Skip to main content
Log in

The effects of grapevine trunk diseases (GTDs) on vine physiology

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Esca disease as well as Botryosphaeria and Eutypa dieback cause considerable economic problems for vineyards worldwide, and currently, no efficient treatment is available to control these diseases. For these three grapevine trunk diseases (GTDs), the main physiological effects reported concern carbohydrate metabolism and defence responses in the different organs of vine. In the trunk, a depletion of starch reserves in woody tissues is associated with fungal colonization; in the leaves, where pathogens are not present, the carbohydrate metabolism is also affected as revealed by a decline of the photosynthetic rate. A consequence of these disturbances is a lower pool of carbon reserves that might contribute to a decrease of plant development and vigour during the subsequent year. Other metabolic activities such as lipid and amino acid metabolism are down regulated. The perturbation of these primary metabolisms is often associated with the induction of defence responses. The development of biochemical barriers resulting from the accumulation of both tyloses and gummosis is observed during the infection of the wood causing blockage of the xylem vessels and thus limiting the fungal invasion. Their progression in the wood is also inhibited by the formation of polyphenol-rich reaction zones and by the accumulation of pathogenesis-related proteins, and the oxidative burst and the production of reactive oxygen species. Additionally, detoxification processes of the vine are involved; this reaction could be linked to the production of extracellular compounds by GTD agents some of which are phytotoxic. As a consequence, the sensory quality of berries and probably the wine made from these berries decrease. This review presents an overview of the physiological modifications described in vines affected by GTDs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abou-Mansour, E., Débieux, J.-L., Ramírez-Suero, M., Bénard-Gellon, M., Magnin-Robert, M., Spagnolo, A., et al. (2015). Phytotoxic metabolites from Neofusicoccum parvum, a pathogen of Botryosphaeria dieback of grapevine. Phytochemistry. doi:10.1016/j.phytochem.2015.01.012.

    PubMed  Google Scholar 

  • Agrelli, D., Amalfitano, C., Conte, P., & Mugnai, L. (2009). Chemical and spectroscopic characteristics of the wood of Vitis vinifera Cv. Sangiovese affected by esca disease. Journal of Agricultural and Food Chemistry, 57(24), 11469–11475. doi:10.1021/jf903561x.

    Article  CAS  PubMed  Google Scholar 

  • Almeida, F. (2007). Technical note 2 – “grapevine wood diseases—eutypa dieback and esca”. ADVID Technical Notes, 1–14.

  • Al-Whaibi, M. H. (2011). Plant heat-shock proteins: a mini review. Journal of King Saud University - Science, 23(2), 139–150. doi:10.1016/j.jksus.2010.06.022.

    Article  Google Scholar 

  • Amalfitano, C., Evidente, A., Surico, G., Tegli, S., Bertelli, E., & Mugnai, L. (2000). Phenols and stilbene polyphenols in the wood of esca-diseased grapevines. Phytopathologia Mediterranea, 39, 178–183.

    CAS  Google Scholar 

  • Amalfitano, C., Agrelli, D., Arrigo, A., Mugnai, L., Surico, G., & Evidente, A. (2011). Stilbene polyphenols in the brown red wood of Vitis vinifera cv. Sangiovese affected by “esca proper”. Phytopathologia Mediterranea, 50, S224–S235.

    Google Scholar 

  • Andolfi, A., Mugnai, L., Luque, J., Surico, G., Cimmino, A., & Evidente, A. (2011). Phytotoxins produced by fungi associated with grapevine trunk diseases. Toxins, 3(12), 1569–1605. doi:10.3390/toxins3121569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arimura, G., Ozawa, R., Nishioka, T., Boland, W., Koch, T., Kuhnemann, F., et al. (2002). Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant Journal, 29(1), 87–98. doi:10.1046/j.1365-313x.2002.01198.x.

