Zoete immuniteit: kunnen suikers zorgen voor een betere bescherming van appelbladeren tegen appelschurft ?

Evelien Deleye
Drie verschillende fructaansuikers (graminanen, inulinen en levanen) werden getest als primingcomponenten op appelbladeren om verdedigingsmechanismen van de plant te activeren tegen appelschurft.
Levanen kunnen als potentiële sweet immunity primers hand in hand gaan met fungiciden tegen het bestrijden van appelschurft op appelbladeren in de toekomst.

Zoete immuniteit: kunnen suikers zorgen voor een betere bescherming van appelbladeren tegen appelschurft ?

Op een gemiddelde dag eten 64 % van de Belgen een stuk fruit met daarbij appel als koploper (VLAM, 2014). Wereldwijd is appel (Malus x domestica) een belangrijk economisch gewas. Toch bereiken veel gewassen die vandaag de dag geteeld worden hun maximaal mogelijke opbrengst niet. Verschillende ziekten en plagen leiden tot grote opbrengstverliezen en hoge kosten voor de sector door hun chemische bestrijding.

De meest vernietigende ziekte in de commerciële appelteelt is appelschurft, een schimmelziekte veroorzaakt door de hemibiotroof Venturia inaequalis. Telers combineren preventieve en curatieve fungicidenbehandelingen om de schimmelontwikkeling op een zo efficiënt mogelijke manier te onderdrukken. Door deze chemische controle kan een hogere opbrengst van het gewas bekomen worden en kan de voedselproductie op peil gehouden worden. Deze intense chemische bestrijding heeft niet alleen een duur prijskaartje voor de teler, maar is ook schadelijk voor zowel de menselijke gezondheid als  het ecosysteem en de omgeving.

Daarom limiteert de wetgeving dan ook sterk het gebruik van pesticiden. Om maximale residuen in het voedsel niet te overschrijden, wordt voor elk pesticide een veiligheidstermijn ingevoerd. Dit betekent dat er een minimale tijd moet zijn tussen de behandeling met het pesticide en de oogst van het gewas, waarna de overblijvende (lage) residuen op het gewas niet meer als toxisch voor de mens kunnen beschouwd worden. Bovendien ontbreekt een correct pesticidenmanagement in vele ontwikkelingslanden en ook in ontwikkelde landen wordt niet altijd correct omgesprongen met pesticide-adviezen.

Daarentegen leidt een veelvuldig gebruik van fungiciden tot het ontstaan van schurftstammen die niet meer gevoelig zijn aan de gewasbeschermingsmiddelen (Carrisse & Jobin, 2006). Hoewel genetisch gewijzigde gewassen hier een oplossing kunnen bieden, ligt dit onderwerp nog steeds zeer gevoelig en maakt het deel uit van een moeilijk maatschappelijk debat.

Vanuit het oogpunt van een meer duurzame en ecologisch verantwoorde landbouw wordt daarom wereldwijd dringend gezocht naar alternatieven waarmee onder andere appelschurft kan bestreden worden. Zo kreeg het zoete immuniteitsconcept onlangs veel aandacht, omdat suikers de verdediging van planten tegen ziekten en plagen mogelijks zouden kunnen verhogen bij een volgende infectie (Bolouri-Moghaddam & Van den Ende, 2012; Morkunas & Ratajczak, 2014).

In deze thesis testen we de werking van dit concept bij appelbladeren tegen appelschurft met enkele veelbelovende suikers en kijken we wat het effect hiervan is op de inwendige suikerconcentraties van de bladeren.

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 In twee infectie-experimenten werden de drie jongste en meest schurftgevoelige appelbladeren besproeid met drie verschillende fructaansuikers: graminanen, inulinen en levanen. Verneveling met fosetyl-aluminum en water werd respectievelijk als positieve en negatieve controle ingezet. Drie dagen na het besproeien van de bladeren met fructanen werden deze appelbladeren geïnfecteerd met schimmelsporen van V. inaequalis. Vervolgens werd de schimmelgroei op de bladeren opgevolgd in de tijd op zowel visueel als DNA niveau. Daarnaast werden op verschillende tijdstippen ook bladstalen genomen en geanalyseerd om het DNA van de schimmel en de suikerconcentraties (glucose, fructose en sucrose) van de appelbladeren te meten, om zo mogelijke effecten van een verbeterde verdediging te kunnen linken aan veranderingen van de suikergehalten van de bladeren. Verder werden ook op verschillende posities van de plant bladstalen genomen om zo het effect van de suikers en dus ook van de verdediging van het blad in functie van de leeftijd van het blad te kunnen onderzoeken.

Als laatste werd ook het direct effect van de geteste suikers onderzocht op de in vitro groei van de schimmel. Hierbij werden verschillende voedingsmedia aangemaakt waar vervolgens een specifiek suiker met specifieke concentratie werd aan toegevoegd. Daarna werd een kleine cirkelvormige schimmelkolonie overgebracht op deze verschillende suikermedia waarna de groei van de diameter van elke schimmelkolonie (zie foto hieronder) werd opgevolgd in de tijd.

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Van alle geteste componenten blijken levanen de meest belovende suikers te zijn door een lagere groei en DNA concentratie van de schimmel op de appelbladeren. Dit wordt toegeschreven aan een mogelijke PAMP (pathogen-associated molecular pattern) rol, waardoor patroonherkenningsreceptoren van bladeren levanen kunnen herkennen en zo verdedigingsmechanismen van de plant kunnen activeren (Versluys et al., 2017). Verder zorgen levanen ook voor een sterke daling van de totale suikerconcentratie, en meer specifiek van de glucoseconcentratie, in de besproeide bladeren, waardoor minder glucose kan worden door de schimmel. Glucose vormt één van de belangrijkste energiebronnen voor schimmels (Berger et al., 2007) en hieruit kunnen we dus besluiten dat er voldoende suikers aanwezig moeten zijn in de appelbladeren opdat de schimmel de bladeren kan infecteren en hierin verder groeien.

Daarentegen lijken inulinen de schimmelgroei te bevorderen op de appelbladeren (zie foto hieronder) alsook in vitro, omdat ze vermoedelijk als voedingsbron gebruikt worden door de schimmel. Vervolgens blijken graminanen de schimmelgroei niet te verminderen op de bladeren. Samengevat kunnen levanen als mogelijke verdediging verhogende suikers hand in hand gaan met fungiciden tegen het bestrijden van appelschurft op appelbladeren in de toekomst.

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Bibliografie

Aderhold, R. 1900. Die Fusicladien unserer Obstbäume. II Teil. Landwirtsch Jahrb 29, p. 541-588.

Agarwal, P.K. 2007. Climate change: Implications for Indian agriculture. 22, p. 37–46.

Andreasson, E. & Ellis, B. 2010. Convergence and specificity in the Arabidopsis MAPK nexus. Trends in Plant Science 15, p. 106–113.

Annis, S.L. & Goodwin, P.H. 1997. Recent advances in the molecular genetics of plant cell wall degrading enzymes produced by plant pathogenic fungi. European Journal of PlantPathology 103, p. 1-14.

Apel, K. & Hirt, H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, p. 373–399.

Aranega-bou, P., De la O Leyva, M., Finiti, I., García-agustín, P. & González-Bosch, C. 2014. Priming of Plant Resistance by Natural Compounds. Hexanoic Acid as a Model. Fontiers in plant science 5, p. 1–12.

Arnault, I., Ondet, S.J., Lombarkia, N., Warlop, F. & Derridj, S. 2016. Preliminary results of foliar applications of fructose to reduce codling moth Cydia pomonella L.(Lepidoptera, Tortricidae) damages on apple tree in organic farming. Ecofruit. 17th International Conference on Organic Fruit-Growing: Proceedings, 15-17 February 2016, Hohenheim, Germany, p. 196-199.

Asai, T., Tena, G., Plotnikova, J.,Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M. & Sheen, J. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, p. 977–983.

Asai, Y., Kobayashi, Y. & Kobayashi, I. 2016. Increased expression of the tomato SISWEET15 gene during grey mold infection and the possible involvement of the sugar efflux to apoplasm in the disease susceptibility. J Plant Pathol Microbiol 7, p. 1– 8.

Atkinson, N.J. & Urwin, P.E. 2012. The Interaction of Plant Biotic and Abiotic Stresses: From Genes to the Field. Journal of Experimental Botan 63(10), p. 3523–44.

Ausubel, F.M. 2005. Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol 6, p. 973–79.

Aziz, A., Heyraud, A. & Lambert, B. 2004. Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea. Planta 218, p. 767-774.

