Photosynthetica 2002, 40(2):183-193 | DOI: 10.1023/A:1021577521522

Chlorophyll-Deficient Mutant in Oak (Quercus petraea L.) Displays an Accelerated Hypersensitive-Like Cell Death and an Enhanced Resistance to Powdery Mildew Disease

V. Repka1
1 Laboratory of Molecular Biology and Virology, Research Institute of Viticulture and Enology (CRIVE), Bratislava, Slovakia, e-mail

Plants of the discovered chlorophyll-deficient mutant of oak (ML) display enhanced disease resistance to the fungus Erysiphe cichoracearum, causal agent of powdery mildew. Quantitative imaging of chlorophyll (Chl) fluorescence revealed that the net photosynthetic rate (PN) declined progressively in both untreated and invaded ML leaves as well as in inoculated wild-type (WT) leaves. Images of non-photochemical fluorescence quenching (NPQ) in both untreated and infected mutant leaves suggested that the capacity of Calvin cycle had been reduced and that there was a complex metabolic heterogeneity within the ML leaf. The ML mutant accumulates reactive oxygen species, ROS (H2O2) from the oxidative burst followed by spontaneous cell death that mimic the hypersensitive response. Reduction in pathogen sporulation on ML leaves correlated with the accumulation of soluble saccharides and a more rapid induction of defence responses including expression of some defence proteins (β-1,3-glucanase and chitinase). Unlike to WT plants, ML- conferred phenotype activates and/or de-represses multiple defence responses, making them more easily induced by pathogens.

Additional key words: chlorophyll fluorescence; gene expression; hypersensitive reaction; photosynthesis; programmed cell death; proteins; reactive oxygen species; sugars