    Article  CAS  PubMed  Google Scholar 

  • Baker, N. R., Nogués, S., & Allen, D. J. (1997). Photosynthesis and photoinhibition. In P. J. Lumsden (Ed.), Plants and UV-B: responses to environmental change (pp. 95–111). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Baskarathevan, J., Jaspers, M. V., Jones, E. E., & Ridgway, H. J. (2012). Incidence and distribution of botryosphaeriaceous species in New Zealand vineyards. European Journal of Plant Pathology, 132(4), 549–560. doi:10.1007/s10658-011-9900-5.

    Article  Google Scholar 

  • Berger, S., Sinha, A. K., & Roitsch, T. (2007). Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. Journal of Experimental Botany, 58(15–16), 4019–4026. doi:10.1093/jxb/erm298.

    Article  CAS  PubMed  Google Scholar 

  • Bertsch, C., Ramirez-Suero, M., Magnin-Robert, M., Larignon, P., Chong, J., Abou-Mansour, E., et al. (2013). Grapevine trunk diseases: complex and still poorly understood. Plant Pathology, 62(2), 243–265. doi:10.1111/j.1365-3059.2012.02674.x.

    Article  Google Scholar 

  • Bolton, M. D. (2009). Primary metabolism and plant defence-fuel for the fire. Molecular Plant-Microbe Interactions, 22(5), 487–497. doi:10.1094/mpmi-22-5-0487.

    Article  CAS  PubMed  Google Scholar 

  • Bruez, E., Grosman Jacques, L. P., Bruno, D., Bertsch, C., Fontaine, F., Ugaglia, A., Teissedre, P.-L., Da Costa Jean-Pierre, G.-D. L., & Patrice, R. (2013). Overview of grapevine trunk diseases in France in the 2000s. Phytopathologia Mediterranea, 52(2), 262–275.

    Google Scholar 

  • Bruez, E., Vallance, J., Gerbore, J., Lecomte, P., Da Costa, J.-P., Guerin-Dubrana, L., et al. (2014). Analyses of the temporal dynamics of fungal communities colonizing the healthy wood tissues of esca leaf-symptomatic and asymptomatic vines. Plos One, 9(5), doi:10.1371/journal.pone.0095928.

  • Calzarano, F., Cichelli, A., & Odoardi, M. (2001). Preliminary evaluation of variations in composition induced by esca on cv. Trebbiano d’Abruzzo grapes and wines. Phytopathologia Mediterranea, 40, 443–448.

    Google Scholar 

  • Calzarano, F., Seghetti, L., Del Carlo, M., & Cichelli, A. (2004). Effect of esca on the quality of berries, musts and wines. Phytopathologia Mediterranea, 43(1), 125–135.

    CAS  Google Scholar 

  • Calzarano, F., Amalfitano, C., Seghetti, L., & D’Agostino, V. (2007). Foliar treatment of esca-proper affected vines with nutrients and bioactivators. Phytopathologia Mediterranea, 44, 207–217.

    Google Scholar 

  • Calzarano, F., D’Agostino, V., & Del Carlo, M. (2008). Trans-resveratrol extraction from grapevine: application to berries and leaves from vines affected by esca proper. Analytical letters 41, 1-13.

  • Calzarano, F., Di Marco, S., D’Agostino, V., Schiff, S., & Mugni, L. (2014). Grapevine leaf stripe disease symtpoms (esca complex) are reduced by a nutrients and seaweed mixture. Phytopathologia Mediterranea, 53(3), 543–558.

    Google Scholar 

  • Camps, C., Kappel, C., Lecomte, P., Leon, C., Gomes, E., Coutos-Thevenot, P., et al. (2010). A transcriptomic study of grapevine (Vitis vinifera cv. Cabernet-Sauvignon) interaction with the vascular ascomycete fungus Eutypa lata. Journal of Experimental Botany, 61(6), 1719–1737. doi:10.1093/jxb/erq040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiarappa, L. (1959). Wood decay of the grapevine and its relationship with black measles disease. Phytopathology, 49(8), 510–519.