Badel, J.L. Charkowski, A.O. Deng, W.-L. & Collmer, A. 2002. A Gene in the Pseudomonas syringae pv . tomato Hrp pathogenicity island conserved effector locus , hopPtoA1 , contributes to efficient formation of bacterial colonies in planta and is duplicated elsewhere in the genome. The American Phytopathological Society 15(10), p. 1014–24.

Barron, G. 2013. Venturia inaequalis - cause of Apple Scab. [online afbeelding] Beschikbaar op: https://atrium.lib.uoguelph.ca/xmlui/bitstream/handle/10214/5908/Ventur… [datum van opzoeking: 16/11/2017].

Baydoun, E. A. H. & Fry, S. C. 1985. The immobility of pectic substances in injured tomato leaves and its bearing on the identity of the wound hormone. Planta 165, p. 269–276.

Bayer CropScience. 2012. Product Information sheet Aliette®. [online] Beschikbaar op: www.bayercropscience.be/Bayer/CropScience/BCS_Belgium.nsf/id/NL_ALiette… [datum van opzoeking: 4/4/2018].

Beckers, G.J., Jaskiewicz, M., Liu, Y., Underwood, W.R., He, S.Y., Zhang, S., & Conrath, U. 2009. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21, p. 944–953.

Belete, T., & Boyraz, N. 2017. Critical Review on Apple Scab (Venturia inaequalis) Biology , Epidemiology , Economic Importance , Management and Defense Mechanisms to the Causal Agent. Journal of Plant Physiology & Pathology 5, p. 1-11.

Belfanti, E., Silfverberg-Dilworth, E., Tartarini, S., Patocchi, A., Barbieri, M., Zhu, J., Vinatzer, B.A., Gianfranceschi, L., Gessler, C., & Sansavini, S. 2004. The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proceedings of the National Academy of Sciences of the United States of America 101(3), p. 886–890.

Bellin, D., Shuta, A., Delledonne, M., & Yoshioka, H. 2013. Nitric Oxide as a Mediator for Defense Responses 26(3), p. 271–77.

Berger, S., Sinha, A.K., & Roitsch, T. 2007. Plant Physiology Meets Phytopathology : Plant Primary Metabolism and Plant – Pathogen Interactions 58(15), p. 4019–26.

Biemelt, S. & Sonnewald, U. 2006. Plant-microbe interactions to probe regulation of plant carbon metabolism. J Plant Physiol 163, p. 307–318.

Billiard, S., Lopez-Villaviciencio, M., Devier, B., Hood, M.E., Fairhead, C., & Giraud, T. 2011. Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biological Reviews 86, p. 421–442.

Blakeman, J.P., 1975. Germination of Botrytis cinerea conidia in vitro in relation to nutrient conditions on leaf surfaces. Trans. Br. Mycol.

Soc. 65, p. 239–247.

Böhm, H., Albert, I., Fan, L., Reinhard, A., & Nürnberger, T. 2014. Immune receptor complexes at the plant cell surface. Current Opinion in Plant Biology 20, p. 47-54.

Bolouri-Moghaddam, M.R., & Van den Ende, W. 2012. Sugars and plant innate immunity. Journal of Experimental Botany 63, p. 3989–3998.

Bolouri-Moghaddam, M.R., Le Roy, K., Xiang, L., Rolland, F., & Van den Ende, W. 2010. Sugar signalling and antioxidant network connections in plant cells. FEBS Journal 277, p. 2022–2037.

Bolouri-Moghaddam, M.R., & Van den Ende, W. 2013a. Sweet immunity in the plant circadian regulatory network. J. Exp. Bot. 64, p. 1439–1449.

Bolouri-Moghaddam, M.R., Vilcinskas, A., & Rahnamaeian, M. 2015. Cooperative interaction of antimicrobial peptides with the interrelated immune pathways in plants. Molecular Plant Pathology.

Bolton, M.D. 2009. Primary metabolism and plant defense-fuel for the fire. Mol Plant Microbe Interact 22, p. 487–497.

Boone, D.M. 1971. Genetics ofVenturia inaequalis. Annual Review of Phytopathology 9, p. 297–318.

Both, M., Csukai, M., Stumpf, M.P.H., & Spanu, P.D. 2005. Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. The Plant Cell 17(7), p. 2107-2122.

Boudsocq, M., Willmann, M.R., McCormack, M., Lee, H., Shan, L., He, P., Bush, J., Cheng, S.-H., & Sheen, J. 2010. Nature 464(7287), p. 418–22.

Bowen, J.A., Mesarich, C.H., Bus, V.G.M., Beresford, R.M., Plummer, K.M., & Templeton, M.D. 2011. Venturia inaequalis: the causal agent of apple scab. Molecular Plant Pathology 12, p. 105–122.

Bowles, D.J. 1990. Defense-related proteins in higher plants. Annu. Rev. Biochem 59, p. 873–907.

Braam, J. & Davis, R.W. 1990. Rain-, Wind-, and Touch-Induced Expression of Calmodulin and Calmodulin-Related Genes in Arabidopsis. Cell 60, p. 357-364.

Braun, U., Crous, P.W., Groenewald, J.Z. & Scheuer, C. 2011. Pseudovirgaria, a fungicolous hyphomycete genus. IMA Fungus 2(1), p. 65–69.

Braybrook, S.A., & Peaucelle, A. 2013. Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin. PloS one 8(3).

Brutus, A., Sicilia, F., Macone, A., Cervone, F., & De Lorenzo, G. 2010. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl. Acad. Science U.S.A. 107, p. 9452–9457.

Bus, V.G.M., Rikkerink, E.H.A., Caffier, V., Durel, C.-E., & Plummer, K.M. 2011. Revision of the nomenclature of the differential host-pathogen interactions of Venturia inaequalis and Malus. Annual Review of Phytopathology 49, p. 391-413.

Bus, V.G.M., Rikkerink, E.H.A., van de Weg, W.E., Rusholme, R.L., Gardiner, S.E., Bassett, H.C.M., Kodde, L.P., Parisi, L., Laurens, F.N.D., Meulenbroek, E.J., & Plummer, K.M. 2005a. The Vh2 and Vh4 scab resistance genes in two differential hosts derived from Russian apple R12740-7A map to the same linkage group of apple. Molecular Breeding 15, p. 103-116.

Bush, D.S. 1995. Calcium regulation in plant cells and its role in signaling. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, p. 95–122.

Cameron, R.K., et al. 1999. Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. tomato in Arabidopsis. Physiol. Mol. Plant Pathol. 55, p. 121–130.

Cammue, B. 2016-2017. 02 Ziekte-ontwikkeling: algemeen. Levenswijzen van pathogenen. Dia 3.

Cammue, B. 2016-2017. 07 Afweermechanismen van planten. Vorming van thyllen. Dia 21.

Cammue, B. 2016-2017. 08 Genetica. Genetische basis van gastheer-resistentie. Dia 6.

Cammue, B. 2016-2017. 08 Genetica. Resistentie versus tolerantie. Dia 2.

Cánovas, F., Lüttge, U., & Matyssek, R. 2017. Progress in Botany 78, p.14.

Cao, H., et al. 1998. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc. Natl. Acad. Science U.S.A. 95, p. 6531–6536.

Carisse, O., & Jobin, T. 2006. Apple Scab : Improving Understanding for Better Management. Agriculture and Agri-Food, Canada, p.1-22.

Caverzan, A., Casassola, A., & Brammer, S.P. 2016. Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives. Reactive Oxygen Species and Antioxidant Enzymes Involved in Plant Tolerance to Stress 20, p.463–480.

Ceusters, J., Borland, A.M., & De Proft, M.P. 2009a. Drought adaptation in plants with crassulacean acid metabolism involves the flexible use of different storage carbohydrate pools. Plant Signal Behav. 4, p. 212–214.

Ceusters, J., Borland, A.M., Londers, E., Verdoodt, V., Godts, C., & De Proft, M.P. 2009b. Differential usage of storage carbohydrates in the CAM bromeliad Aechmea ‘Maya’ during acclimation to drought and recovery from dehydration. Physiol. Plant 135, p. 174–184.

Chen, H.Y., Huh, J.H., Yu, Y.C., Ho, L.H., Chen, L.Q., Tholl, D., Frommer, W., & Guo, W.J. 2015. The Arabidopsis vacuolar sugar transporter SWEET2 limits carbon sequestration from roots and restricts Pythium infection. The Plant Journal 83(6), p. 1046-1058.

Cheng, C., Gao, X., Feng, B., Sheen, J., Shan, L., & He, P. 2013. Plant immune response to pathogens differs with changing temperatures. Nature Communications 4, p. 1–9.

