Scholar 

  • Jordan BR (1996) The effects of ultraviolet-B radiation on plants: a molecular perspective. Adv Bot Res 22:97–162

    CAS  Google Scholar 

  • Kalbin G, Ohlsson AB, Berglund T, Rydstrom J, Strid A (1997) Ultraviolet-B-radiation-induced changes in nicotinamide and glutathione metabolism and gene expression in plants. Eur J Biochem 249:465–472

    Article  PubMed  CAS  Google Scholar 

  • Keyse SM, Tyrell RM (1989) Heme oxygenase is the major 32-kDa-stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 8:99–103

    Article  Google Scholar 

  • Kyokane T, Norimizu S, Taniai H, Naito M, Takeoka S, Tsuchida E, Nimura Y, Ishimura Y, Suematsu M (2001) Carbon monoxide from heme catabolism protects against hepatobiliary dysfunction in endotoxin-treated rat liver. Gastroenterology 120:1227-1240

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Maines MD (1988) Heme oxygenase: function, multiplicity, regulatory mechanisms and clinical applications. FASEB J 2:2557–2568

    PubMed  CAS  Google Scholar 

  • Maines MD, Kappas A (1976) Studies on the mechanism of induction of heme oxygenase by cobalt and other metal ions. Biochem J 154:125–131

    PubMed  CAS  Google Scholar 

  • Maines MD, Trakshel GM, Kutty RK (1986) Characterization of two constitutive forms of rat liver microsomal heme oxygenase only one molecular species of the enzyme is inducible. J Biol Chem 261:411–419

    PubMed  CAS  Google Scholar 

  • McCoubrey WK, Huang TJ, Maines MD (1997) Isolation and characterization of a cDNA from rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 247:725–732

    Article  PubMed  CAS  Google Scholar 

  • Muramoto T, Kohchi T, Yokota A, Hwang I, Goodman HM (1999) The Arabidopsis photomorphogenic mutant HY1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11:335–348

    Article  PubMed  CAS  Google Scholar 

  • Muramoto T, Tsurui N, Terry MJ, Yokota A, Kohchi T (2002) Expression and biochemical properties of a ferredoxin-dependent heme oxygenase required for phytochrome chromophore synthesis. Plant Physiol 130:1958–1966

    Article  PubMed  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nath KA, Balla G, Vercellotti G, Balla J, Jacob HS, Levitt MD, Rosenberg ME (1992) Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 90:267–270

    Article  PubMed  CAS  Google Scholar 

  • Noriega GO, Gonzales S, Tomaro ML, Batlle AM (2002) Paraquat-generated oxidative stress in rat liver induces heme oxygenase-1 and aminolevulinic acid synthase. Free Radic Res 36:633–639

    Article  PubMed  CAS  Google Scholar 

  • Noriega GO, Balestrasse KB, Batlle A, Tomaro ML (2004) Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. Biochem Biophys Res Com 323:1003–1008

    Article  PubMed  CAS  Google Scholar 

  • Otterbein LE, Soares MP, Yamashita K, Bach FH (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449–455

    Article  PubMed  CAS  Google Scholar 

  • Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signaling. Curr Opin Plant Biol 6:379–389

    Article  PubMed  CAS  Google Scholar 

  • Rhie G, Beale SI (1994) Regulation of heme oxygenase activity in Cyanidium caldarium by light, glucose, and phycobilin precursors. J Biol Chem 269:9620–9626

    PubMed  CAS  Google Scholar 

  • Richaud C, Zabulon G (1997) The heme oxygenase gene (pbsA) in the red alga Rhodella violacea is discontinuous and transcriptionally activated during iron limitation. Proc Natl Acad Sci USA 94:11736–11741

    Article  PubMed  CAS  Google Scholar 

  • Ritz M, Thomas JC, Spilar A, Etienne AL (2000) Kinetics of photoacclimation in response to a shift to high light of the red alga Rhodella violacea adapted to low irradiance. Plant Physiol 123:1415–1425

    Article  PubMed  CAS  Google Scholar 

  • Shimasaki KI, Sakaki T, Kondo N, Sugahara K (1980) Active oxygen participation in chlorophyll destruction and lipid peroxidation in SO2-fumigated leaves of spinach. Plant Cell Physiol 21:1193–1204

    Google Scholar 

  • Smirnoff N (1998) Plant resistance to environmental stress. Curr Opin Biotechnol 9:214–219

    Article  PubMed  CAS  Google Scholar 

  • Stadtman ER (1992) Protein oxidation and aging. Science 257:1220-1224

    Article  PubMed  CAS  Google Scholar 

  • Surplus SL, Jordan BR, Murphy AM, Carr JP, Thomas B, A-H-Mackerness S (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 

  • Takahashi S, Nakajima N, Saji H, Kondo N (2002) Diurnal change of cucumber CPD photolyase gene (CsPHR) expression and its physiological role in growth under UV-B irradiation. Plant Cell Physiol 43:342–349

    Article  PubMed  CAS  Google Scholar 

  • Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61:748–755

    Article  PubMed  CAS  Google Scholar 

  • Tomaro ML, Frydman J, Frydman RB (1991) Heme oxygenase induction by Cl2Co, Co-protoporphyrin-IX, phenylhydrazine, and diamide: evidence for oxidative stress involvement. Arch Biochem Biophys 22:10–17

    Google Scholar 

  • Ulm R, Baumann A, Oravecz A, Mate Z, Adam E, Oakeley EJ, Schafer E, Nagy F (2004) Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc Natl Acad Sci USA 101:1397–1402

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. T. Kohchi for kindly providing the A. thaliana HO-1 antibodies. This work was supported by grants from the Universidad de Buenos Aires (Argentina) and from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) (Argentina). A. B. and M.L.T. are Career Investigators from CONICET.

Author information

Authors and Affiliations

  1. Departamento de Química Biológica, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Junín 956, Buenos Aires, 1113, Argentina

    Gustavo G. Yannarelli & Maria L. Tomaro

  2. Centro de Investigaciones sobre Porfirinas y Porfirias (CIPYP), CONICET, Buenos Aires, Argentina

    Guillermo O. Noriega & Alcira Batlle

Authors
  1. Gustavo G. Yannarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guillermo O. Noriega
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alcira Batlle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria L. Tomaro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gustavo G. Yannarelli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yannarelli, G.G., Noriega, G.O., Batlle, A. et al. Heme oxygenase up-regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta 224, 1154–1162 (2006). https://doi.org/10.1007/s00425-006-0297-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-006-0297-x

Keywords

Search

Navigation