    Google Scholar 

  • Christen, D. (2006). Towards an integrative management of eutypa dieback and esca disease of grapevine. Thesis of the Swiss Federal Institute of Technology, Zurich, Switzerland.

  • Christen, D., Schonmann, S., Jermini, M., Strasser, R. J., & Defago, G. (2007). Characterization and early detection of grapevine (Vitis vinifera) stress responses to esca disease by in situ chlorophyll fluorescence and comparison with drought stress. Environmental and Experimental Botany, 60(3), 504–514. doi:10.1016/j.envexpbot.2007.02.003.

    Article  CAS  Google Scholar 

  • Colditz, F., Niehaus, K., & Krajinski, F. (2007). Silencing of PR-10-like proteins in Medicago truncatula results in an antagonistic induction of other PR proteins and in an increased tolerance upon infection with the oomycete Aphanomyces euteiches. Planta, 226(1), 57–71. doi:10.1007/s00425-006-0466-y.

    Article  CAS  PubMed  Google Scholar 

  • Constabel, C. P., Bergey, D. R., & Ryan, C. A. (1995). Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defence signaling pathway. Proceedings of the National Academy of Sciences of the United States of America, 92(2), 407–411. doi:10.1073/pnas.92.2.407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deytieux, C., Geny, L., Lapaillerie, D., Claverol, S., Bonneu, M., & Doneche, B. (2007). Proteome analysis of grape skins during ripening. Journal of Experimental Botany, 58(7), 1851–1862. doi:10.1093/jxb/erm049.

    Article  CAS  PubMed  Google Scholar 

  • Di Marco, S., & Osti, F. (2009). Effect of biostimulant sprays on Phaeomoniella chlamysdospora and esca proper infected vines under greenhouse and field conditions. Phytopathologia Mediterranea, 48, 1150–1157.

    Google Scholar 

  • Di Marco, S., Osti, F., Calzarano, F., Roberti, R., Veronesi, A., & Amalfitnao, C. (2011). Effects of grapevine applications of fosetyl-aluminium formulations for downy mildew control on “esca” and associated fungi. Phytopathologia Mediterranea, 50S, S285–S299.

    Google Scholar 

  • Diaz, G. A., Auger, J., Besoain, X., Bordeu, E., & Latorre, B. A. (2013). Prevalence and pathogenicity of fungi associated with grapevine trunk diseases in Chilean vineyards. Ciencia E Investigacion Agraria, 40(2), 327–339.

    Article  Google Scholar 

  • Dixon, R. A., Achnine, L., Kota, P., Liu, C. J., Reddy, M. S. S., & Wang, L. J. (2002). The phenylpropanoid pathway and plant defence - a genomics perspective. Molecular Plant Pathology, 3(5), 371–390. doi:10.1046/j.1364-3703.2002.00131.x.

    Article  CAS  PubMed  Google Scholar 

  • Edwards, J., Marchi, G., & Pascoe, I. (2001). Young esca in Australia. Phytopathologia Mediterranea, 40, S303–S310.

    Google Scholar 

  • Edwards, J., Salib, S., Thomson, F., & Pascoe, I. G. (2007a). The impact of Phaemoniella chlamydospora infection on the grapevine’s physiological response to water stress part 1: Zinfandel. Phytopathologia Mediterranea, 46, 26–37.

    Google Scholar 

  • Edwards, J., Salib, S., Thomson, F., & Pascoe, I. G. (2007b). The impact of Phaeomoniella chlamydospora infection on the grapevine’s physiological response to water stress part 2: Cabernet Sauvignon and Chardonnay. Phytopathologia Mediterranea, 46, 38–49.

    Google Scholar 

  • Felgueiras, M. L., Chicau, G., Moutinho-Pereira, J. M., & Dias, A. C. P. (2007). Effects of esca disease on leaf gas exchanges of cv. Alvarinho in a vineyard of the Portuguese Vinho Verde Region. Phytopathologia Mediterranea, 46(1), 119–119.