Chern, M., Fitzgerald, H.A., Canlas, P.E., Navarre, D.A., & Ronald, P.C. 2005. Overexpression of a rice NPR1 homolog leads to constitutive activation of defence response and hypersensitivity to light. Mol. Plant Microbe Interact 18, p. 511–520.

Chevalier, M., Lespinasse, Y., & Renaudin, S. 1991. A microscopic study of the different classes of symptoms coded by the Vf gene in apple for resistance to scab (Venturia inaequalis). Plant Pathology 40, p. 249–256.

Chevreau, E., Dupuis, F., Ortolan, C. et al. 2001. Transformation of apple for durable scab resistance, expression of a puroindoline gene in a susceptible and resistant (Vf )genotype. Acta Horti- culturae 560, p. 323–326.

Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nurnberger, T., Jones, J.D.G., Felix, G., & Boller, T. 2007. A flagellin- induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, p. 497–500.

Chisholm, S.T., Coaker, G., Day, B., & Staskawicz, B.J. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, p. 803–814.

Cho, Y.-H., & Yoo, S-D. 2011. Signaling Role of Fructose Mediated by FINS1 / FBP in Arabidopsis Thaliana. PLoS Genet 7(1), p. 1–10.

Christ, B. & Hörtensteiner, S. 2014. Mechanism and Significance of Chlorophyll Breakdown. J Plant Growth Regul (November 2013), p. 1–17.

Claeyssen, É., & J. Rivoal 2007. Isozymes of plant hexokinase: Occurrence, properties and functions. Phytochemistry 68(6), p. 709-731.

Cohen, Y.R. 2002. β-Aminobutyric acid–induced resistance against plant pathogens. PlantDis 86, p. 448–57.

Conrath, U. 2009. Priming of induced plant defence responses. In: Van Loon, L.C. (Editor), Advances in Botanical Research, Elsevier, p. 361–395.

Conrath, U. 2009. Priming of induced plant defense responses. Advances in Botanical Research 51, p. 361-395.

Conrath, U. 2011. Molecular aspects of defence priming. Trends Plant Science 16, p. 524–531.

Conrath, U., Pieterse, C.M.J., & Mauch-Mani, B. 2002. Priming in plant-pathogen interactions. Trends Plant Science 7, p. 210–216.

Conrath, U., Beckers, G.J., Flors, V., Garcia-Agustin, P., Jakab, G., Mauch, F., Newman, M.A., Pieterse, C.M., Poinssot, B., Pozo, M.J., Pugin, A., Schaffrath, U., Ton, J., Wendehenne, D., Zimmerli, L., & Mauch-Mani, B. 2006. Priming: getting ready for battle. Mol. Plant Microbe Interact 19, p. 1062–1071.

Conrath, U., Beckers, G.J.M., Langenbach, C.J.G., & Jaskiewicz, M.R. 2015. Priming for enhanced defense. Annu. Rev. Phytopathol. 53, p. 97–119.

Cook, D.E., Mesarich, C.H., & Thomma, B.P. 2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53, p. 541–563.

Cote, F., Ham, K.S., Hahn, M.G. & Bergmann, C.W. 1998. Oligosaccharide elicitors in host-pathogen interactions. Generation, perception, and signal transduction. Subcell Biochem 29, p. 385-432.

Couée, I., Sulmon, C., Gouesbet, G., & El Amrani, A. 2006. Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. Journal of Experimental Botany 57, p. 449–459.

Dam, N. 2013. Spores do travel. Mycologia 105, p. 1618-1622.

Dangl, J.L., & Jones, J.D.G. 2001. Plant pathogens and integrated defense responses. Nature 411, p. 826–833.

Daniels, B. 2013. Response of apple (Malus X Domestica) to Venturia Inaequalis, the causal agent of apple scab: a real-time PCR and proteomics study. p. 1-199.

Darvill, A., Augur, C., Bergmann, C., Carlson, R. W., Cheong, J.-J., Eberhard, S., Hahn, M. G., Lo, V.-M., Marfa, V., Meyer, B., Mohnen, D., O'Neill, M.A., Spiro, M. D., van Halbeek, H., Work, W. S. & Albersheim, P. 1992.Glycobiology 2, p. 181-198.

Davis, K.R., Darvill, A.G., Albersheim, P., & Dell, A. 1986. Host pathogen interactions XXIX. Oligogalacturonides released from sodium polypectate by endopolygalacturonic acid lyase are elicitors of phytoalexins in soybean. Plant Physiology 80, p. 568-577.

De Coninck, B., Le Roy, K., Francis, I., Clerens, S., Vergauwen, R., Halliday, A.M., Smith, S.M., Van Laere, A. & Van den Ende, W. 2005. Arabidopsis AtcwINV3 and 6 are not invertases bu are fructan exohydrolases (FEHs) with different substrate specificities. Plant, Cell & Environment 28, p. 432–443.

Demel, R.A., Dorrepaal, E., Ebskamp, M.J.M., Smeekens, J.C.M., & de Kruijff, B. 1998. Fructans interact strongly with model mem- branes. Biochim. Biophys. Acta 1375, p. 36–42.

Demidchik, V. 2015. Mechanisms of Oxidative Stress in Plants: From Classical Chemistry to Cell Biology. Environmental and Experimental Botany 109, p. 212–28.

Demidchik, V., & Maathuis, F.J.M., 2007. Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. Transl. Rev. New Phytol. 175, p. 387-405.

Denoux, C., Galletti, R., Mammarella, N., Gopalan, S., Werck, D., De Lorenzo, G., Ferrari, S., Ausubel, F.M., & Dewdney, J. 2008. Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Molecular Plant 1(3), p. 423-445.

Doehlemann, G., Wahl, R., Horst, R.J., Voll, L.M., Usadel, B., Poree, F., Stitt, M., Pons-Kühnemann, J., Sonnewald, U., Kahmann, R. & Kämper, J. 2008. Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56, p. 181–195.

Dong, X. 2004. NPR1, all things considered. Current Opinion in Plant Biology 7, p. 547–552.

Duran-Flores, D., & Heil, M. 2016. Sources of specificity in plant damaged-self recognition. Curr. Opin. Plant Biol. 32, p. 77–87.

Engelsdorf, T., Horst, R. J., Pröls, R., Pröschel, M., Dietz, F., Hückelhoven, R. & Voll, L. M. 2013. Reduced carbohydrate availability enhances the susceptibility of Arabidopsis toward Colletotrichum higginsianum. Plant physiology 162(1), p. 225-238.

Eichert, T., Kurtz, A., Steiner, U. & Goldbach, H. E. 2008. Size exclusion lim- its and lateral heterogeneity of the stomatal foliar uptake pathway for aqueous solutes and water-suspended nanoparticles. Physiol. Plant. 134, p. 151–160.

Espinas, N.A., Saze, H., & Saijo, H. 2016. Epigenetic Control of Defense Signaling and Priming in Plants 7, p. 1–7.

Essmann, J., Schmitz-Thom, I., Schon, H., Sonnewald, S., Weis, E., & Scharte, J. 2008. RNA interference-mediated repression of cell wall invertase impairs defence in source leaves of tobacco. Plant Physiology 147, p. 1288–1299.

Eulgem, T. 2005. Regulation of the Arabidopsis defence transcriptome. Trends Plant Science 10, p. 71–78.

Eyidogan, F., Oz, M.T., Yucel, M., & Oktem, H.A. 2012. Signal transduction of phytohormones under abiotic stresses. Khan et al. (Editors), Phytohormones and Abiotic Stress Tolerance in Plants. Springer-Verlag Heidelberg, Berlin, 2012.

FAO, 2013. FAO SPECIFICATIONS AND EVALUATIONS FOR AGRICULTURAL PESTICIDES. FOSETYL-ALUMINIUM. p. 1-36.

Farooq, M., Hussain, M., Wahid, A., & Siddique, K.H.M. 2012. Plant Responses to Drought Stress: Chapter 1:Drought Stress in Plants : An Overview. Plant Responses to Drought Stress, p.1–6.

Ferrari, S., Galletti, R., Denoux, C., De Lorenzo, G., Ausubel, F.M., & Dewdney, J. 2007. Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiology 144, p. 367-379.

Ferrari, S., Savatin, D.V., Sicilia, F., Gramegna, G., Cervone, F., & De Lorenzo, G. 2013. Oligogalacturonides: Plant damage-associated molecular patterns and regulators of growth and development. Frontiers in Plant Science 4(49), p. 1-9.

Fu, Z.Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., Mohan, R., Spoel, S.H., Tada, Y., Zheng, N., & Dong, X. 2014. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486(7402), p. 228–232.

