American Journal of Potato Research

, Volume 85, Issue 6, pp 466–476 | Cite as

Relationship Between Pink Eye Symptoms and Cell Damage in the Tuber Periderm and Cortex

  • Robert P. Sabba
  • Alvin J. Bussan
  • Edward C. Lulai
Article
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Accepted:

Abstract

Pink eye (PE) is a tuber disorder that leads to processing complications and bud-end rot in storage. Despite the significance of PE for the potato processing industry, limited progress has been made in understanding the physiological basis of this disorder. Although the internal autofluorescence that characterizes PE has been described, the external symptoms of PE have not been well characterized or correlated with internal cellular symptoms. It is of vital importance to determine the physiological and cytological effects of PE in order to understand how it is caused and to develop effective management strategies to prevent the disorder. External symptoms progressed from pinkish discoloration around tuber eyes to water-soaked and corky patch lesions. Internal symptoms progressed from erratic browning around cortical cell walls to necrotic zones and cells with dark, circular inclusions. These areas often became surrounded by an internal PE-related periderm, while the native periderm often became compromised or lost. Vital staining with fluorescein diacetate showed that cortical and periderm cells underneath the native phellem became non-viable in PE tissue. Immunolocalization of homogalacturonan and extensin epitopes indicated that these cell wall polymers were not altered in pink eye afflicted tissues. These results conclusively show that the PE disorder results in or is caused by cell death in tissue underneath the native phellem, but does not lead to either cell wall breakdown or extensin deposition which is often characteristic of pathogen activity.

Keywords

Corky patch Extensin Fluorescein diacetate Periderm Pectin Polyphenolic Polyaliphatic Potato Solanum tuberosum L Vital stain 

Abbreviations

BSA

bovine serum albumin

HG

homogalacturonan

PBS

phosphate-buffered saline

PE

pink eye

SPA

suberin poly(aliphatic)

SPP

suberin poly(phenolic)

TBO

toluidine blue O

Resumen

El ojo rosado (PE por sus siglas en inglés), es un desorden que lleva a complicaciones en el procesamiento y una pudrición del terminal de la yema en almacenamiento. A pesar del significado del PE para la industria, se han hecho avances limitados para comprender la base fisiológica de este desorden. Aunque ha sido descrita la autofluorescencia que caracteriza al PE, los síntomas externos no han sido bien caracterizados o correlacionados con los síntomas celulares internos. Es de importancia fundamental determinar los efectos fisiológicos y citológicos del PE, con el objeto de comprender como es causado y poder desarrollar estrategias de manejo para prevenir este desorden. Los síntomas externos desarrollaron a partir de una ligera decoloración rosada alrededor de los ojos y se convirtieron en lesiones corchosas húmedas. Los síntomas internos pasaron de un oscurecimiento irregular alrededor de la pared de las células corticales a zonas necróticas y células con inclusiones circulares oscuras. Estas áreas a menudo estaban circundadas por un peridermo relacionado con el PE, mientras que el peridermo nativo a menudo se vio comprometido o perdido. La coloración vital con acetato de fluoresceína mostró que las células corticales y del peridermo debajo del felema no estaban viables en el tejido con PE. La inmuno localización de homogalacturonan y epitopes de extensina indicaron que estos polímeros de la pared celular no fueron alterados en el tejido afectado por ojo rosado. Estos resultados demuestran concluyentemente que la afección de PE resulta o es causada por muerte de las células en el tejido que queda debajo del felema, pero no lleva a la descomposición de la pared celular o a la deposición de extensina, la cual es a menudo característica de actividad patogénica.

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Notes

Acknowledgements

Research support was derived from the Wisconsin Potato Improvement Board, Wisconsin Potato Research Exchange, and a USDA Block Grant.