    Google Scholar 

  • Feliciano, A., Eskalen, A., & Gubler, W. (2004). Differential susceptibility of three grapevine cultivars to Phaeoacremonium aleophilum and Phaeomoniella chlamydospora in California. Phytopathologia Mediterranea, 43, 66–69.

    Google Scholar 

  • Fleurat-Lessard, P., Bourbouloux, A., Thibault, F., Menard, E., Bere, E., Valtaud, C., et al. (2013). Differential occurrence of suberized sheaths in canes of grapevines suffering from black dead arm, esca or Eutypa dieback. Trees-Structure and Function, 27(4), 1087–1100. doi:10.1007/s00468-013-0859-z.

    Article  Google Scholar 

  • Frova, C. (2003). The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiologia Plantarum, 119(4), 469–479. doi:10.1046/j.1399-3054.2003.00183.x.

    Article  CAS  Google Scholar 

  • Graniti, A., Surico, G., & Mugnai, L. (2000). Esca of grapevine: a disease complex or a complex diseases? Phytopathologia Mediterranea, 39, 16–20.

    Google Scholar 

  • Grant, O. M., Tronina, L., Jones, H. G., & Chaves, M. M. (2007). Exploring thermal imaging variables for the detection of stress responses in grapevine under different irrigation regimes. Journal of Experimental Botany, 58(4), 815–825. doi:10.1093/jxb/erl153.

    Article  CAS  PubMed  Google Scholar 

  • Grosman, J. D. B. (2012). Maladie du bois de la vigne – Synthèse des dispositifs d’observation au vignoble, de l’observatoire 2003–2008 au résau d’épidemiosurveillance actuel. Phytoma, 651(2), 31–34.

    Google Scholar 

  • Gubler, W., Rolshausen, P., Trouillas, F., Urbez, J., Voegel, T., Leavitt, G., et al. (2005). Grapevine trunk diseases in California. Pratical Winery and Vineyard Magazine, 6–25.

  • Gurley, W. B. (2000). HSP101: a key component for the acquisition of thermotolerance in plants. The Plant Cell, 12(4), 457–460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hofstetter, V., Buyck, B., Croll, D., Viret, O., Couloux, A., & Gindro, K. (2012). What if esca disease of grapevine were not a fungal disease? Fungal Diversity, 54(1), 51–67. doi:10.1007/s13225-012-0171-z.

    Article  Google Scholar 

  • Hussain, S. S., Ali, M., Ahmad, M., & Siddique, K. H. M. (2011). Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnology Advances, 29(3), 300–311. doi:10.1016/j.biotechadv.2011.01.003.

    Article  CAS  PubMed  Google Scholar 

  • Kortekamp, A. (2006). Expression analysis of defence-related genes in grapevine leaves after inoculation with a host and a non-host pathogen. Plant Physiology and Biochemistry, 44(1), 58–67. doi:10.1016/j.plaphy.2006.01.008.

    Article  CAS  PubMed  Google Scholar 

  • Koussa, T., Dubos, B., & Cherrad, M. (2002). Les teneurs en acides gras, en eau et en acide abscissique des feuilles de vigne (Vitis vinifera L. var. Cabernet Sauvignon) infectées par Eutypa lata. Vitis, 43, 143–146.

    Google Scholar 

  • Lambert, C., Bisson, J., Waffo-Teguo, P., Papastamoulis, Y., Richard, T., Corio-Costet, M. F., et al. (2012). Phenolics and their antifungal role in grapevine wood decay: focus on the Botryosphaeriaceae family. Journal of Agricultural and Food Chemistry, 60(48), 11859–11868. doi:10.1021/jf303290g.