Gau, A.E., Koutb, M., Piotrowski, M., & Klopp- stech, K. 2004. Accumulation of pathogenesis-related proteins in the apoplast of a susceptible cultivar of apple (Malus domestica cv. Elstar) after infection by Venturia inaequalis and constitutive expression of PR genes in the resistant cultivar Remo. European Journal of Plant Pathology 110(7), p. 703– 711.

Gebauer, P., Korn, M., Engelsdorf, T., Sonnewald, U., Koch, C. & Voll, L.M. 2017. Sugar accumulation in leaves of Arabidopsis sweet11/sweet12 double mutants enhances priming of the salicylic acid-mediated defense response. Front. Plant Sci., 8.

Gibertia S., Berteab, C.M., Narayanab, R., Maffeib, M.E. & Forlani, G. 2012. Two phenylalanine ammonia lyase isoforms are involved in the elicitor-induced response of rice to the fungal pathogen Magna- porthe oryzae. J Plant Physiol 169, p.249–254.

Gibson, S.I. 2005. Control of plant development and gene expression by sugar signaling. Current Opinion in Plant Biology 8, p. 93-102.

Gimenez, E., Salinas, M. & Manzano-agugliaro, F. 2018. Worldwide Research on Plant Defense against Biotic Stresses as Improvement for Sustainable Agriculture. Sustainability 10, p. 1–19.

Gisi, U., Sierotzki, H., Cook, A., & McCaffery, A. 2002. Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Management Science 58, p. 859-867.

Goellner, K. & Conrath, U. 2008. Priming: it’s all the world to induced disease resistance. Eur J Plant Pathol 121, p.233–242.

Gomez-Ariza, J., Campo, S., Rufat, M., Estopa, M.,Messeguer, J., San Segundo, B., et al. 2007. Sucrose-mediated priming of plant defense responses and broad- spectrumdisease resistance by overexpression of themaize pathogenesis-related PRms protein in rice plants. Mol. Plant Microbe Interact. 20, p. 832–842.

Gonçalves, P., Rodrigues, D.E., Sousa, H. & Spencer-Martins, I., 2000.

FSY1, a novel gene encoding a speciWc fructose/H+ symporter in the type strain of Saccharomyces carlsbergensis. J. Bacteriol. 182, p. 5628–5630.

Granot, D., David-Schwartz, R., & Kelly, G. 2013. Hexose kinases and their role in sugar-sensing and plant development. Frontiers in Plant Science 4(44), p. 1-17.

Guest, D.I. 1984. Modification of defense responses in tobacco and capsicum following treatment with Fosetyl-Al [Aluminium tris (o-ethyl phosphonate)]. Physiological Plant Pathology 25(2), p. 125-134.

Guest, D.I., Saindrenan, P., Barchietto, T., & Bompeix, G. 1988. The phosphonates, anti- oomycete chemicals with a complex mode of action. Proceedings of the 5th International congress on Plant Pathology, Kyoto, p. 333.

Gusberti, M., Gessler, C. & Broggini, G. A. L. 2013. RNA-Seq Analysis Reveals Candidate Genes for Ontogenic Resistance in Malus-Venturia Pathosystem. Plos 8, p. 1-14.

Hamad, H. O., Alma, M. H., Ismael, H. M. & Ali, Goceri, A. 2014. The Effect of Some Sugars on the Growth of Aspergillus Niger. KSU J. Nat. Sci 17(4), p. 7–11.

Harborne, J.B., & Williams, C.A. 2000. Advances in flavonoid research since 1992. Phytochemistry 55, p. 481–504.

Hayes, M.A., Feechan, A., & Dry, I.B. 2010. Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal infection. Plant Physiology 153, p. 211–221.

Hayward, A.P., Tsao, J., & Dinesh-Kumar, S.P. 2009. Autophagy and plant innate immunity: defense through degradation. Semin. Cell Dev. Biol. 20, p. 1041–1047.

He, Z.H., He, D.Z., & Kohorn, B.D. 1998. Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. Plant Journal 14, p. 55–63.

Hendry, G.A.F., 1993. Evolutionary origins and natural functions of fruc- tans-aclimatological, biogeographic and mechanistic appraisal. New Phy.- tol. 123, p. 3–14.

Hernandez-Marin, E., & Martínez, A. 2012. Carbohydrates and their free radical scavenging capability: a theoretical study. The Journal of Physical Chemistry 116, p. 9668–9675.

Hey, S.J., Byrne, E., Halford, N.G. 2010. The interface between metabolic and stress signaling. Ann Bot 105, p.197–203.

Hilker, M., et al. 2015. Priming and memory of stress responses in organisms lacking a nervous system. Biol. Rev.

Hincha, D.K., Zuther, E., & Heyer, A.G. 2003. The preservation of lipo- somes by raffinose family oligosac- charides during drying is mediated by effects on fusion and lipid phase transitions. Biochim. Biophys. Acta 1612, p. 172–177.

Hincha, D.K., Zuther, E., Hellwege, E.M., & Heyer, A.G. 2002. Specific effects of fructo- and gluco- oligosaccharides in the preservation of liposomes during drying. Glycobiology 12, p. 103–110.

Horsfall, J.G., & Dimond, A.E. 1957. Interactions of tissue sugar, growth substances and disease susceptibility. Zeitschrift für Pflanzenkrankheiten und Pflanzenschulz 64, p. 415-421.

Hrazdina, G., Borejsza-Wysocki, W. & Lester, C. 1997. Phy-toalexin production in an apple cultivar resistant to Venturia inaequalis. Phytopathology 87(8), p. 868–876.

Hussain, F., Shaukat, S. S., Abid, M., Usman, F. & Akbar, M. 2014. The Effects of Fungicides Alone and in Conjunction with Chitin on the Control of Some Fungal Pathogens Associated with Chilli Seeds. World Applied Sciences Journal 32(5), p. 977–85.

Hyun, T.K., Hoffmann, A., Sinha, A.K., & Roitsch, T. 2009. Tomato mitogen activated protein kinases regulate the expression of extracellular invertase Lin6 in response to stress related stimuli. Functional Plant Biology 36, p. 1088–1097.

Ichimura, K., Casais, C., Peck, S.C., Shinozaki, K., & Shirasu, K. 2006. MEKK1 is required for MPK4 activation and regulates tissue- specific and temperature-dependent cell death in Arabidopsis. Journal of Biological Chemistry 281, p. 36969–36976.

IPCC. 2014. Klimaatverandering 2014: Gevolgen, Aanpassing en Kwetsbaarheid. Evaluatierapport van het IPCC 5, p. 1–6.

Ishihama, N., & Yoshioka, H. 2012. Post-Translational Regulation of WRKY Transcription Factors in Plant Immunity. Current Opinion in Plant Biology 15, p. 431–437.

Jacobson, E. S. 2000. Pathogenic roles for fungal melanins. Clinical Microbiology Reviews 13(4), p. 708–717.

Janda, M., & Ruelland, E. 2015. Magical mystery tour: Salicylic acid signaling. Environmental and Experimental Botany 114, p. 117-128.

Jaskiewicz, M., Conrath, U., & Peterhänsel, C. 2011. Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Reports 12(1), p. 50-55.

Jha, G., Thakur, K., & Thakur, P. 2009. The Venturia Apple Pathosystem: Pathogenicity Mechanisms and Plant Defense Responses. Journal of Biomedicine and Biotechnology 2009, p. 1-10.

Jones, J.D.G., & Dangl, J.L. 2006. The Plant Immune System. Nature 444, p. 323–329.

Jones, P., & Vogt, T. 2001. Glycosyltransferases in secondary plant metabolism: tranquilizers and stimulant controllers. Planta 213, p. 164-174.

Jung, H.W., Tschaplinksi, T.J., Wang, L., Glazebrook, J., & Greenberg, J.T. 2009. Priming in systemic plant immunity. Science 324, p. 89–91.

Kang, Y., Khan, S., & Ma, X. 2009. Climate change impacts on crop yield , crop water productivity and food security – A review. Progress in Natural Science 19(12), p.1665–1674.

Kawano, Y., & Shimamoto, K. 2013. Early signaling network in rice PRR-mediated and R-mediated immunity. Current Opinion in Plant Biology 16, p. 496-504.

Kempel, A., Schädler, M., Chrobock, T., Fischer, M., & van Kleunen, M. 2011. Tradeoffs Associated with Constitutive and Induced Plant Resistance against Herbivory. PNAS 108(14), p.5685–89.