References

  1. Artschwager, E. 1924. Studies on the potato tuber. Journal of Agricultural Research 27: 809–835.Google Scholar
  2. Bernards, M.A. 2002. Demystifying suberin. Canadian Journal of Botany 80: 227–240.CrossRefGoogle Scholar
  3. Blokhina, O., E. Virolainen, and K.V. Fagerstedt. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91: 179–194.PubMedCrossRefGoogle Scholar
  4. Bradley, D.J., P. Kjellbom, and C.J. Lamb. 1992. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70: 21–30.PubMedCrossRefGoogle Scholar
  5. Cetas, R.C. 1971. Lack of correlation between pinkeye and Verticillium wilt susceptibility among potato cultivars and breeding lines. American Potato Journal 48: 306.Google Scholar
  6. Clausen, M.D., W.G.T. Willats, and J.P. Knox. 2003. Synthetic methyl hexagalacturonate haptan inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydrate Research 338: 1797–1800.PubMedCrossRefGoogle Scholar
  7. Copas, M.E., A.J. Bussan, M.J. Drilias, and A. Charkowski. 2008. Influence of compaction and subsoil tillage on soil conditions and pink eye. American Journal of Potato Research. 85: 342–352.Google Scholar
  8. Crawford, R.M.M., and R. Braendle. 1996. Oxygen deprivation stress in a changing environment. Journal of Experimental Botany 47: 145–159.CrossRefGoogle Scholar
  9. de Vries, R.P., and J. Visser. 2001. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiology and Molecular Biology Reviews 65: 497–522.PubMedCrossRefGoogle Scholar
  10. Drew, M.C. 1997. Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual Review of Plant Physiology 48: 223–250.CrossRefGoogle Scholar
  11. Folsom, D., and B.A. Friedman. 1959. Pseudomonas fluorescens in relation to certain diseases of potato tubers in Maine. American Potato Journal 36: 90–97.CrossRefGoogle Scholar
  12. Frank, J.A., R.E. Webb, and D.R. Wilson. 1973. The relationship between Verticillium wilt and the pinkeye disease on potatoes. American Potato Journal 50: 431–438.CrossRefGoogle Scholar
  13. Gahan, P.B. 1984. Vital dyes. In Plant Histochemistry and Cytochemistry. An Introduction, ed. P.B. Gahan, , 124–130. London: Academic.Google Scholar
  14. Gladish, D.K., J. Xu, and T. Niki. 2006. Apoptosis-like programmed cell death occurs in procambium and ground meristem of pea (Pisum sativum) root tips exposed to sudden flooding. Annals of Botany 97: 895–902.PubMedCrossRefGoogle Scholar
  15. Goth, R.W., K.G. Haynes, and D.R. Wilson. 1993. Relationship of Verticillium wilt with pink-eye of potato in Maine. Plant Disease 77: 402–405.Google Scholar
  16. Greenburg, J.T. 1997. Programmed cell death in plant–pathogen interactions. Annual Review of Plant Physiology 48: 525–545.CrossRefGoogle Scholar
  17. Jackson, P.A., C.I.R. Galinha, C.S. Pereira, A. Fortunato, N.C. Soares, S.B.Q. Amancio, and C.P.P. Ricardo. 2001. Rapid deposition of extensin during the elicitation of grapevine callus cultures is specifically catalyzed by a 40-kilodalton peroxidase. Plant Physiology 127: 1065–1076.PubMedCrossRefGoogle Scholar
  18. Li, S., and A.M. Showalter. 1996. Immunolocalization of extensin and potato tuber lectin in carrot, tomato and potato. Plant Physiology 97: 708–718.CrossRefGoogle Scholar
  19. Lulai, E.C. 2001. Tuber periderm and disease resistance. In Compendium of Potato Diseases, eds. W.R. Stevenson, , R. Loria, G.D. Franc, and D.P. Weingartner, 3–6. St. Paul: APS.Google Scholar
  20. Lulai, E.C. 2005. Non-wound-induced suberization of tuber parenchyma cells: a physiological response to the wilt disease pathogen Verticillium dahliae. American Journal of Potato Research 82: 433–440.CrossRefGoogle Scholar
  21. Lulai, E.C. 2007. Skin-set, wound-healing and related defects. In Potato Biology and Biotechnology: Advances and Perspectives, ed. Dick Vreugdenhil, , 471–496. Amsterdam: Elsevier.Google Scholar
  22. Lulai, E.C., and D.L. Corsini. 1998. Differential depositions of suberin phenolic and aliphatic domains and their roles in resistance to infection during potato tuber (Solanum tuberosum L.) wound-healing. Physiological and Molecular Plant Pathology 53: 209–222.CrossRefGoogle Scholar
  23. Lulai, E.C., J.J. Weiland, J.C. Suttle, R.P. Sabba, and A.J. Bussan. 2006. Pink eye is an unusual periderm disorder characterized by aberrant suberization: a cytological analysis. American Journal of Potato Research 83: 409–421.Google Scholar
  24. Nolte, P., G.A. Secor, N.C. Gudmestad, and P.J. Henningson. 1993. Detection and identification of fluorescent compounds in potato tuber tissue with corky patch syndrome. American Potato Journal 70: 649–666.CrossRefGoogle Scholar
