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Induction of Polyphenol Oxidase Activity in Dormant Wild Oat (Avena fatua) Seeds and Caryopses: A Defense Response to Seed Decay Fungi

Published online by Cambridge University Press:  20 January 2017

E. Patrick Fuerst ,
James V. Anderson ,
Ann C. Kennedy  and
Robert S. Gallagher
E. Patrick Fuerst*
Affiliation:
Department of Crop and Soil Sciences, Washington State University, Pullman, WA 99164
James V. Anderson
Affiliation:
USDA-ARS, Biosciences Research Laboratory, 1605 Albrecht Blvd, Fargo, ND 58102
Ann C. Kennedy
Affiliation:
USDA-ARS, Land Management and Water Conservation, 215 Johnson Hall, Washington State University, Pullman WA 99164
Robert S. Gallagher
Affiliation:
Department of Crop and Soil Sciences, The Pennsylvania State University, University Park, PA 16801
*
Corresponding author's E-mail: [email protected]
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Abstract

Persistence of the soil seed bank requires both dormancy and resistance to seed decay organisms. However, there is little or no information evaluating biochemical responses of dormant weed seeds to pathogens. Wild oat caryopses were incubated with four pathogenic fungal isolates to evaluate the response of the pathogen defense enzyme, polyphenol oxidase (PPO). Caryopsis PPO activity was induced by three Fusarium spp. isolates previously obtained from whole seeds incubated in the field whereas caryopsis PPO activity was decreased by a Pythium isolate. Fusarium avenaceum isolate F.a.1 caused the greatest PPO induction and was studied in more detail. When whole wild oat seeds were incubated on F.a.1, PPO activity was induced in seeds, hulls (lemma and palea), and caryopses. Incubation of whole seeds on F.a.1 gradually induced caryopsis PPO activity over an 8-d period, whereas incubation of caryopses on F.a.1 over a 4-d period caused a greater and more rapid induction of PPO activity. Very little PPO activity could be leached from untreated caryopses, but nearly all of the induced PPO activity in F.a.1-treated caryopses was readily leached when incubated in buffer. In Western blots, both untreated and F.a.1-treated leachates contained a ∼57-kilodalton (kD) protein, putatively the mature and relatively inactive form of PPO. However, lower molecular weight antigenic proteins between ∼52 and ∼25 kD were strongly induced in F.a.1-treated caryopses, with this induction being correlated with the increase in PPO activity. We hypothesize that dormant weed seeds possess biochemical defenses against pathogens and, more specifically, that proteolysis in the presence of fungal pathogens may release an activated form of PPO from the surface of wild oat caryopses and hulls.

