Abstract
Alternaria tagetica, a fungus that causes early blight in marigold (Tagetes erecta), produces two groups of phytotoxic metabolites: one hydrophilic and the other lipophilic that show phytotoxic activity when tested by the leaf-spot assay in T. erecta. We evaluated the cellular effects of the phytotoxic culture filtrate of A. tagetica and the hydrophilic and lipophilic fractions, then determined whether the filtrate or the fractions differentially induced pathogenesis-related mechanisms in the plant. The culture filtrate and the phytotoxic fractions had adverse effects on cell viability, fresh mass, and the number of cells, and induced ROS accumulation, lipid peroxidation and DNA damage on T. erecta cell suspension cultures, and these effects are related to pathogenic mechanisms attributed to phytotoxins. However, although exposure of marigold cells to the phytotoxic culture filtrate of A. tagetica triggered programmed cell death, the hydrophilic and the lipophilic phytotoxic fractions induced death that was more related to a toxic effect leading to necrosis. This study presents a complementary perspective in the search for the roles of metabolites, including phytotoxins, produced by phytopathogenic fungi during plant infection.
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References
Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM (2000) Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12:1823–1835
Bandyopadhyay U, Das D, Banerjee RK (1999) Reactive oxygen species: oxidative damage and pathogenesis. Curr Sci 77:658–666
Cotty PJ, Misaghi IJ (1984) Zinniol production by Alternaria species. Phytopathology 74:785–788
Cotty PJ, Misaghi IJ, Hine RB (1983) Production of zinniol by Alternaria tagetica and its phytotoxic effect on Tagetes erecta. Phytopathology 73:1326–1328
Dangl JL, Dietrich RA, Richberg MH (1996) Death don’t have no mercy: cell death programs in plant–microbe interactions. Plant Cell 8:1793–1807
Erdelmeier I, Gérard-Monnier D, Yadan J-C, Chaudière J (1998) Reactions of N-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Mechanistic aspects of the colorimetric assay of lipid peroxidation. Chem Res Toxicol 11:1184–1194
Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11:81–128
Gamboa-Angulo MM, Alejos-González F, Escalante-Erosa F, García-Sosa K, Delgado-Lamas G, Peña-Rodríguez LM (2000) Novel dimeric metabolites from Alternaria tagetica. J Nat Prod 63:1117–1120
Gamboa-Angulo MM, Escalante-Erosa F, García-Sosa K, Alejos-González F, Delgado-Lamas G, Peña-Rodríguez LM (2002) Natural zinniol derivates from Alternaria tagetica. Isolation, synthesis, and structure-activity correlation. J Agric Food Chem 50:1053–1058
Garcia-Medrano RME, Miranda-Ham ML (2003) Analysis of elicitor-induced cell viability changes in Lycopersicon esculentum Mill. suspension culture by different methods. In Vitro Cell Dev Biol Plant 39:236–239
Gilchrist DG (1998) Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol 36:393–414
Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757
Greenberg JT (1997) Programmed cell death in plant–pathogen interactions. Annu Rev Plant Physiol Mol Biol 48:525–545
Greenberg JT, Guo A, Klessig DF, Ausubel FM (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77:551–563
Heiser I, Oßwald W, Elstner EF (1998) The formation of reactive oxygen species by fungal and bacterial phytotoxins. Plant Physiol Biochem 36:703–713
Huang J-S (ed) (2001) Plant pathogenesis and resistance, biochemistry and physiology of plant–microbe interactions. Kluwer, Norwell
Knoche HW, Duvick JP (1987) The role of fungal toxins in plant disease. In: Pegg G, Ayres P (eds) Fungal infection of plants. Symposium of the British mycological society. Cambridge University Press, Cambridge, pp 158–192
Knogge W (1996) Fungal infection of plants. Plant Cell 8:1711–1722
Marré MT, Amicucci E, Zingarelli L, Albergoni F, Marré E (1998) The respiratory burst and electrolyte leakage induced by sulfhydryl blockers in Egeria densa leaves are associated with H2O2 production and are dependent on Ca2+ influx. Plant Physiol 118:1379–1387
Messner B, Boll M (1994) Cell suspension cultures of spruce (Picea abies): inactivation of extracellular enzymes by fungal elicitor-induced transient release of hydrogen peroxide (oxidative burst). Plant Cell Tiss Org Cult 39:69–78
Morales L (2003) Cuantificación de zinniol, tirosol y ácido p-hidroxibenzoico en cultivos de Alternaria tagetica. B.Sc. thesis, Universidad Autónoma de Yucatán, Yucatán, México (in Spanish)
Navarre DA, Wolpert TJ (1999) Victorin induction of an apoptotic/senescence-like response in oats. Plant Cell 11:237–249
Oliver RP, Solomon PS (2004) Does the oxidative stress used by plants for defense provide a source of nutrients for pathogenic fungi? Trends Plant Sci 9:472–473
Otani H, Kohomoto K, Kodama M (1995) Alternaria toxins and their effects on host plants. Can J Bot 73:453–458
Paciolla C, Dipierro N, Mulè G, Logrieco A, Dipierro S (2004) The mycotoxins beauvericin and T-2 induce cell death and alteration to the ascorbate metabolism in tomato protoplasts. Physiol Mol Plant Pathol 65:49–56
Robert ML, Herrera JL, Contreras F, Scorer KN (1987) In vitro propagation of Agave fourcroydes Lem. (Henequen). Plant Cell Tiss Org Cult 8:37–48
Street H (ed) (1977) Introduction to plant tissue and cell culture. Blackwell, London
Tada Y, Hata S, Takata Y, Nakayashiki H, Tosa Y, Mayama S (2001) Induction and signaling of an apoptotic response typified by DNA laddering in the defense response of oats to infection and elicitors. Mol Plant Microbe Interact 14:477–486
Tiedemann AV (1997) Evidence for a primary role of active oxygen species in induction of host cell death during infection of bean leaves with Botrytis cinerea. Physiol Mol Plant Pathol 50:151–166
Van Kan JAL (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247–253
Wang H, Li J, Bostock RM, Gilchrist DG (1996) Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8:375–391
Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40:251–285
Wood RKS, Ballio A, Graniti A (eds) (1972) Phytotoxins in plant diseases. Academic Press, London
Zhang HK, Zhang X, Mao BZ, Li Q, He ZH (2004) Alpha-picolinic acid, a fungal toxin and mammal apoptosis-inducing agent, elicits hypersensitive-like response and enhances disease resistance in rice. Cell Res 14:27–33
Acknowledgments
This work has been supported by the National Science and Technology Council (CONACyT, Mexico) through grant No. 54868 and a doctoral scholarship for J.Q.-Z. (183263). We wish to thank Professor Anne E. Osbourn, John Innes Centre, Norwich UK, for her valuable comments on reviewing the manuscript, and PanAmerican Seed™ for providing T. erecta seeds.
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Qui, J.A., Castro-Concha, L.A., García-Sosa, K. et al. Differential effects of phytotoxic metabolites from Alternaria tagetica on Tagetes erecta cell cultures. J Gen Plant Pathol 75, 331–339 (2009). https://doi.org/10.1007/s10327-009-0184-y
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DOI: https://doi.org/10.1007/s10327-009-0184-y