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Enhanced resistance to Phytophthora infestans and Alternaria solani in leaves and tubers, respectively, of potato plants with decreased activity of the plastidic ATP/ADP transporter

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Abstract

Recently, it has been reported that tubers of transgenic potato (Solanum tuberosum L.) plants with decreased activity of the plastidic ATP/ADP transporter (AATP1) contain less starch, despite having an increased glucose level [P. Geigenberger et al. (2001) Plant Physiol 125:1667–1678]. The metabolic alterations correlated with enhanced resistance to the bacterium Erwinia carotovora. Here it is shown that transgenic potato tubers, possessing less starch yet increased glucose levels due to the expression of a cytoplasm-localized yeast invertase, exhibit drastic susceptibility to E. carotovora. In addition, it is demonstrated that AATP1 anti-sense tubers show an increased capacity to ward off the pathogenic fungus Alternaria solani. In contrast to AATP1 anti-sense tubers, the corresponding leaf tissue does not show changes in carbohydrate accumulation. However, upon elicitor treatment, AATP1 anti-sense leaves possess an increased capacity to release H2O2 and activate various defence-related genes, reactions that are associated with substantially delayed appearance of disease symptoms caused by Phytophthora infestans. Grafting experiments between AATP1 anti-sense plants and wild-type plants indicate the presence of a signal that is generated in AATP1 rootstocks and primes wild-type scions for potentiated activation of cellular defence responses in leaves. Together, the results suggest that (i) the enhanced pathogen tolerance of AATP1 anti-sense tubers is not due to "high sugar resistance", (ii) the increased disease resistance of AATP1 anti-sense tubers is effective against different types of pathogen and (iii) a systemic signal induced by antisensing the plastidic ATP/ADP transporter in potato tubers confers increased resistance to pathogens.

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Abbreviations

AATP1:

plastidic ATP/ADP transporter

BGL:

β-1,3-glucanase

DHSA:

dihydroxy stearic acid

PAL:

phenylalanine ammonia-lyase

Pmg:

cell wall elicitor from Phytophthora sojae

PR:

pathogenesis related

References

  • Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29:23–32

    Article  CAS  PubMed  Google Scholar 

  • Boch J, Verbsky ML, Roberston, TL, Larkin JC, Kunkel BN (1998) Analysis of resistance gene-mediated defense responses in Arabidopsis thaliana plants carrying a mutation in CPR5. Plant Microbe Interact 12:1196–1206

    Google Scholar 

  • Bolwell GP, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, MinobayevaF, Rowntree FG, Wojtaszek P (1999) Recent advances in understanding the origin of the apoplastic oxidative burst in plant cells. Free Radic Res [Suppl] 31:137–145

  • Börnke R, Hajirezaei M-R, Heineke D, Melzer M, Herbers K, Sonnewald U (2002) High-level production of the non-cariogenic sucrose isomer palatinose in transgenic tobacco plants strongly impairs development. Planta 214:356–364

    PubMed  Google Scholar 

  • Bradley DJ, Kjellbom P, Lamb CJ (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

    CAS  PubMed  Google Scholar 

  • Bruce RJ, West CA (1989) Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean. Plant Physiol 91:889–897

    CAS  Google Scholar 

  • Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129:716

    Article  Google Scholar 

  • Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant–pathogen interactions. Trends Plant Sci 7:210–217

    Article  CAS  PubMed  Google Scholar 

  • Düring K, Porsch P, Fladung M, Lörz H (1993) Transgenic potato plants resistant to the phytopathogenic bacterium Erwinia carotovora. Plant J 3:587–598

    Article  Google Scholar 

  • Ehness R, Ecker M, Godt DE, Roitsch T (1997) Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9:1825–1841

    Article  CAS  PubMed  Google Scholar 

  • Farré EM, Tiessen A, Roessner U, Geigenberger P, Trethewey RN, Willmitzer L (2001) Analysis of the compartmentation of glycolytic intermediates, nucleotides, sugars, organic acids, amino acids, and sugar alcohols in potato tubers using a nonaqueous fractionation method. Plant Physiol 127:685–700

