Effect of hydrogen peroxide on catalase gene expression, isoform activities and levels in leaves of potato sprayed with homobrassinolide and ultrastructural changes in mesophyll cells
José M. Almeida A B , Fernanda Fidalgo A B , Ana Confraria A B , Arlete Santos A B , Helena Pires A and Isabel Santos A B CA Institute for Molecular and Cellular Biology, University of Porto, Rua do Campo Alegre, 823, 4150-180 Porto, Portugal.
B Botany Department, School of Sciences, University of Porto, Rua do Campo Alegre, 1191, 4150-180 Porto, Portugal.
C Corresponding author. Email: isantos@ibmc.up.pt
Functional Plant Biology 32(8) 707-720 https://doi.org/10.1071/FP04235
Submitted: 11 December 2004 Accepted: 6 May 2005 Published: 3 August 2005
Abstract
The effect of hydrogen peroxide (H2O2) on catalase (CAT) isoform activities and amounts and on mRNA levels was studied in leaves from potato plants untreated and treated with homobrassinolide (HBR). Northern blot analysis revealed that 100 mm H2O2 supplied through the leaf petiole for 4 h did not induce CAT expression. In contrast, CAT1 and CAT2 responded differently to longer treatment, as CAT2 transcript levels increased markedly whereas CAT1 transcript levels remained unchanged. Western blot analysis showed disparity between the level of CAT1 transcript and CAT1 amount, which actually decreased after 28 h. CAT2 amount correlated well with transcript accumulation and CAT2 activity as visualised by zymogram analysis. H2O2 modified the relative importance of CAT isoforms. After 4 h, CAT1 was prevalent in untreated and H2O2-treated leaves. After 28 h, CAT2 was prevalent in H2O2-treated leaves; therefore, the quantified increase in total CAT activity in these leaves was due to the rise in CAT2. HBR pre-treatment increased CAT2 basal level not changing the pattern of CAT responses to H2O2, only lowering its amplitude. Even so, ultrastructural studies showed that HBR significantly reduced H2O2 negative effects on cellular sub-structures, allowing better recovery of affected structures and reducing the macroscopic injury symptoms on leaves, thus data point to a HBR protective role.
Keywords: brassinosteroids, catalase gene expression, catalase isozymes, hydrogen peroxide, oxidative stress.
Acknowledgments
The work was supported by the Fundação para a Ciência e Tecnologia (FCT, Lisboa, Portugal — project POCTI / BME / 33044 / 2000).
Anderson JA
(2002) Catalase activity, hydrogen peroxide content and thermotolerance of pepper leaves. Scientia Horticulturae 95, 277–284.
| Crossref | GoogleScholarGoogle Scholar |
Blokhina O,
Virolainen E, Fagerstedt KV
(2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91, 179–194.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Castle, J ,
Montoya, T ,
and
Bishop, GJ (2003). Selected physiological responses of brassinosteroids: a historical approach. In ‘Brassinosteroids: bioactivity and crop productivity’. pp. 45–68. (Kluwer Academic Publishers: Dordrecht)
Čiamporová, M (1989). Recovery of ultrastructure in water stressed root epidermal cells of Zea mays. In ‘Structural and functional aspects of transport in roots’. pp. 263–267. (Kluwer Academic Publishers: London)
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 Radical Research 31, S235–S241.
| PubMed |
Dat J,
Vandenabeele S,
Vranová E,
Van Montagu M,
Inzé D, Van Breusegem F
(2000) Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57, 779–795.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dat JF,
Lopez-Delgado H,
Foyer CH, Scott IM
(1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiology 116, 1351–1357.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dat JF,
Pellinen R,
Beeckman T,
Van de Cotte B,
Langebartels C,
Kangasjarvi J,
Inzé D, Van Breusegem F
(2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. The Plant Journal 33, 621–632.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Desikan R,
Reynolds A,
Hancock JT, Neill SJ
(1998) Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures. Biochemical Journal 330, 115–120.
| PubMed |
Desikan R,
Cheung M-K,
Clarke A,
Golding S,
Sagi M,
Fluhr R,
Rock C,
Hancock JT, Neill SJ
(2004) Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum.
Functional Plant Biology 31, 913–920.
| Crossref | GoogleScholarGoogle Scholar |
Doulis AG,
Debian N,
Kingston-Smith AH, Foyer CH
(1997) Differential localization of antioxidants in maize leaves. Plant Physiology 114, 1031–1037.
| PubMed |
Dutilleul C,
Garmier M,
Noctor G,
Mathieu C,
Chetrit P,
Foyer CH, de Paepe R
(2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. The Plant Cell 15, 1212–1226.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Frohman MA,
Dush MK, Martin GR
(1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proceedings of the National Academy of Sciences USA 85, 8998–9002.