Published: June 1, 2002  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Repka, V. (2002). Chlorophyll-Deficient Mutant in Oak (Quercus petraea L.) Displays an Accelerated Hypersensitive-Like Cell Death and an Enhanced Resistance to Powdery Mildew Disease. Photosynthetica, 40(2), 183-193. doi: 10.1023/A:1021577521522
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Agrios, G.N.: Plant Pathology. 3rd Ed.-Academic Press, San Diego 1988. Go to original source...
    2. Asada, K.: Production and action of active oxygen species in photosynthetic tissues.-In: Foyer, C.H., Mullineaux, P.M. (ed.): Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. Pp. 77-103. CRC Press, Boca Raton-Ann Arbor-London-Tokyo 1994. Go to original source...
    3. Barnes, S.A., Nishizawa, N.K., Quaggio, R.B., Whitelam, G., Chua, N.-H.: Far-red light blocks greening of Arabidopsis seedlings via a phytochrome A-mediated change in plastid development.-Plant Cell 8: 601-615, 1996. Go to original source...
    4. Chen, Z.X., Silva, H., Klessig, D.F.: Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid.-Science 262: 1883-1886, 1993. Go to original source...
    5. Chou, H.M., Bundock, N., Rolfe, S.A., Scholes, J.D.: Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism.-Mol. Plant Pathol. 1: 99-113, 2000. Go to original source...
    6. Dai, N., Schaffer, A., Petreikov, M., Shahak, Y., Giller, Y., Ratner, K., Levine, A., Granot, D.: Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence.-Plant Cell 11: 1253-1266, 1999. Go to original source...
    7. Dietrich, R.A., Delaney, T.P., Uknes, S.J., Ward, E.R., Ryals, J.A., Dangl, J.L.: Arabidopsis mutants simulating disease resistance response.-Cell 77: 565-577, 1994. Go to original source...
    8. Farrar, J.F., Lewis, D.H.: Nutrient relations in biotrophic infections.-In: Pegg, G., Ayers, P. (ed.): Fungal Infections of Plants. Pp. 92-132. Cambridge Univ. Press, Cambridge 1987.
    9. Genoud, T., Millar, A.J., Nishizawa, N., Kay, S.A., Schäfer, E., Nagatani, A., Chua, N.-H.: An Arabidopsis mutant hypersensitive to red and far-red light signals.-Plant Cell 10: 889-904, 1998. Go to original source...
    10. Glazebrook, J., Rogers, E.E., Ausubel, F.M.: Use of Arabidopsis for genetic dissection of plant defense responses.-Annu. Rev. Genet. 31: 547-569, 1997. Go to original source...
    11. Hammond-Kosack, K.E., Jones, J.D.G.: Plant disease resistance genes.-Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 575-607, 1997. Go to original source...
    12. Herbers, K., Sonnewald, U.: Altered gene expression brought about by inter-and intracellularly formed hexoses and its possible implication for plant-pathogen interactions.-J. Plant Res. 111: 323-328, 1998. Go to original source...
    13. Jang, J.-C., Léon, P., Zhou, L., Sheen, J.: Hexokinase as a sugar sensor in higher plants.-Plant Cell 9: 5-19, 1997. Go to original source...
    14. Jang, J.-C., Sheen, J.: Sugar sensing in higher plants.-Plant Cell 6: 1665-1679, 1994. Go to original source...
    15. Karpinsky, S., Escobar, C., Karpinska, B., Creissen, G., Mullineaux, P.M.: Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress.-Plant Cell 9: 627-640, 1997. Go to original source...
    16. Koch, K.E.: Carbohydrate-modulated gene expression in plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 509-540, 1996. Go to original source...
    17. Lamb, C.J., Dixon, R.A.: The oxidative burst in plant disease resistance.-Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 251-275, 1997. Go to original source...
    18. Levine, A., Tenhaken, R., Dixon, R., Lamb, C.: H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.-Cell 79: 583-593, 1994. Go to original source...
    19. Lichtenthaler, H.K.: Chlorophylls and carotenoids-pigments of photosynthetic biomembranes.-In: Colowick, S.P., Kaplan, N.O. (ed.): Methods in Enzymology. Vol. 148. Pp. 350-382. Academic Press, San Diego-New York-Berkeley-Boston-London-Sydney-Tokyo-Toronto 1987. Go to original source...
    20. Memelink, J., Linthorst, H.J.M., Schilperoort, R.A., Hoge, J.H.C.: Tobacco genes encoding acidic and basic isoforms of pathogenesis-related proteins display different expression patterns.-Plant mol. Biol. 14: 119-126, 1990. Go to original source...
    21. Nagatani, A., Reed, J.W., Chory, J.: Isolation and initial characterization of Arabidopsis mutants that are deficient in phytochrome A.-Plant Physiol. 102: 269-277, 1993. Go to original source...
    22. Oswald, O., Martin, T., Dominy, P.J., Graham, I.A.: Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression.-Proc. nat. Acad. Sci. USA 98: 2047-2052, 2001. Go to original source...
    23. Parks, B.M., Quail, P.H.: hy8, a new class of Arabidopsis long hypocotyl mutants deficient in functional phytochrome A.-Plant Cell 5: 39-48, 1993. Go to original source...
    24. Peng, M., Kuc, J.A.: Peroxidase-mediated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks.-Phytopathology 82: 696-699, 1992. Go to original source...
    25. Rate, D.N., Cuenca, J.V., Bowman, G.R., Guttman, D.S., Greenberg, J.T.: The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defense, and cell growth.-Plant Cell 11: 1695-1708, 1999. Go to original source...
    26. Repka, V., Fischerová, I.: Induction and distribution of amylolytic activity in Cucumis sativus L. in response to virus infection.-Acta virol. 43: 227-235, 1999.
    27. Repka, V., ©tetková, D., Fischerová, I.: The substrate preference and histochemical localization argue against the direct role of cucumber stress-related anionic peroxidase in lignification.-Biol. Plant. 43: 549-558, 2000. Go to original source...
    28. Rolfe, S.A., Scholes, J.D.: Quantitative imaging of chlorophyll fluorescence.-New Phytol. 131: 69-79, 1995. Go to original source...
    29. Salzman, R.A., Tikhonova, I., Bordelon, B.P., Hasegawa, P.M., Bressan, R.A.: Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally-controlled defense response during fruit ripening in grape.-Plant Physiol. 117: 465-472, 1998. Go to original source...
    30. Scholes, J.D.: Photosynthesis: cellular and tissue aspects in diseased leaves.-In: Ayres, P.G. (ed.): Pests and Pathogens. Pp. 85-105. BIOS Sci. Publishers, Oxford 1992.
    31. Scholes, J.D., Lee, P.J., Horton, P., Lewis, D.H.: Invertase: understanding changes in the photosynthetic and carbohydrate metabolism of barley leaves infected with powdery mildew.-New Phytol. 126: 213-222, 1994. Go to original source...
    32. Schwacke, R., Hager, A.: Fungal elicitors induce a transient release of active oxygen species from cultured spruce cells that is dependent of Ca2+ and protein-kinase activity.-Planta 187: 136-141, 1992. Go to original source...
    33. Seo, S., Okamoto, M., Iwai, T., Iwano, M., Fukui, K., Isagi, A., Nakajima, N., Ohashi, Y.: Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction.-Plant Cell 12: 917-932, 2000. Go to original source...
    34. Sheen, J.: Feedback control of gene expression.-Photosynth. Res. 39: 427-438, 1994. Go to original source...
    35. Smeekens, S., Rook, F.: Sugar sensing and sugar-mediated signal transduction in plants.-Plant Physiol. 115: 7-13, 1997. Go to original source...
    36. Somssich, I.E., Bollmann, J., Hahlbrock, K., Kombrink, E., Schulz, W.: Differential early activation of defense-related genes in elicitor-treated parsley cells.-Plant mol. Biol. 12: 227-234, 1989. Go to original source...
    37. Sticher, L., Mauch-mani, B., Métraux, J.-P.: Systemic acquired resistance.-Annu. Rev. Phytopathol. 35: 325-370, 1997. Go to original source...
    38. Thordal-Christensen, H., Zhang, Z., Wei, Y., Collinge, D.B.: Subcellular localization of H2O2: H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction.-Plant. J. 11: 1187-1194, 1997. Go to original source...
    39. Van der Plank, J.: Sink-induced loss of resistance, high sugar disease processess and biotrophy.-In: Van der Plank, J. (ed.): Disease Resistance in Plants. 2nd Ed. Pp. 107-121. Academic Press, London 1984.

    Return to the content