    Article  CAS  PubMed  Google Scholar 

  • Lambert, C. K. K. I., Lucas, S., Télef-Micoleau, N., Mérillon, J.-M., & Cluzet, S. (2013). A faster and stronger defence response: one of the key elements in grapevine explaining its lower susceptibility to esca? Phytopathology, 103(10), 1028–1034.

    Article  CAS  PubMed  Google Scholar 

  • Larignon, P., & Dubos, B. (1997). Fungi associated with esca disease in grapevine. European Journal of Plant Pathology, 103(2), 147–157. doi:10.1023/a:1008638409410.

    Article  Google Scholar 

  • Larignon, P. F. R., Cere, L., & Dubos, B. (2001). Observation on black dead arm in French vineyards. Phytopathologia Mediterranea, 40S(3), 336–342.

    Google Scholar 

  • Larignon, P. F. F., Farine, S., Clément, C., & Bertsch, C. (2009). Esca et black dead arm: deux acteurs majeurs des maladies du bois chez la vigne. Comptes Rendus de l’Académie des Sciences III-Vie, 333(9), 765–783.

    Google Scholar 

  • Leavitt, G. (1991). Diseases. In: Grape pest management, 2nd Ed., Univ. of California IPM Manual. Flaherty, D., et al. (eds), Chapter 22, 162–172.

  • Lebon, G., Wojnarowiez, G., Holzapfel, B., Fontaine, F., Vaillant-Gaveau, N., & Clement, C. (2008). Sugars and flowering in the grapevine (Vitis vinifera L.) (vol 59, pg 2565, 2008). Journal of Experimental Botany, 59(15), doi:10.1093/jxb/ern325.

  • Lecomte, P., Darrieutort, G., Liminana, J. M., Comont, G., Muruamendiaraz, A., Legorburu, F. J., et al. (2012). New insights into esca of grapevine: the development of foliar symptoms and their association with xylem discoloration. Plant Disease, 96(7), 924–934. doi:10.1094/pdis-09-11-0776-re.

    Article  Google Scholar 

  • Letousey, P., Baillieul, F., Perrot, G., Rabenoelina, F., Boulay, M., Vaillant-Gaveau, N., et al. (2010). Early events prior to visual symptoms in the apoplectic form of grapevine esca disease. Phytopathology, 100(5), 424–431. doi:10.1094/phyto-100-5-0424.

    Article  CAS  PubMed  Google Scholar 

  • Lima, M. R. M., Felgueiras, M. L., Graca, G., Rodrigues, J. E. A., Barros, A., Gil, A. M., et al. (2010). NMR metabolomics of esca disease-affected Vitis vinifera cv. Alvarinho leaves. Journal of Experimental Botany, 61(14), 4033–4042. doi:10.1093/jxb/erq214.

    Article  CAS  PubMed  Google Scholar 

  • Lima, M. R. M., Ferreres, F., & Dias, A. C. P. (2012). Response of Vitis vinifera cell cultures to Phaeomoniella chlamydospora: changes in phenolic production, oxidative state and expression of defence-related genes. European Journal of Plant Pathology, 132(1), 133–146. doi:10.1007/s10658-011-9857-4.

    Article  CAS  Google Scholar 

  • Lorrain, B., Ky, I., Pasquier, G., Jourdes, M., Dubrana, L. G., Geny, L., et al. (2012). Effect of Esca disease on the phenolic and sensory attributes of Cabernet Sauvignon grapes, musts and wines. Australian Journal of Grape and Wine Research, 18(1), 64–72. doi:10.1111/j.1755-0238.2011.00172.x.

    Article  CAS  Google Scholar 

  • Luque, J., Elena, G., Garcia-Figueres, F., Reyes, J., Barrios, G., & Legorburu, F. J. (2014). Natural infections of pruning wounds by fungal trunk pathogens in mature grapevines in Catalonia (Northeast Spain). Australian Journal of Grape and Wine Research, 20(1), 134–143. doi:10.1111/ajgw.12046.