Gechev T,
Gadjev I,
Van Breusegem F,
Inzé D,
Dukiandjiev S,
Toneva V, Minkov I
(2002) Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cellular and Molecular Life Sciences 59, 708–714.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Guan LM, Scandalios G
(2000) Hydrogen peroxide-mediated catalase gene expression in response to wounding. Free Radical Biology and Medicine 28, 1182–1190.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hernandez JA,
Ferrer MA,
Jiménez A,
Barceló AR, Sevilla F
(2001) Antioxidant systems and O2·– / H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiology 127, 817–831.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Karpinski S,
Reynolds H,
Karpinska B,
Wingsle G,
Creissen G, Mullineaux P
(1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis.
Science 284, 654–657.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Krishna P
(2003) Brassinosteroid-mediated stress responses. Journal of Plant Growth Regulation 22, 289–297.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kulaeva, OP ,
Burkhanova, EA ,
Fedina, AB ,
Khokhlova, VA ,
Bokebayeva, GA ,
Vorbrodt, HM ,
and
Adam, G (1991). Effect of brassinosteroids on protein synthesis and plant-cell ultrastructure under stress conditions. In ‘Brassinosteroids: chemistry, bioactivity, and applications’. pp. 141–155. (American Chemical Society: Washington)
Levine A,
Tenhaken R,
Dixon R, Lamb C
(1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583–593.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lopez-Delgado H,
Dat JF,
Foyer CH, Scott IM
(1998) Induction of thermotolerance in potato microplants by acetylsalicylic acid and H2O2. Journal of Experimental Botany 49, 713–720.
| Crossref | GoogleScholarGoogle Scholar |
Mazorra LM,
Nunez M,
Hechavarria M,
Coll F, Sanchez-Blanco MJ
(2002) Influence of brassinosteroids on antioxidant enzymes activity in tomato under different temperatures. Biologia Plantarum 45, 593–596.
| Crossref | GoogleScholarGoogle Scholar |
Morita S,
Kaminaka H,
Masumura T, Tanaka K
(1999) Induction of rice cytosolic ascorbate peroxidase mRNA by oxidative stress; the involvement of hydrogen peroxide in oxidative stress signalling. Plant and Cell Physiology 40, 417–422.
Müssig C, Altmann T
(1999) Physiology and molecular mode of action of brassinosteroids. Plant Physiology and Biochemistry 37, 363–372.
| Crossref | GoogleScholarGoogle Scholar |
Nakashita H,
Yasuda M,
Nitt T,
Asami T,
Fujioka S,
Arai Y,
Sekimata K,
Takatsuto S,
Yamaguchi I, Yoshida S
(2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. The Plant Journal 33, 887–898.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Neill S,
Desikan R, Hancock J
(2002a) Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388–395.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Neill SJ,
Desikan R,
Clarke A,
Hurst RD, Hancock JT
(2002b) Hydrogen peroxide and nitric oxide as signalling molecules in plants. Journal of Experimental Botany 53, 1237–1247.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Noailles M-C
(1978) Étude ultrastructurale de la récupération hydrique après une période de sécheresse cez une hypnobryale: Pleurozium schreberi (Willd.) Mitt. Annales des Sciences Naturelles — Botanique et Biologie Végétale 19, 249–265.
Núñez M,
Mazzafera P,
Mazorra LM,
Siqueira WJ, Zullo MAT
(2003) Influence of a brassinosteroid analogue on antioxidant enzymes in rice grown in culture medium with NaCl. Biologia Plantarum 47, 67–70.
| Crossref | GoogleScholarGoogle Scholar |
Oksanen E,
Sober J, Karnosky DF
(2001) Impacts of elevated CO2 and / or O3 on leaf ultrastructure of aspen (Populus tremuloids) and birch (Betula papyrifera) in the Aspen FACE experiment. Environmental Pollution 115, 437–446.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Özdemir F,
Bor M,
Demiral T, Türkan Ï
(2004) Effects of 24-epibrassinolide on seed germination, seedling growth, lipid peroxidation, proline content and antioxidative system of rice (Oryza sativa L.) under salinity stress. Plant Growth Regulation 42, 203–211.