Keywords

Wild oat, Avena fatua L. AVEFAFusarium avenaceumF. culmorumPythium ultimumpolyphenol oxidaseseed decay resistancedeterioration resistanceseed longevity
Type
Physiology, Chemistry, and Biochemistry
Information
Weed Science , Volume 59 , Issue 2 , June 2011 , pp. 137 - 144
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Anderson, J. V., Fuerst, E. P., Hurkman, W. J., Vensel, W. H., and Morris, C. F. 2006. Biochemical and genetic characterization of wheat (Triticum spp.) kernel polyphenol oxidases. J. Cereal Sci. 44:353–367.Google Scholar
Anderson, J. V., Fuerst, E. P., Tedrow, T., Hulke, B., and Kennedy, A. C. 2010. Activation of polyphenol oxidase in dormant wild oat caryopses by a seed-decay isolate of Fusarium avenaceum . J. Agric. Food Chem. 58:10597–10605.Google Scholar
Anderson, J. V. and Morris, C. F. 2001. An improved whole-seed assay for screening wheat germplasm for polyphenol oxidase activity. Crop Sci. 41:1697–1705.Google Scholar
Anderson, J. V. and Morris, C. F. 2003. Purification and analysis of wheat grain polyphenol oxidase protein. Cereal Chem. 80:135–143.Google Scholar
Anderson, R. C., Liberta, A. E., Packheiser, J., and Neville, M. E. 1980. Inhibition of selected fungi by bacterial isolates from Tripsacum dactyloides L. Plant and Soil. 56:149–152.Google Scholar
Bettge, A. D. 2004. Collaborative study on L-DOPA—wheat polyphenol oxidase assay (AACC Method 22–85). Cereal Foods World. 49:338–342.Google Scholar
Bidochka, M. J., Burke, S., and Ng, L. 1999. Extracellular hydrolytic enzymes in the fungal genus Verticillium: adaptations for pathogenesis. Can. J. MicroBiol. 45:856–864.Google Scholar
Boss, P. K., Gardner, R. C., Janssen, B. J., and Ross, G. S. 1995. An apple polyphenol oxidase cDNA is up-regulated in wounded tissues. Plant Mol. Biol. 27:429–433.Google Scholar
Chancellor, R. J. 1976. Seed behavior. Pages 65–87 in Jones, D. P., ed. Wild Oats in World Agriculture. London Agricultural Research Council.Google Scholar
Chee-Sanford, J. C., Williams, M. M., Davis, A. S., and Sims, G. K. 2006. Do microorganisms influence seed-bank dynamics? Weed Sci. 54:575–587.Google Scholar
Constabel, C. P., Yip, L., Patton, J. J., and Christopher, M. E. 2000. Polyphenol oxidase from hybrid poplar: cloning and expression in response to wounding and herbivory. Plant Physiol. 124:285–296.Google Scholar
De Luna, L. Z., Kennedy, A. C., Hansen, J. C., Paulitz, T. C., Gallagher, R. S., and Fuerst, E. P. 2011. Mycobiota on wild oat (Avena fatua L.) seed and their caryopsis decay potential. Plant Health Progress. DOI: 10-1094/PHP-2011-0210-01-RS.Google Scholar
De Luna, L. Z., Stubbs, T. L., Kennedy, A. C., and Kremer, R. J. 2005. Deleterious bacteria in the rhizosphere. Pages 233–261 in Zobel, R. W. and Wright, S. F., eds. Roots and Soil Management: Interactions between Roots and the Soil. Madison ASA Agronomy Monograph no. 48.Google Scholar
Flurkey, W. H. and Inlow, J. K. 2008. Proteolytic processing of polyphenol oxidase from plants and fungi. J. Inorg. BioChem. 102:2160–2170.Google Scholar
Fuerst, E. P., Anderson, J. V., and Morris, C. F. 2006a. Polyphenol oxidase in wheat grain: whole-kernel and bran assays for total and soluble activity. Cereal Chem. 83:10–16.Google Scholar
Fuerst, E. P., Anderson, J. V., and Morris, C. F. 2006b. Delineating the role of polyphenol oxidase in the darkening of alkaline wheat noodles. J. Agric. Food Chem. 54:2378–2384.CrossRefGoogle ScholarPubMed
Fuerst, E. P., Anderson, J. V., and Morris, C. F. 2010. Polyphenol oxidase and darkening of Asian noodles: measurement and improvement. Pages 285–312 in Hou, G., ed. Asian Noodles: Science, Technology, and Processing. Hoboken, NJ John Wiley & Sons.Google Scholar
Gallagher, R. S. and Fuerst, E. P. 2006. The ecophysiology of seed longevity. Pages 521–557 in Basra, A. S., ed. Handbook of Seed Science. Binghamton, NY Haworth Food Products.Google Scholar
Gallandt, E. R., Fuerst, E. P., and Kennedy, A. C. 2004. Effect of tillage, fungicide seed treatment, and soil fumigation on seed bank dynamics of wild oat (Avena fatua). Weed Sci. 52:597–604.Google Scholar
Gatehouse, J. A. 2002. Plant resistance towards insect herbivores: a dynamic interaction. New Phytol. 156:145–169.Google Scholar
Halloin, J. M. 1983. Deterioration resistance mechanisms in seeds. Phytopathology. 73:335–339.Google Scholar
