Do polyamines modulate the Lotus glaber NADPH oxidation activity induced by the herbicide methyl viologen?
Juan C. Cuevas A , Diego H. Sánchez A , María Marina A and Oscar A. Ruiz A BA Unidad de Biotecnología 1, Instituto Tecnológico de Chascomús / Universidad Nacional de General San Martín-Consejo Nacional de Investigaciones Científicas y Técnicas (IIB-INTECH / UNSAM-CONICET), Camino circunvalación laguna, Km. 6 CC164 (B7130IWA) Chascomús, Pcia. de Buenos Aires, Argentina.
B Corresponding author; email: ruiz@intech.gov.ar
Functional Plant Biology 31(9) 921-928 https://doi.org/10.1071/FP04007
Submitted: 13 January 2004 Accepted: 7 June 2004 Published: 27 September 2004
Abstract
In recent years, there has been a growing interest in NADPH-oxidases which are involved in the active generation of reactive oxygen species (ROS), owing to their role in oxidative burst, signalling and oxidative damage derived from biotic and abiotic stresses. NADPH oxidase activity is enhanced by some environmental cues, such as zinc deficiency and chilling stress, where zinc and polyamines have been suggested to be involved in the modulation of ROS generation. In order to further characterise NADPH oxidation activity during oxidative stress we exposed Lotus glaber Mill. (narrow-leaf trefoil; syn. L. tenuis Waldst. et Kit. ex Wild var. Miller) plants to the herbicide methyl viologen (MV) and evaluated zinc and polyamines as oxidative stress regulatory compounds. For this purpose we conducted in vitro and in vivo experiments, observing that zinc and the higher polyamines spermidine and spermine inhibited the NADPH oxidation activity in vitro while preventing methyl viologen-induced superoxide production in vivo. It is suggested that these substances act through a direct effect on flavin oxidases. However, it was not possible to correlate free polyamine content of L. glaber with their hypothetical inhibitory role during oxidative stress, probably owing to the plant’s natural tolerance to the herbicide tested. Therefore, tobacco, a more sensitive species, was tested for methyl viologen toxicity. High concentrations of methyl viologen induced free polyamine levels in crude extracts and intercellular fluids. However, only free polyamine content in the intercellular fluids was increased in plants treated with low methyl viologen concentrations. These results support the notion that polyamine metabolism in the apoplast is involved in the physiological response to oxidative stress.
Keywords: Lotus glaber, methyl viologen, NADPH oxidase, polyamines, zinc.
Acknowledgments
This work was supported by grants from the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina), The Third World Academy of Sciences (TWAS) and the Agencia Española de Cooperación Internacional (AECI). MM is a fellow of UNSAM, while DHS is a fellow of CONICET. OAR is a member of the research committee from CONICET. We thank Gabriela K. Lopez for outstanding technical assistance and to Dr Gustavo Somoza and Dr Leandro Miranda for providing histological supplies and equipment. We also thank Dr Ana Menendez for assessment and experience on botanical issues, and Dr Estela Valle for critical revision of the manuscript and helpful comments.
Allen RD
(1995) Dissection of oxidative stress tolerance using transgenics plants. Plant Physiology 107, 1–7.
| PubMed |
Asada K, Endo T, Mano J, Miyake C
(1998) Molecular mechanisms for relaxation of and protection from light stress. ‘Stress responses of photosynthetic organisms’. (Eds K Sato, N Murata)
pp. 37–52. (Elsevier Science Publishing: Amsterdam, The Netherlands)
Asada K
(1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Besford RT,
Richardson CM,
Campos JL, Tiburcio AF
(1993) Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189, 201–206.
| Crossref |
Blumenthal MJ, McGraw RL
(1999) Lotus adaptations, use and management. ‘Trefoil: the science and technology of ’. (Ed. PR Beuselinck)
pp. 97–119. (CSSA special publication 28)
Bors W,
Langebartels C,
Michel C, Sandermann H
(1989) Polyamines as radical scavengers and protectans against ozone damage. Phytochemistry 28, 1589–1595.
| Crossref | GoogleScholarGoogle Scholar |
Bouchereau A,
Aziz A,
Larher F, Martin-Tanguy J
(1999) Polyamines and environmental challenges: recent development. Plant Science 140, 103–125.
| Crossref | GoogleScholarGoogle Scholar |
Borrell A,
Carbonell L,
Farrás R,
Puig-Parellada P, Tiburcio AF
(1997) Inhibition of lipid peroxidation by polyamines in senescent oat leaves in vivo. Physiologia Plantarum 99, 385–390.
| Crossref | GoogleScholarGoogle Scholar |
Bradford MM
(1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
| Crossref |
PubMed |
Bustos DM, Iglesias AA
(2002) Non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase is post-translationally phosphorylated in heterotrophic cells of wheat (Triticum aestivum). FEBS Letters 530, 169–173.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cakmak I
(2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytologist 146, 185–205.
| Crossref | GoogleScholarGoogle Scholar |
Cakmak I, Marschner H
(1988a) Enhanced superoxide radicals production in roots of Zn-deficient plants. Journal of Experimental Botany 39, 1449–1460.
Cakmak I, Marschner H
(1988b) Zinc-dependent changes in ESR signals, NADPH oxidase and plasma membrane permeability in cotton roots. Physiologia Plantarum 73, 182–186.
Flores HE
(1991) Changes in polyamine metabolism in response to abiotic stress. ‘Biochemistry and physiology of polyamines in plants’. (Eds RD Slocum, HE Flores)
pp. 213–228. (CRC Press: Boca Raton, FL)
Foyer CH
(1997) Oxygen metabolism and electron transport in photosynthesis. ‘Oxidative stress and the molecular biology of antioxidant defenses’. (Ed. JG Scandalios)
pp. 587–621. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY)
Foyer CH,
Descourvieres P, Kunert KJ
(1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant, Cell and Environment 17, 507–523.