Keyse, S.M. 2000. Protein phosphatases and the regulatio,n of mitogen- activated protein kinase signalling. Curr. Opin. Cell Biol. 12, p. 186–192.

Knogge, W. 1996. Fungal Infection of Plants. 8, p. 1711–22.

Koch, K. 2004. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7, p. 235–246.

Koch, K.E. 1996. Carbohydrate-modulated gene expression in plants. Annu.Rev. Plant Physiol. Plant Mol. Biol. 47, p. 509–540.

Koczan, J. M., Mcgrath, M. J., Zhao, Y. & Sundin, G. W. 2009. Contribution of Erwinia Amylovora Exopolysaccharides Amylovoran and Levan to Biofilm Formation : Implications in Pathogenicity. The American Phytopathological Society 99(11), p. 1237–44.

Kohorn, B.D., & Kohorn, S.L. 2012. The cell wall-associated kinases, WAKs, as pectin receptors. Frontiers in Plant Science 3(88), p. 1-5.

Kohorn, B.D., Kohorn, S.L., Todorova, T., Baptiste, G., Stansky, K., & McCullough, M. 2011. A dominant allele of Arabidopsis pectin- binding wall-associated kinase induces a stress response suppressed by MPK6 but not MPK3 mutations. Molecular Plant.

Kombrink, A., Sánchez-Vallet, A., & Thomma, B.P.H.J. 2011. The role of chitin detection in plant-pathogen interactions. Microbes and Infection 13, p. 1168-1176.

Komjanc, M., Festi, S., Rizzotti, L., Cattivelli, L., Cervone, F., & De Lorenzo, G. 1999. A leucine-rich repeat receptor-like protein kinase (LRPKm1) gene is induced in Malus x domestica by Venturia inaequalis infection and salicylic acid treatment. PlantMolecular Biology 40(6), p. 945–957.

Kunz, S., Gardeström, P., Pesquet, E., & Kleczkowski, L.A. 2015. Hexokinase 1 is required for glucose- induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis. Front Plant Science 6, p. 525.

Lamb, C., & Dixon, R.A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, p. 251–275.

Landgraf, R., Schaarschmidt, S., & Hause, B. 2012. Repeated Leaf Wounding Alters the Colonization of Medicago Truncatula Roots by Beneficial and pathogenic microorganisms. Plant, Cell and Environment 35, p. 1344–57.

Lastdrager, J., Hanson, J., & Smeekens, J. 2014. Sugar Signals and the Control of Plant Growth and Development. Journal of Experimental Botany 65(3), p. 799–807.

Leben, C., & Keitt, G.W. 1948. Venturia inaequalis (Cke.) Wint. V. The influence of carbon and nitrogen sources and vitamins on growth in vitro. American journal of botany, p. 337-343.

Lecompte, F., Nicot, P.C., Ripoll, J., Abro, M.A., Raimbault, A.K., Lopez-Lauri, F., & Bert in, N. 2017. Reduced susceptibility of tomato stem to the necrotrophic fungus Bot rytis cinerea is associated with a specific adjustment of fructose content in the host sugar pool. Annals of Botany.

Lee, K.W., Kim, Y.J., Kim, D.O., Lee, H.J., & Lee, C.Y. 2003. Major phenolics in apple and their contribution to the total antioxidant capacity. Journal of agricultural and food chemistry 51(22), p. 6516-6520.

Leon, J., Lawton, M.A., & Raskin, L. 1995. Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiology 108, p. 1673–1678.

Li, W.L., Faris, J.D., Muthukrishnan, S., Liu, D.J., Chen, P.D., & Gill, B.S. 2001. Isolation and Characterization of Novel cDNA Clones of Acidic Chitinases and β -1 , 3-Glucanases from Wheat Spikes Infected by Fusarium Graminearum. Theor Appl Genet 102, p. 353–62.

Longhi, S., & Cambillau, C. 1999. Structure-Activity of Cutinase, a Small Lipolytic Enzyme. Biochimica et Biophysica Acta 1441, p. 185-196.

van Loon, L., Rep, M., & Pieterse, C. 2006. Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44, p. 135-162.

Low, P.S. & Merida, J.R. 1996. The oxidative burst in plant defense: Function and signal transduction. Physiol Plant 96, p.533-542.

MacHardy, W. E. 1996. Apple Scab, Biology, Epidemiology, and Management, APS. St. Paul, Minn, USA.

Macho, A.P., & Zipfel, C. 2014. Plant PRRs and the activation of innate immune signaling. Molecular Cell 54, p. 263-272.

Mahajan, S., & Tuteja, N. 2005. Cold , Salinity and Drought Stresses : An Overview. Archives of Biochemistry and Biophysics 444, p. 139–58.

Maldonado, A.M., Doerner, P., Dixon, R.A., Lamb, C.J., & Cameron, R.K. 2002. A putative lipid transfer protein involved in systemic acquired resistance signalling in Arabidopsis. Nature 419, p. 399–403.

MAPK-Group. 2002. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends in Plant Sciences 7, p. 301–308.

Marínez-Noël, G.M.A., Tognetti, J.A., Salerno, G.L., Wiemken, A., & Pontis, H.G. 2009. Protein phosphatase activity and sucrose-mediated induction of fructan synthesis in wheat. Planta 230, p. 1071–1079.

Meng, X., Xu, J., He, Y., Yang, K.-Y., Mordorski, B., Liu, Y., & Zhang, S. 2013. Phosphorylation of an ERF Transcription Factor by Arabidopsis MPK3 / MPK6 Regulates Plant Defense Gene Induction and Fungal Resistance. The Plant Cell 25, p. 1126–42.

Meskiene, I., Baudouin, E., Schweighofer, A., Liwosz, A., Jonak, C., Rodriguez, P.L., Jelinek, H., & Hirt, H. 2003. The stress-induced protein phosphatase 2C is a negative regulator of amitogen-activated protein kinase. J. Biol. Chem. 278, p. 18945–18952.

Mills, W.D., & LaPlante, A.A. 1954. Apple scab. In: Disease and insects in the orchard, Cornell Extension Bulletin 711, p. 20–28.

Mishina, T.E., & Zeier, J. 2007. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50, p. 500–513.

Mittler, R. 2002. Oxidative Stress , Antioxidants and stress tolerance. TRENDS in Plant Science 7(9), p. 405–10.

Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., Narusaka, Y., Kawakami, N., Kaku, H. & Shibuya, N. (2007). CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, p. 19613–19618.

Molinier, J., Ries, G., Zipfel, C., & Hohn, B. 2006. Transgeneration memory of stress in plants. Nature 442, p. 1046–1049.

Monoghan, J., & Zipfel, C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Current Opinion in Plant Biology 15, p. 349-357.

Moreau, M., Tian, M., & Klessig, D.F. 2012. Salicylic Acid Binds NPR3 and NPR4 to Regulate NPR1-Dependent Defense Responses. Cell Research 22, p. 1631–33.

Morkunas, I., & Ratajczak, L. 2014. The Role of Sugar Signaling in Plant Defense Responses against Fungal Pathogens. Acta Physiol Plant 36, p. 1607–19.

Morkunas, I., Marczak, Q., Stachowiak, J., & Stobiecki, M. 2005. Sucrose-stimulated accumulation of isoflavonoids as a defence response of lupine to Fusarium oxysporum. Plant Physiology and Biochemistry 43, p. 363–73.

Morkunas, I., Stobiecki, M., Marczak, Ł., Stachowiak, J., Narozna, D., & Remlein-Starosta, D. 2010. Changes in carbohydrate and isoflavonoid metabolism in yellow lupine in response to infection by Fusarium oxysporum during the stages of seed germination and early seedling growth. Physiol Mol Plant Pathol 75, p. 46–55.

Mou, Z., Fan, W., & Dong, X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, p. 935-944.

Muthamilarasan, M., & Prasad, M. 2013. Review Plant Innate Immunity: An Updated Insight into Defense Mechanism. J. Biosci 38, p. 433–449.

Nägele, T., & Heyer, A.G. 2013. Approximating subcellular organi- sation of carbohydrate metabolism during cold acclimation in differ- ent natural accessions of Arabidopsis thaliana. New Phytol. 198, p. 777–787.

Nakagami, H., Kiegerl, S., & Hirt, H. 2004. OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. Journal of Biological Chemistry 279, p. 26959–26966.

Nakagami, H., Soukupova, H., Schikora, A., Zarsky, V., & Hirt H. 2006. A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. Journal of Biological Chemistry 281, p. 38697–38704.

Naseem, M., Kunz, M. & Dandekar, T. 2017. Plant–Pathogen Maneuvering over Apoplastic Sugars. Plant Science 22, p. 740-743.