| Crossref | GoogleScholarGoogle Scholar |
Pääkkönen E,
Günthardt-Georg M, Holopainen T
(1998) Responses of leaf processes in a sensitive birch (Betula pendula Roth) clone to ozone combined with drought. Annals of Botany 82, 45–59.
| Crossref |
Polidoros AN, Scandalios JG
(1999) Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L.). Physiologia Plantarum 106, 112–120.
| Crossref | GoogleScholarGoogle Scholar |
Prasad TK,
Anderson MD,
Martin BA, Stewart CR
(1994a) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen-peroxide. The Plant Cell 6, 65–74.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Prasad T,
Anderson M, Steward C
(1994b) Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiology 105, 619–627.
| PubMed |
Rao MV,
Paliyath G, Ormrod DP
(1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana.
Plant Physiology 110, 125–136.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Salema R, Brandão I
(1973) The use of PIPES buffer in the fixation of plant cells for electron microscopy. Journal Submicroscopy Cytolology 5, 317–329.
Sam O,
Núñez M,
Ruiz-Sánchez MC,
Dell’amico J,
Falcón V,
De La Rosa MC, Seoane J
(2001) Effect of a brassinosteroid analogue and high temperature stress on leaf ultrastructure of Lycopersicon esculentum.
Biologia Plantarum 44, 213–218.
| Crossref | GoogleScholarGoogle Scholar |
Sambrook, J ,
Fritsch, EF ,
and
Maniatis, T (1989).
Santos I,
Fidalgo F,
Almeida JM, Salema R
(2004) Biochemical and ultrastructural changes in leaves of potato plants grown under supplementary UV-B radiation. Plant Science 167, 925–935.
| Crossref | GoogleScholarGoogle Scholar |
Scandalios, JG ,
Guan, L ,
and
Polidoros, AN (1997). Catalases in plants: gene structure, properties, regulation and expression. In ‘Oxidative stress and the molecular biology of antioxidant defenses’. pp. 343–406. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY)
Stefanowska M,
Kuras M, Kacperska A
(2002) Low temperature-induced modifications in cell ultrastructure and localization of phenolics in winter oilseed rape (Brassica napus L. var. oleifera L.) leaves. Annals of Botany 90, 637–645.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Uchida A,
Jagendorf AT,
Hibino T,
Takabe T, Takabe T
(2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science 163, 515–523.
| Crossref | GoogleScholarGoogle Scholar |
Van Breusegem F,
Vranova E,
Dat JF, Inzé D
(2001) The role of active oxygen species in plant signal transduction. Plant Science 161, 405–414.
| Crossref | GoogleScholarGoogle Scholar |
Vandenabeele S,
Van Der Kelen K,
Dat J,
Gadjev I, Boonefaes T ,
et al
.
(2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proceedings of the National Academy of Sciences USA 100, 16113–16118.
| Crossref | GoogleScholarGoogle Scholar |
Vardhini BV, Rao SSR
(2003) Amelioration of osmotic stress by brassinosteroids on seed germination and seedling growth of three varieties of sorghum. Plant Growth Regulation 41, 25–31.
| Crossref | GoogleScholarGoogle Scholar |
Vranová E,
Atichartpongkul S,
Villarroel R,
Van Montagu M,
Inzé D, Van Camp W
(2002) Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proceedings of the National Academy of Sciences USA 99, 10 870–10 875.
| Crossref | GoogleScholarGoogle Scholar |
Wang Z-Y, He J-X
(2004) Brassinosteroid signal transduction — choices of signals and receptors. Trends in Plant Science 9, 91–96.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Willekens H,
Chamnongpol S,
Davey M,
Schraudner M,
Langebartels C,
Van Montagu M,
Inzé D, Van Camp W
(1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO Journal 16, 4806–4816.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Willekens H,
Langebartels C,
Tire C,
Van Montagu M,
Inzé D, Van Camp W
(1994a) Differential expression of catalase genes in Nicotiana plumbaginifolia (L.). Proceedings of the National Academy of Sciences USA 91, 10 450–10 454.
Willekens H,
Van Camp W,
Van Montagu M,
Inzé D,
Sandermann H, Langebartels C
(1994b) Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia (L.). Plant Physiology 106, 1007–1014.
| PubMed |
Willekens H,
Villarroel R,
Van Montagu M,
Inzé D, Van Camp W
(1994c) Molecular identification of catalases from Nicotiana plumbaginifolia (L.). FEBS Letters 352, 79–83.
| Crossref | GoogleScholarGoogle Scholar | PubMed |