Hart JJ,
Ditomaso JM, Kochian LV
(1993) Characterization of paraquat transport in protoplast from maize (Zea mays L.) suspension cells. Plant Physiology 103, 963–969.
| PubMed |
He L,
Nada K,
Kasukabe Y, Tachibana S
(2002) Enhanced tolerance of photosynthesis to low-temperature photoinhibition due to interruption of chill-induced increase of S-adenosylmethionine decarboxilase activity in leaves of spinach (Spinacia olaracea L.). Plant and Cell Physiology 43, 196–206.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kaur-Sawhney R, Galston A
(1991) Physiological and biochemical studies on the anti-senescence properties of polyamines in plants. ‘Biochemistry and physiology of polyamines in plants’. (Eds RD Slocum, HE Flores)
pp. 201–211. (CRC Press: Boca Raton, FL)
Kawano T,
Kawano N,
Muto S, Lapeyrie F
(2002) Retardation and inhibition of the cation-induced superoxide generation in BY-2 tobacco cell suspension culture by Zn+2 and Mn+2. Physiologia Plantarum 114, 395–404.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Keller T,
Damude HG,
Wener D,
Doerner P,
Dixon RA, Lamb C
(1998) A plant homologue of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca+2 binding motifs. The Plant Cell 10, 255–266.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kim TE,
Kim SK,
Han TJ,
Lee JS, Chang SC
(2002) ABA and polyamines act independently in primary leaves of cold-stressed tomato (Lycopersicon esculentum). Physiologia Plantarum 115, 370–376.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kurepa J,
Smalle J,
Van Montagu M, Inzé D
(1998) Polyamines and paraquat toxicity in Arabidopsis thaliana. Plant and Cell Physiology 39, 987–992.
| PubMed |
Kwon SY,
Jeong YJ,
Lee HS,
Kim JS,
Cho KY,
Allen DR, Kwak SS
(2002) Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. Plant, Cell and Environment 25, 873–882.
| Crossref | GoogleScholarGoogle Scholar |
Laterra P
(1997) Post-burn recovery in the flooding-pampa: impact of an invasive legume. Journal of Range Management 50, 274–277.
Lichtenthaler HK
(1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
| Crossref | GoogleScholarGoogle Scholar |
Liu K,
Fu H,
Bei Q, Luan S
(2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiology 124, 1315–1326.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maiale S,
Sanchez DH,
Guirado A,
Vidal A, Ruiz OA
(2004) Spermine accumulation under salt stress. Journal of Plant Physiology 161, 35–42.
| PubMed |
Mano J,
Ohno C,
Domae Y, Asada K
(2001) Chloroplastic ascorbate peroxidase is the primary target of methylviologen-induced photo oxidative stress in spinach leaves: its relevance to monodehydroascorbate radical detected with in vivo ERS. Biochimica et Biophysica Acta 1504, 275–287.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mano J
(2002) Early events in environmental stresses in plants–induction mechanisms of oxidative stress. ‘Oxidative stress in plants’. (Eds D Inze, M Van Montagu)
pp. 217–245. (Taylor and Francis: London)
Marcé M,
Brown DS,
Capell T,
Figueras X, Tiburcio AF
(1995) Rapid high performance liquid chromatographic method for the quantitation of polyamines as their dansyl derivatives: application to plant and animal tissues. Journal of Chromatography B 666, 329–335.
| Crossref | GoogleScholarGoogle Scholar |
Medda R,
Padiglia A, Floris G
(1995) Plant copper-amine oxidases. Plant Science 39, 1–9.
| Crossref | GoogleScholarGoogle Scholar |
Mittler R
(2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Palatnik J,
Valle E, Carillo N
(1997) Oxidative stress causes ferredoxin-NADP+ reductase solubilization from the thylakoid membranes in methyl viologen-treated plants. Plant Physiology 115, 1721–1727.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Palatnik J,
Carillo N, Valle E
(1999) The role of photosynthetic electron transport in the oxidative degradation of chloroplastic glutamine synthetase. Plant Physiology 121, 471–478.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pinton R,
Cakmak I, Marschner H
(1994) Zinc deficiency enhanced NADPH-dependent superoxide radical production in plasma membrane vesicles isolated from roots of bean plants. Journal of Experimental Botany 45, 45–50.
Sebela M,
Radova A,
Angelini R,
Tavladoraki P,
Frebort I, Pec P
(2001) FAD-containing polyamine oxidases: a timely challenge for researchers in biochemistry and physiology of plants. Plant Science 160, 197–207.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shen W,
Nada K, Tachibana S
(2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiology 124, 431–439.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Slocum RD
(1991) Tissue and subcellular localization of polyamines and enzymes of polyamine metabolism in plants. ‘Biochemistry and physiology of polyamines in plants’. (Eds RD Slocum, HE Flores)
pp. 93–104. (CRC Press: Boca Raton, FL)
de Wit PJ, Spikman G
(1982) Evidence for the occurrence of race and cultivar-specific elicitors of necrosis in intercellular fluids of compatible interactions of Cladosporium fulvum and tomato. Physiological and Molecular Plant Pathology 21, 1–11.
Yamakawa H,
Kamada H,
Satoh M, Ohashi Y
(1998) Spermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against tobacco mosaic virus infection. Plant Physiology 118, 1213–1222.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ye B,
Muller HH,
Zang J, Gressel J
(1997) Constitutively elevated levels of putrescine and putrescine-generating enzymes correlated with oxidant stress resistance in Conyza bonariensis and wheat. Plant Physiology 115, 1443–1451.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yoda H,
Yamaguchi Y, Sano H
(2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiology 132, 1973–1981.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