Nelson, D.L., & Cox, M. M. 2005. Lehninger's Principles of Biochemistry, 4th Edition. W. H. Freeman and Company, New York.

Nikraftar, F., Taheri, P., Rastegar, M.F., & Tarighi, S. 2013. Tomato partial resistance to Rhizoctonia solani involves antioxidative defense mechanisms. Physiol Mol Plant Pathol 81, p. 74–83.

Nishizawa, A., Yabuta, Y., & Shigeoka, S. 2008. Galactinol and raffinose con- stitute a novel function to protect plants from oxidative damage. Plant Physiology 147, p. 1251–1263.

Osbourn, A.E. 1996. Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell 8, p. 1821–1831.

Osman, M. & Valadon, L.R.G. 1979. EFFECT OF LIGHT QUALITY ON GROWTH AND SPORULATION IN VERTICILLIUM AGARICINUM. The British Mycological Society 72(1), p. 145–46.

Osuna, D., Usadel, B., Morcuende, R., Gibon, Y., Bläsing, O.E., Höhne, M., Günter, M., Kamlage, B., Trethewey, R., Scheible, W., & Stitt, M. 2007. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. The Plant Journal 49, p. 463-491.

Pandey, S.P., & Somssich, I.E. 2009. The Role of WRKY Transcription Factors in. Plant Physiology 150(August), p. 1648–55.

Parisi, L., & Lespinasse, Y. 1996. Pathogenicity of Venturia inaequalis strains of race 6 on apple clones (Malus sp.). Plant Disease 80, p. 1179–1183.

Park, S.-W., Kaimoyo, E., Kumar, D., Mosher, S., & Klessig, D.F. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, p. 113–116.

Pastor, V., Luna, E., Mauch-Mani, B., Ton, J. & Flors, V. 2012. Primed plants do not forget. Environmental and Experimental Botany 94. p. 46-56.

Peshev, D., Vergauwen, R., Moglia, A., Hideg, E., & Van den Ende, W. 2013. Towards understanding vacuolar antioxidant mechanisms: a role for fructans? Journal of Experimental Botany 64, p. 1025–1038.

Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H.B., Lacy, M., Austin, M.J., Parker, J.E., et al. 2000. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103, p. 1111–1120.

Petkovsek, Stampar & Veberic. 2007. Parameters of inner quality of the apple scab resistant and susceptible apple cultivars ( Malus domestica Borkh.). Scientia Horticulturae 114(1), p. 37-44.

Pieterse, C.M.J., & Dicke, M. 2007. Plant interactions with microbes and insects: From molecular mechanisms to ecology. Trends in Plant Science 12(12), p. 564-569.

Pozo, M.J., Van Der Ent, S., Van Loon, L.C., & Pieterse, C.M.J. 2008. Transcription factor MYC2 is involved in priming for enhanced defence during rhizobacteria-induced systemic resistance in Arabidopsis thaliana RID A-9326-2011. New Phytol. 180, p. 511–523.

Raa, J. 1968. Natural resistance of Apple Plants to Venturia inaequalis. Ph.D. thesis. Univ, Utrecht, Utrecht, The Netherlands. P. 1-100.

Ramegowda, V., & Senthil-Kumar, M. 2015. The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. J. Plant Physiol. 176, p. 47–54.

Reddy, V.S., & Reddy, A.S.N. 2004. Proteomics of Calcium-Signaling Components in Plants. Phytochemistry 65, p. 1745–76.

Reina-Pinto, J.J., & Yephremov, A. 2009. Surface lipids and plant defences. Plant Physiology and Biochemistry 47, p. 540–549.

Ren, D.T., Yang, H.P., & Zhang, S.Q. 2002. Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabi- dopsis. J. Biol. Chem. 277, p. 559–565.

Reymond, P., Grünberger, S., Kalanethee, P., Müller, M. & Farmer, E.E. 1995. Oligogalacturonide Defense Signals in Plants : Large Fragments Interact with the Plasma Membrane in vitro. Proc. Natl. Acad. Sci. USA 92, p. 4145–49.

Robinson, R. A. 1976. Plant Pathosystems. Advanced Series in Agricultural Sciences 3. Springer-Verlag. Berlijn. p. 1-184.

Rodriguez, M.C.S., Petersen, M., & Mundy, J. 2010. Mitogen-activated protein kinase signaling in plants. Annual Review of Plant Biology 61, p. 621–649.

Rohila, J.S., & Yang, Y.N. 2007. Rice mitogen-activated protein kinase gene family and its role in biotic and abiotic stress response. Journal of Integrative Plant Biology 49, p. 751–759.

Roitsch, T. 1999. Source-sink regulation by sugar and stress. Current Opinion in Plant Biology 2, p. 198-206.

Roitsch, T., Balibrea, M.E., Hofmann, M., Proels, R., & Sinha, A.K. 2003. Extracellular invertase: key metabolic enzyme and PR protein. Journal of Experimental Botany 54, p. 513–524.

Rolland, F., Baena-Gonzalez, E., & Sheen, J. 2006. Sugar sensing and signalling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57, p. 675–709.

Rosenberger, D. 2016. RIMpro as a Tool for Management of Apple Scab. p. 1–3.

Rosenzweig, C., Iglesius, A., Yang, X.B., Epstein, P.R., & Chivian, E. 2001. Climate Change and Extreme Weather Events - Implications for Food Production, Plant Diseases, and Pests. GLOBAL CHANGE & HUMAN HEALT 2, p. 90-104.

Rossi, V., Ponti, I., Marinelli, M., Giosue, S., & Bugiani, R. 2001. Environmental factors influencing the dispersal of Venturia inaequalis ascospore in orchards air. Journal of Fythopathology 149, p. 11-19.

Ruan, Y. 2014. Sucrose metabolism: Gateway to diverse carbon use and sugar signaling. Annual Review of Plant Biology 65, p. 33-67.

Rushton, P.J., Torres, J.T., Parniske, M., Wernert, P., Hahlbrock, K., & Somssich, I.E. 1996. Interaction of Elicitor-Induced DNA-Binding Proteins with Elicitor Response Elements in the Promoters of parsley PR1 genes. The EMBO Journal 15(20), p. 5690–5700.

Savary, S., Ficke, A., Aubertot, J.N. & Hollier, C. 2012. Crop losses due to diseases and their implications for global food production losses and food security. Food Sec. 4, p. 519-537.

Savatin, D.V., Gramegna, G., Modesti, V., & Cervone, F. 2014. Wounding in the Plant Tissue : The Defense of a Dangerous Passage. Frontiers in Plant Science 5, p. 1–11.

Schonherr, J. 2006. Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J. Exp. Bot. 57, p. 2471–2491.

Schulze-Lefert, P., & Panstruga, R. 2003. Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu. Rev. Phytopathol. 41, p. 641 –667.

Schwabe, W.F.S. 1979. Changes in scab susceptibilty of apple leaves as influenced by age. Phytophylactica 11, p. 53-56.

Schweikert, C., Liszkay, A., & Schopfer, P. 2000. Scission of polysaccharides by peroxidase-generated hydroxyl radicals. Phy- tochemistry 53, p. 565–570.

Schymanski, S.J. & Or, D. 2015. Wind effects on leaf transpiration challenge the concept of “potential evaporation”. IAHS 371, p. 99-107.

Shah, J., & Zeier, J. 2013. Long-Distance Communication and Signal Amplification in Systemic Acquired Resistance. Frontiers in Plant Science 4, p. 1–16.

Shanker, A.K., & Shanker, C. 2016. Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives. Intech, p. 1-768.

Sheen, J. 2014. Master Regulators in Plant Glucose Signaling Networks. J. Plant Biol 57, p. 67–79.

Sheen, J., Zhou, L., & Jang, J.C. 1999. Sugars as signaling molecules.Curr.Opin. Plant Biol. 2, p. 410–418.

Shi, H-B., Liang, S., Huang, L.-Y., Liu, X.-H., Zhu, X.-M., Zhao, Y.-H., & Lin, F.-C. 2016. Autophagy in Current Trends in Cellular Physiology and Pathology. Autophagy in Plant Plant Pathogenic Pathogenic Fungi Autophagy Fungi 12, p. 221–41.

Sinha, S.K., & Swaminathan, M.S. 1991. Deforestation, climate change and sustainable nutrition security. Clim change 16, p. 33-45.

Slaughter, A., Daniel, X., Flors, V., Luna, E., Hohn, B., & Mauch-Mani, B. 2012. Descendants of Primed Arabidopsis Plants Exhibit Resistance to Biotic Stress 1. Plant Physiology 158, p. 835–43.