Hetherington, S. D., Smith, H. E., Scanes, M. G., and Auld, B. A. 2002. Effects of some environmental conditions on the effectiveness of Drechslera avenacea (Curtis ex Cooke) Shoem.: a potential bioherbicide organism for Avena fatua L. Biol. Control. 24:103–109.Google Scholar
Holm, L. G., Plucknett, D. L., Pancho, J. V., and Herberger, J. P. 1977. Avena fatua L. and other members of the ‘wild oat’ group. Pages 105–113 in The World's Worst Weeds: Distribution and Biology. Chapter 13. Honolulu, HI Hawaii University Press.Google Scholar
Jordan, N. 1996. Weed prevention: priority research for alternative weed management. J. Prod. Agric. 9:485–490.Google Scholar
Kennedy, A. C., Elliot, L. F., Young, F. L., and Douglas, C. L. 1991. Rhizobacteria suppressive to the weed downy brome. Soil Sci. Soc. Am. J. 55:722–727.Google Scholar
Kiewnick, I. 1964. Untersuchungen uber den einfluss der samen- und bodenmikroflora auf die lebensdauer der spelzfruchte des flughafers (Avena fatua L.). II. Zum einfluss der mikroflora auf die lebensdauer der samen im boden. Weed Res. 4:31–43.Google Scholar
Kremer, R. J. 1993. Management of weed seed banks with microorganisms. Ecol. Applic. 3:42–52.Google Scholar
Kremer, R. J. 2002. Bioherbicides: potential successful strategies for weed control. Pages 307–323 in Koul, O. and Dhaliwal, G. S., ed. Microbial Biopesticides. New York Taylor and Francis.Google Scholar
Kremer, R. J., Hughes, L. B., and Aldrich, R. J. 1984. Examination of microorganisms and deterioration resistance mechanisms associated with velvetleaf seed. Agron. J. 76:745–749.Google Scholar
Li, L. and Steffens, J. C. 2002. Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta. 215:239–247.Google Scholar
Marshall, M. R., Kim, J., and Wei, C. 2000. Enzymatic Browning in Fruits, Vegetables and Seafoods. Rome. FAO. 54.Google Scholar
Mayer, A. M. 2006. Polyphenol oxidases in plants and fungi: going places? A review. PhytoChem. 67:2318–2331.Google Scholar
Mohammadi, M. and Kazemi, H. 2002. Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Sci. 162:491–498.Google Scholar
Naylor, J. M. and Jana, S. 1976. Genetic adaptation for seed dormancy in Avena fatua . Can. J. Bot. 54:306–312.Google Scholar
Robinson, S. P. and Dry, I. B. 1992. Broad bean leaf polyphenol oxidase is a 60-kilodalton protein susceptible to proteolytic cleavage. Plant Physiol. 99:317–323.Google Scholar
Schmitz, G. E., Sullivan, M. L., and Hatfield, R. D. 2008. Three polyphenol oxidases from red clover (Trifolium pratense) differ in enzymatic activities and activation properties. J. Agric. Food Chem. 56:272–280.Google Scholar
Sharma, M. P. and Vanden Born, W. H. 1978. The biology of Canadian weeds: 27. Avena fatua L. Canadian J. Plant Sci. 58:141–157.Google Scholar
Steffens, J. C., Harel, E., and Hunt, M. D. 1994. Polyphenol oxidase. Pages 275–312 in Ellis, B. E., Kuroki, G. W., and Stafford, H. A., eds. Recent Advances in Phytochemistry, Genetic Engineering of Plant Secondary Metabolism. New York Plenum Press.Google Scholar
Van Gelder, C. W. G., Flurkey, W. H., and Wichers, H. J. 1997. Sequence and structural features of plant and fungal tyrosinases. PhytoChem. 45:1309–1323.Google Scholar
Van Loon, L. C., Rep, M., and Pieterse, C. M. J. 2006. Significance of inducible defense-related proteins in infected plants. Ann. Rev. Phytopathol. 44:135–162.Google Scholar
Virador, V. M., Reyes-Grajeda, J. P., Blanco-Labra, A., Mendiola-Olaya, E., Smith, G., Moreno, A., and Whitaker, J. R. 2010. Cloning, sequencing, purification, and crystal structure of Grenache (Vitis vinifera) polyphenol oxidase. J. Agric. Food Chem. 58:1189–1201.Google Scholar
Wagner, M. and Mitschunas, N. 2008. Fungal effects on seed bank persistence and potential applications in weed biocontrol: a review. Basic Appl. Ecol. 9:191–203.CrossRefGoogle Scholar
Wang, J. and Constabel, C. P. 2004. Three polyphenol oxidases from hybrid poplar are differentially expressed during development and after wounding and elicitor treatment. Physiol. Plant. 122:344–353.Google Scholar
Whitaker, J. R. and Lee, C. Y. 1995. Recent advances in chemistry of enzymatic browning: an overview. Pages 2–7 in Lee, C. Y., and Whitaker, J. R., eds. Enzymatic Browning and Its Prevention. Washington, DC American Chemical Society.Google Scholar
Yoruk, R. and Marshall, M. R. 2003. Physicochemical properties and function of plant polyphenol oxidase: a review. J. Food BioChem. 27:361–422.Google Scholar