    Google Scholar 

  • Fauth M, Merten A, Hahn MG, Jeblick W, Kauss H (1996) Competence for elicitation of H2O2 in hypocotyls of cucumber is induced by breaching the cuticle and is enhanced by salicylic acid. Plant Physiol 110:347–354

    CAS  PubMed  Google Scholar 

  • Frommer WB, Sonnewald U (1995) Molecular analysis of carbon partitioning in solanaceous species. J Exp Bot 46:587–607

    CAS  Google Scholar 

  • Geigenberger P, Stamme C, Tjaden J, Schulze A, Quick WP, Betsche T, Kersting HJ, Neuhaus HE (2001) Tuber physiology and properties of starch from tubers of transgenic potato plants with altered plastidic adenylate transporter activity. Plant Physiol 125:1667–1678

    Article  CAS  PubMed  Google Scholar 

  • Hajirezaei M-R, Takahata Y, Trethewey RN, Willmitzer L, Sonnewald U (2000) Impact of elevated cytosolic and apoplastic invertase activity on carbon metabolism during potato tuber development. J Exp Bot 51:439–445

    Article  CAS  PubMed  Google Scholar 

  • Heineke D, Sonnewald U, Büssis D, Gunter G, Leidreiter K, Wilke I, Raschke K, Willmitzer L, Heldt HW (1992) Apoplastic expression of yeast-derived invertase in potato. Effects on photosynthesis, leaf solute composition, water relations, and tuber composition. Plant Physiol 100:301–308

    CAS  Google Scholar 

  • Herbers K, Meuwly P, Frommer WB, Métraux J-P, Sonnewald U (1996a) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793–803

    Article  CAS  PubMed  Google Scholar 

  • Herbers K, Meuwly P, Métraux J-P, Sonnewald U (1996b) Salicylic acid-independent induction of pathogenesis-related protein transcripts by sugars is dependent on leaf developmental stage. FEBS Lett 397:239–244

    Article  CAS  PubMed  Google Scholar 

  • Horsfall JG, Dimond AE (1957) Interactions of tissue sugar, growth substances, and disease susceptibility. Z Pflanzenkr Pflanzenschutz 27:415–421

    Google Scholar 

  • Jackson SD, James P, Prat S, Thomas B (1998) Phytochrome B affects the levels of a graft-transmissible signal involved in tuberization. Plant Physiol 117:29–32.

    Article  CAS  PubMed  Google Scholar 

  • Jang JC, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679

    Article  CAS  PubMed  Google Scholar 

  • Johnson R, Ryan CA (1990) Wound-inducible potato inhibitor II genes: enhancement of expression by sucrose. Plant Mol Biol 14:527–536

    CAS  PubMed  Google Scholar 

  • Kauss H (1992) Callose and callose synthase. In: Guro SJ, McPherson MJ, Bowles DJ (eds) Molecular plant pathology. Oxford University Press, Oxford, pp 1–8

  • Kauss H, Fauth M, Merten A, Jeblick W (1999) Cucumber hypocotyls respond to cutin monomers via both an inducible and a constitutive H2O2-generating system. Plant Physiol 120:1175–1182

    Article  CAS  PubMed  Google Scholar 

  • Keil M, Sanchez-Serrano JJ, Willmitzer L (1986) Primary structure of a proteinase inhibitor II gene from potato (Solanum tuberosum). Nucleic Acids Res 14:5641–5650

    CAS  PubMed  Google Scholar 

  • Kombrink E, Hahlbrock K, Hinze K, Schröder M (1991) Molecular responses of potato to infection with Phytophtora infestans. In: Smith CJ (ed) Biochemistry and molecular biology of plant–pathogen interaction. Clarendon Press, Oxford

  • Lalonde S, Boles E, Hellmann H, Barker L, Patrick JW, Frommer WB, Ward JM (1999) The dual function of sugar carriers: transport and sugar sensing. Plant Cell 11:707–726

    CAS  PubMed  Google Scholar 

  • Lamb C, Dixon R (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    CAS  Google Scholar 

  • Levine, A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    CAS  PubMed  Google Scholar 