Smeekens, S., & Hellmann, H.A. 2014. Sugar sensing and signaling in plants. Front. Plant Science 5, p. 113.

Smeekens, S., Ma, J., Hanson, J., & Rolland, F. 2010. Sugar signals and molecular networks controlling plant growth. Curr. Opin. Plant Biol. 13, p. 274–279.

Smith, J.L., De Moraes, C.M., & Mescher, M.C. 2009. Jasmonate- and salicylate- mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Management Science 65, p. 497-503.

Solfanelli, C., Poggi, A., Loreti, E., Alpi, A., & Perata, P. 2006. Sucrose- specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiology 140, p. 637–646.

Soriano, J.M., Joshi, S.G., van Kaauwen, M., Noordijk, Y., Groenwold, R., Henken, B., van de Weg, W.E., & Schouten, H.J. 2009. Identification and mapping of the novel apple scab resistance gene Vd3. Tree Genetics and Genomes 5(3), p. 475–482.

Soriano, J.M., Joshi, S.G., van Kaauwen, M., Noordijk, Y., Groenwold, R., Henken, B., van de Weg, W.E., & Schouten, H. J. 2009. Identification and Mapping of the Novel Apple Scab Resistance Gene Vd3. Tree Genetics & Genomes 5, p. 475–82.

Spoel, S.H., et al. 2009. Proteasome-mediated turnover of the transcription co-activator NPR1 plays dual roles in regulating plant immunity. Cell 137, p. 860–872.

Stael, S.P., Kmiecik, P., Willems, K., Van Der Kelen, N.S., Coll, M., Teige & Van Breusegem, F. 2015. Plant innatie immunity – Sunny side up? Trends in Plant Science 20(1), p. 3-11.

Stotz, H.U., Waller, F., & Wang, K. 2013. Innate Immunity in Plants: The Role of Antimicrobial Peptides. p.29–52.

Stoyanova, S., Geuns, J., Hideg, E., & Van den Ende, W. 2011. The food additives inulin and stevioside counteract oxidative stress. International Journal of Food Sciences and Nutrition 62, p. 207–214.

Struck, C. 2006. Chapter 4: Infection strategies of plant parasitic fungi. In: Cooke, B.M. Jones, D.G. & Kaye, B. (Editors), The Epidemiology of Plant Diseases, Springer, p. 117- 137.

Suarez-Rodriguez, M.C., Adams-Phillips, L., Liu, Y., Wang, H., Su, S.H., Jester, P.J., Zhang, S., Bent, A.F., & Krysan, P.J. 2007. MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiology 143, p. 661–669.

Sun, F., Zhang, P., Guo, M., Yu, W., & Chen, K. 2013. Burdock fructooligosaccharide induces fungal resistance in postharvest Kyoho grapes by activating the salicylic acid-dependent pathway and inhibiting browning. Food Chem. 138, p. 539–546.

Suzuki, N., Rivero, R.M., Shulaec, V., Blumwald, E., & Mittler, R. 2014. Tansley Review Abiotic and Biotic Stress Combinations. New Phytologist 203, p.32-43.

 Szankowski, I., Waidmann, S., Degenhardt, J., Patocchi, A., Paris, R., Silfverberg-Dilworth, E., Broggini, G., & Gessler, C. 2009. Highly scab-resistant transgenic apple lines achieved by introgression of HcrVf2 controlled by different native promoter lengths. Tree Genetics and Genomes 5(2), p. 349–358.

Tadege, M., Bucher, M., Stähli, W., Suter, M., Dupuis, I. & Kuhlemeier, C. 1998. Activation of plant defense responses and sugar efflux by expression of pyruvate decarboxylase in potato leaves. Plant J. 16, p. 661–671.

Takahashi, F., Mizoguchi, T., Yoshida, R., Ichimura, K., & Shinozaki, K. 2011. Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Molecular Cell 41, p. 649–660.

Tarkowski, Ł.P., & Van den Ende, W. 2015. Cold tolerance triggered by soluble sugars: a multifaceted countermeasure. Front Plant Science 6, p. 203.

Tauzin, A.S., & Giardina, T. 2014. Sucrose and Invertases, a Part of the Plant Defense Response to the Biotic Stresses RESPONSE. Frontiers in Plant Science 5, p. 1–8.

Tena, G., Boudsocq, M., & Sheen, J. 2011. Protein Kinase Signaling Networks in Plant Innate Immunity. Curr Opin Plant Biol 14(5), p. 519–29.

Teng, S., Keurentjes, J., Bentsink, L., Koornneef, M., & Smeekens, S. 2005. Sucrose-specific induction of anthocyanin biosynthesis in Ara- bidopsis requires the MYB75/PAP1 gene. Plant Physiol. 139, p. 1840– 1852.

Thibaud, M.C., Gineste, S., Nussaume, L., & Robaglia, C. 2004. Sucrose increases pathogenesis-related PR-2 gene expression in Arabidopsis thaliana through an SA-dependent but NPR1-independent signaling pathway. Plant Physiol. Biochem. 42, p. 81–88.

Thulke, O.U., & Conrath, U. 1998. Salicylic acid has a dual role in the activation of defence-related genes in parsley. Plant J. 14, p. 35–42.

Toksoy, E., Hernández, L., & Combie, J. 2016. Review of levan polysaccharide: from a century of past experiences to future prospects. Biotech. Adv. 34, p. 827–844.

Trapman, M., & Polfliet, M. 1997. Management of primary infections of Apple-scab with the simulation program RIMpro: review of four years field trials. IOBC wprs Bulletin 20, p. 241-250.

Trouvelot, S., Héloir, M., Poinssot, B., Gauthier, A., Paris, F., Guillier, C., Combier, M., Trdá, L., Daire, X., & Adrian, M. 2014. Carbohydrates in plant immunity and plant protection: roles and potential application as foliar sprays. Frontiers in Plant Science 5(592), p. 1-14.

Tsuda, K., Sato, M., Glazebrook, J., Cohen, J.D., & Katagiri, F. 2008. Interplay between MAMP triggered and SA-mediated defense responses. Plant J. 53, p. 763–775.

Turechek, W.W. 2004. Apple diseases and their management: Diseases of fruits and vegetables: Diagnosis and management Volume I. Naqvi, S.A.M.H. (ed.) Kluwer Academic Publishers, Dordrecht, p. 1-108.

USDA. 2017. Fresh Deciduous Fruit: World Markets and Trade (Apples, Grapes & Pears. Fresh apples, p. 1.

Valluru, R., & Van den Ende, W. 2008. Plant fructans in stress environments: emerging concepts and future prospects. J. Exp. Bot. 59, p. 2905–2916.

Valluru, R., & Van den Ende, W. 2011. Myo-inositol and beyond: Emerging networks under stress. Plant Science 181, p. 387-400.

Valluru, R., Lammens, W., Clau- pein, W., & Van den Ende, W. 2008. Freezing tolerance by vesicle-mediated fructan transport. Trends Plant Science 13, p. 409–414.

van Baarlen, P., Legendre, L., & van Kan, J.A.L. 2007. Botrytis: Biology, Pathology and Control. Defence Compounds Against Botrytis Infection. p. 143-155.

 Van den Ende, W., De Coninck, B., Clerens, S., Vergauwen, R. & Van Laere, A. 2003b. Unexpected presence of fructan exohydrolases (6-FEHs) in non-fructan plants: characterization, cloning, mass mapping and functional analysis of a novel ‘cell-wall invertase-like’ specific 6-FEH from sugar beet (Beta vulgaris L.). Plant Journal 36, p. 697–710.

 Van den Ende, W., De Coninck, B. & Van Laere, A. 2004. Plant fructan exohydrolases: a role in signaling and defense? Plant Science 9, p. 1360-1385.

 Van den Ende, W., & El-Esawe, S.K. 2014. Sugar signaling pathways leading to fructan and anthocyanin accumulation: a dual function in abiotic and biotic stress responses? Environ Exp. Bot. 108, p. 4–13.

 Van den Ende, W., & Valluru, R. 2009. Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? Journal of Experimental Botany 60, p. 9–18.

 Van den Ende, W. 2013. Multifunctional Fructans and Raffinose Family Oligosaccharides. Frontiers in Plant Science 4(247), p. 1–11.

 Van den Ende, W., De Coninck, B., & van Laere, A. 2004. Plant fructan exohydrolases: a role in signaling and defense? Trends in Plant Science 9, p. 523–528.

Van Loon, L.C., Rep, M., & Pieterse, C.M.J. 2005. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, p. 135–162.