  25. Okazawa, Y., and N. Iriuda. 1980. On occurrence of defected potato tubers with rough russeted skin. Japanese Journal of Crop Science 49: 58–65.Google Scholar
  26. Palmer, D.A., and C.L. Bender. 1995. Ultrastructure of tomato leaf tissue treated with the pseudomonad phytotoxin coronatine and comparison with methyl jasmonate. Molecular Plant–Microbe Interactions 8: 683–692.Google Scholar
  27. Peterson, R.L., and W.G. Barker. 1979. Early tuber development from explanted stolon nodes of Solanum tuberosum var. Kennebec. Botanical Gazette 140: 398–406.CrossRefGoogle Scholar
  28. Prade, R.A., D. Zhan, P. Ayoubi, and A. Mort. 1999. Pectins, pectinases and plant–microbe interactions. Biotechnology & Genetic Engineering Reviews 16: 361–391.Google Scholar
  29. Rawyler, A., D. Pavelic, C. Gianinazzi, J. Oberson, and R. Braendle. 1999. Membrane lipid integrity relies on a threshold of ATP production rate in potato cell cultures submitted to anoxia. Plant Physiology 120: 293–300.PubMedCrossRefGoogle Scholar
  30. Sabba, R.P., and E.C. Lulai. 2004. Immunological comparison of native and wound periderm maturation in potato tuber. American Journal of Potato Research 81: 119–124.Google Scholar
  31. Sabba, R.P., and E.C. Lulai. 2005. Immunocytological analysis of potato tuber periderm and changes in pectin and extensin epitopes associated with periderm maturation. Journal of the American Society for Horticultural Science 130: 936–942.Google Scholar
  32. Secor, G. 1988. Proceedings of the conference on pink eye disease of potatoes. American Potato Journal 65: 506–507.CrossRefGoogle Scholar
  33. Secor, G., and D. Rouse. 1992. Proceedings of the second conference on pinkeye of potatoes. American Potato Journal 69: 149–154.CrossRefGoogle Scholar
  34. Secor, G.A., and N.C. Gudmestad. 2001. Disease of unknown cause: pink eye. In Compendium of Potato Disease, eds. W.R. Stevenson, W.R., R. Loria, G.D. Franc, and D.P. Weingartner, 15–16. St. Paul: APS.Google Scholar
  35. Shumway, L.K., J.M. Rancour, and C.A. Ryan. 1970. Vacuolar protein bodies in tomato leaf cells and their relationship to storage of chymotrypsin inhibitor I protein. Planta 93: 1–14.CrossRefGoogle Scholar
  36. Shumway, L.K., V.V. Yang, and C.A. Ryan. 1976. Evidence for the presence of proteinase inhibitor I in vacuolar protein bodies of plant cells. Planta 129: 161–165.CrossRefGoogle Scholar
  37. Smallwood, M., H. Martin, and J.P. Knox. 1995. An epitope of rice threonine- and hydroxyproline-rich glycoprotein is common to cell wall and hydrophobic plasma-membrane glycoproteins. Planta 196: 510–522.PubMedCrossRefGoogle Scholar
  38. Thakur, B.R., K.S. Rakesh, and K.H. Avtar. 1997. Chemistry and uses of pectin—a review. Critical Reviews in Food Science and Nutrition 37: 47–73.PubMedCrossRefGoogle Scholar
  39. Thornton, R.E., and A. Kelman. 2001. Internal brown spot and heat necrosis. In Compendium of Potato Diseases, eds. W.R. Stevenson, W.R., R. Loria, G.D. Franc, and D.P. Weingartner, 89–90. St. Paul: APS.Google Scholar
  40. Tiré, C., R. De Rycke, M. De Loose, D. Inzé, M. Van Montagu, and G. Engler. 1994. Extensin gene expression is induced by mechanical stimuli leading to local cell wall strengthening in Nicotiana plumbaginifolia. Planta 195: 175–181.PubMedCrossRefGoogle Scholar
  41. Willats, W.G.T., G. Limberg, H.C. Buchholt, G.J. van Alebeek, J. Benen, T. Christensen, J. Visser, A. Voragen, J.D. Mikkelsen, and J.P. Knox. 2000. Analysis of pectic epitopes recognized by hybridoma and phage display monoclonal antibodies using defined oligosaccharides, polysaccharides, and enzymatic degradation. Carbohydrate Research 327: 309–320.PubMedCrossRefGoogle Scholar
  42. Wilson, L.G., and J.C. Fry. 1986. Extensin—a major cell wall glycoprotein. Plant, Cell and Environment 9: 239–260.Google Scholar
  43. Yamaguchi, M., H. Timm, and A.R. Spurr. 1964. Effects of soil temperature on growth and nutrition of potato plants and tuberization, composition and periderm structure of tubers. Proceedings of the American Society for Horticultural Science 84: 412–423.Google Scholar

Copyright information

© Potato Association of America 2008

Authors and Affiliations

  • Robert P. Sabba
    • 1
  • Alvin J. Bussan
    • 1
  • Edward C. Lulai
    • 2
  1. 1.Department of HorticultureUniversity of Wisconsin—MadisonMadisonUSA
  2. 2.USDA–ARS, Northern Crop Science LaboratoryFargoUSA

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