  • Linke, C, Conrath U, Jeblick W, Betsche T, Mahn A, Düring K, Neuhaus HE. (2002) Inhibition of the plastidic ATP/ADP-transporter protein primes potato tubers for augmented elicitation of defense responses and enhances their resistance against Erwinia carotovora. Plant Physiol 129:1607–1615

    Article  CAS  PubMed  Google Scholar 

  • Neuhaus HE, Emes MJ (2000) Development of non-green plastids. Annu Rev Plant Physiol Plant Mol Biol 51:111–140

    CAS  Google Scholar 

  • Oparka KJ, Prior DAM (1988) Movement of lucifer yellow CH in potato tuber storage tissue: a comparison of symplastic and apoplastic transport. Planta 176:533–540

    CAS  Google Scholar 

  • Otazu V, Secor GA (1981) Soft rot susceptibility of potatoes with high reducing sugar content. Phytopathology 71:290–295

    Google Scholar 

  • Renz A, Stitt M (1993) Substrate specificity and product inhibition of different forms of fructokinase and hexokinase in developing potato tubers. Planta 190:166–175

    CAS  Google Scholar 

  • Robinson SP, Wiskich JT (1977) Uptake of ATP analogs by isolated pea chloroplasts and their effect on CO2 fixation and electron transport. Biochim Biophys Acta 461:131–140

    CAS  PubMed  Google Scholar 

  • Stitt M, McLilley R, Gerhardt R, Heldt HW (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol 174:518–552

    CAS  Google Scholar 

  • Thines E, Weber RW, Talbot NJ (2000) MAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell 12:1703–1718

    Google Scholar 

  • Tjaden J, Möhlmann T, Kampfenkel K, Henrichs G, Neuhaus HE (1998) Altered plastidic ATP/ADP-transporter activity influences potato (Solanum tuberosum) morphology, amount and composition of tuber starch, and tuber morphology. Plant J 16:531–540

    Article  CAS  Google Scholar 

  • Tsukaya H, Ohshima T, Naito S, Chino M, Komeda Y (1991) Sugar-dependent expression of the CHS-A gene for chalcone synthase from petunia in transgenic Arabidopsis. Plant Physiol 97:1414–1421

    CAS  Google Scholar 

  • Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Article  Google Scholar 

  • Yu I-C, Parker J, Bent AF (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci USA 95:7819–7824

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Drs. Jürgen Siegrist and Eckhard Thines for providing fungal and oomycete cultures, respectively. Prof. Klaus Hahlbrock, and Drs. Erich Kombrink and Guenther Strittmatter are thanked for providing cDNA clones. The provision of yeast invertase-expressing plants, originally generated by Prof. U. Sonnewald (Gatersleben), by Dr. U. Rössner (Max Planck Institute for Molecular Plant Physiology, Golm, Germany) is greatly appreciated. We thank Prof. U. Sonnewald for allowing us to work with the invertase potato lines. In the laboratories of U.C. and H.E.N., this project is financially supported by the Deutsche Forschungsgemeinschaft (Ne 418/4-1), and the Schwerpunkt Biotechnologie of the Federal State Rheinland Pfalz.

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  1. Uwe Conrath

    Present address: Department of Molecular Biology, Institute for Botany, University of Bonn, Kirschallee 1, 53115, Bonn, Germany

Authors and Affiliations

  1. Department of Plant Physiology, University of Kaiserslautern, P.O. Box 3049, 67653, Kaiserslautern, Germany

    Uwe Conrath, Christoph Linke, Wolfgang Jeblick & H. Ekkehard Neuhaus

  2. Max Planck Institute of Molecular Plant Physiology, Am Muehlenberg 1, 14476, Golm, Germany

    Peter Geigenberger

  3. Department of Animal and Plant Sciences, University of Sheffield, P.O. Box 601, Sheffield, S10 2UQ, UK

    W. Paul Quick

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  1. Uwe Conrath
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Correspondence to H. Ekkehard Neuhaus.

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Conrath, U., Linke, C., Jeblick, W. et al. Enhanced resistance to Phytophthora infestans and Alternaria solani in leaves and tubers, respectively, of potato plants with decreased activity of the plastidic ATP/ADP transporter. Planta 217, 75–83 (2003). https://doi.org/10.1007/s00425-003-0974-y

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