Van Melckebeke, J. 1990. La lutte intégrée permet-elle de limiter l'utilisation de produits phytopharmaceutiques? Agricontact 23, p. 1-5.

van Wees, S.C.M., Van der Ent, S., & Pieterse, C.M.J. 2008. Plant immune responses triggered by beneficial microbes RID B-8595-2011 RID A-9326-2011. Curr. Opin. Plant Biol. 11, p. 443–448.

Veloso, J., García, T., Bernal, A., & Díaz, J. 2014. New bricks on the wall of induced resistance: Salicylic acid receptors and transgenerational priming. European Journal of Plant Pathology 138, p. 685-693.

Vereyken, I.J., Chupin, V., Demel, R.A., Smeekens, S.C.M., & De Kruijff, B. 2001. Fructans insert between the headgroups of phospholipids. Biochim. Biophys. Acta Biomem. 1510, p. 307–320.

Verhagen, B.W.M., Glazebrook, J., Zhu, T., Chang, H.S., van Loon, L.C., & Pieterse, C.M.J. 2004. The transcriptome of rhizobacteria-induced systemic resistance in Ara- bidopsis. Mol. Plant-Microbe Interact. 17, p. 895–908.

Versluys, M. 2016. Sweet Immunity in Tobacco: Sugar Priming against Botrytis Cinerea Infection. p. 1-71.

Versluys, M., Tarkowski, Ł.P., & Van den Ende, W. 2017. Fructans As DAMPs or MAMPs: Evolutionary Prospects, Cross-Tolerance, and Multistress Resistance Potential. Frontiers in Plant Science 7, p. 1–7.

Verspreet, J., Holmgaard Hanse, A., Harrison, S.J., Vergauwen, R., Van den Ende, W. & Courtin, C.M. 2017. Building a fructan LC–MS2 library and its application to reveal the fine structure of cereal grain fructans. Science 174, p. 343-351.

Vidhyasekaran, P. 2014c. Chapter 4: Calcium ion signaling system – calcium signatures and sensors. In: Vidhyasekaran, P. (Editor), PAMP signals in plant innate immunity, Springer, p. 207-282.

Vinatzer, B.A., Patocchi, A., Gianfranceschi, L., Tartarini, S., Zhang, H.-B., Gessler, C., & Sansavini, S. 2001. Apple contains receptor-like genes homologous to theCladosporium fulvumresistance gene family of tomatowith a cluster of genes cosegregating with Vf apple scab resistance. Molecular Plant- Microbe Interactions 14(4), p. 508–515.

VLAM Marketingdienst. 2017. Belgisch fruit: productie (in HA). Fruitbarometer 2017, p. 1.

VLAM Marketingdienst. 2017. Belgisch fruit: productie (in ton), Fruitbarometer 2017, p. 1.

VLAM. 2014. Het verbruik van agrovoedingsproducten in België in 2014. p. 2.

Voegele, R.T., Wirsel, S., Möll, U., Lechner, M., Mendgen, K. 2006. Cloning and characterization of a novel invertase from the obligate biotroph Uromyces fabae and analysis of expression patterns of host and pathogen invertases in the course of infection. Mol Plant Microbe Interact 19, p. 625–634.

Wulandari, N., To-Anun, C., Hyde, K., Duong, L., de Gruyter, J., Meffert, J., Groenewald, J., Crous, P. 2009. Phyllosticta citriasiana sp. nov., the cause of Citrus tan spot of Citrus maxima in Asia. Fungal Divers 34, p. 23–39.

Wagner, T.A., & Kohorn, B.D. 2001. Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13, p. 303–318.

Walton, J.D. 1994. Deconstructing the Cell Wall. Plant Physiol 104, p.1113-1118.

Wang, D., Pajerowska-Mukhtar, K., Culler, A.H., & Dong, X. 2007. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Current Biology 17(20), p. 1784-1790.

Wang, F., Feng, G., & Chen, K. 2009. Defense responses of harvested tomatofruit to burdock fructooligosaccharide, a novel potential elicitor. Postharv. Biol. Technol. 52, p. 110–116.

Wang, Z.-Y., Xiong, L., Li, W., Zhu, J.-K. & Zhu, J. 2011. The Plant Cuticle Is Required for Osmotic Stress Regulation of Abscisic Acid Biosynthesis and Osmotic Stress Tolerance in Arabidopsis. The Plant Cell 23, p. 1971–84.

Ward, E.R., Uknes, S.J., Williams, S.C., Dincher, S.S., Wied- erhold, D.L., Alexander, D.C., Ahl-Goy, P., Métraux, J.-P., & Ryals, J.A. 1991. Coordinated gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3, p. 1085–1094.

Way, R.D., Alwinckle, H.S., Lamb, R.C., Rejman, A., Sansavini, S., Shen, T., Watkins, R., Westwood, M.N., & Yoshida, Y. 1991. Apples (Malus). Acta Hort 290, p. 3–62.

Wiemken, A., Sprenger, N., & Boller, T. 1995. Fructan: an extension of sucrose by sucrose. Pontis, H.G. Salerno, G.L. & Echeverria, E.J. (Editors), Sucrose, Metabolism, Biochemistry, Physiology and Molecular Biology. Rockville,MD, USA: American Society of Plant Physiologists. p. 178–189.

Winkel-Shirley, B. 2001. Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126, p. 485–493.

Wittstock, U., & Gershenzon, J. 2002. Constitutive Plant Toxins and Their Role in Defense against Herbivores and Pathogens. Current Opinion in Plant Biology 5, p. 1–8.

Xiang, L., Le Roy, K., Bolouri-Moghaddam, M.R., Vanhaecke, M., Lammens, W., Rolland, F., & Van den Ende, W. 2011. Exploring the neutral invertase-oxidative stress defence connection in Arabidopsis thaliana. Journal of Experimental Botany 62, p. 3849–3862.

Xiong, L., & Zhu, J. 2003. Regulation of abscisic acid biosynthesis. Plant Physiology 133(1), p. 29-36.

Xu, H., & Mendgen, K. 1997. Targeted Cell Wall Degradation at the Penetration Site of Cowpea Rust Basidiosporelings. Molecular Plant - Microbe Interaction 10(1), p. 87–94.

Xu, M., & Korban, S.S. 2002. A cluster of four receptor-like genes resides in the Vf locus that confers resistance to apple scab disease. Genetics 162(4), p. 1995–2006.

Yasuda M., Ishikawa A., Jikumaru Y., et al. 2008. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. The Plant Cell 20, p. 1678–1692.

Yamada, K., Saijo, Y., Nakagami, H. & Takano, Y. 2016. Regulation of sugar transporter activity for antibacterial defense in Arabidopsis. Science 354, p. 1427–1430.

Yang, Y., Shah, J., & Klessig, D.F. 1997. Signal Perception and Transduction in Plant Defense Responses. GENES & DEVELOPMENT 11, p. 1621–39.

Yu, S.-M. 1999. Cellular and genetic responses of plants to sugar starvation. Plant Physiol. 121, p. 687–693.

Yun, B.W., Feechan, A. Yin, M., Saidi, N.B., Le Bihan, T., Yu, M., Moore, J.W., Kang, J.G., Kwon, E., Spoel, S.H., Pallas, J.A., & Loake, G.J. 2011. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478, p. 264–268.

Zhang, A.Y. Jiang, M.Y. Zhang, J.H. Tan, M.P. & Hu, Z.L. 2006. Mitogen- activated protein kinase is involved in abscisic acid-induced antioxidant defence and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiology 141, p. 475–487.

Zhang, P.Y., Wang, J.C., Liu, S.H., & Chen, K.S. 2009. A novel burdock fructooligosaccharide induces changes in the production of salicylates, activates defence enzymes and induces systemic acquired resistance to Colletotrichum orbiculare in cucumber seedlings. J. Phytopathol. 157, p. 201–207.

Zhang, T., Liu, Y., Yang, T., Zhang, L., Xu, S., Xue, L., & An, L. 2006. Diverse signals converge at MAPK cascades in plant. Plant Physiology and Biochemistry 44, p. 274–283.

Zucoloto, M., Ku, K.-M., Kim, M.-J., & Kushad, M. M. 2017. Influence of 1-Methylcyclopropene Treatment on Postharvest Quality of Four Scab ( Venturia Inaequalis ) -Resistant Apple Cultivars. Journal of Food Quality 2017, p. 1-12.

Universiteit of Hogeschool
Bio-ingenieurswetenschappen: landbouwkunde
Publicatiejaar
2018
Promotor(en)
Prof Keulemans en Prof Van den Ende
Kernwoorden
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