    Article  Google Scholar 

  • Magnin-Robert, M., Letousey, P., Spagnolo, A., Rabenoelina, F., Jacquens, L., Mercier, L., Clément, C., & Fontaine, F. (2011). Leaf strip of esca induces alteration of photosynthesis and defence reactions in presymptomatic leaves. Functional Plant Biology, 38(11), 856–866.

    Article  CAS  Google Scholar 

  • Magnin-Robert, M., Spagnolo, A., Alayi, T. D., Cilindre, C., Mercier, L., Schaeffer-Reiss, C., Van Dorsselaer, A., Clément, C., & Fontaine, F. (2014). Proteomic insights into changes in wood of Vitis vinifera L. in response to esca proper and apoplexy. Phytopathologia Mediterranea, 53, 173–192.

    Google Scholar 

  • Maimbo, M., Ohnishi, K., Hikichi, Y., Yoshioka, H., & Kiba, A. (2007). Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defence response against Ralstonia solanacearum(1 W). Plant Physiology, 145(4), 1588–1599. doi:10.1104/pp. 107.105353.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchi, G., Peduto, F., Mugnai, L., Di Marco, S., Calzarano, F., & Surico, G. (2006). Some observations on the relationship of manifest and hidden esca to rainfall. Phytopathologia Mediterranea, 45, 117–S126.

    Google Scholar 

  • Martin, M., & Cobos, R. (2007). Identification of fungi associated with grapevine decline in Castilla y Léon (Spain). Phytopathologia Mediterranea, 46, 18–25.

    Google Scholar 

  • Möller, W. J., Kasimatis, A. N., & Kissler, J. J. (1974). A dying arm disease of grape in California. Plant Disease Reporter, 58, 869–871.

    Google Scholar 

  • Möller, M., Alchantis, V., Cohen, Y., Meron, M., Tsipris, J., Naor, A., et al. (2007). Use of thermal and visible imagery for estimating crop water status of irrigation grapevine. Journal of Experimental Botany, 58, 827–838.

    Article  PubMed  Google Scholar 

  • Monteiro, S., Barakat, M., Picarra-Pereira, M. A., Teixeira, A. R., & Ferreira, R. B. (2003). Osmotin and thaumatin from grape: a putative general defence mechanism against pathogenic fungi. Phytopathology, 93(12), 1505–1512. doi:10.1094/phyto.2003.93.12.1505.

    Article  CAS  PubMed  Google Scholar 

  • Morales, A., Latorre, B. A., Piontelli, E., & Besoain, X. (2012). Botryosphaeriaceae species affecting table grape vineyards in Chile and cultivar susceptibility. Ciencia E Investigacion Agraria, 39(3), 445–458.

    Article  Google Scholar 

  • Mugnai, L., Graniti, A., & Surico, G. (1999). Esca (Black measles) and brown wood-streaking: two old and elusive diseases of grapevines. Plant Disease, 83(5), 404–418. doi:10.1094/pdis.1999.83.5.404.

    Article  Google Scholar 

  • Murolo, S., & Romanazzi, G. (2014). Effects of grapevine cultivar, rootstock and clone on esca disease. Australasian Plant Pathology, 43(2), 215–221. doi:10.1007/s13313-014-0276-9.

    Article  CAS  Google Scholar 

  • Pasquier, G., Lapaillerie, D., Vilain, S., Dupuy, J.-W., Lomenech, A.-M., Claverol, S., et al. (2013). Impact of foliar symptoms of “Esca proper” on proteins related to defence and oxidative stress of grape skins during ripening. Proteomics, 13(1), 108–118. doi:10.1002/pmic.201200194.

    Article  CAS  PubMed  Google Scholar 

  • Petit, A. N., Vaillant, N., Boulay, M., Clement, C., & Fontaine, F. (2006). Alteration of photosynthesis in grapevines affected by esca. Phytopathology, 96(10), 1060–1066. doi:10.1094/phyto-96-1060.

    Article  CAS  PubMed  Google Scholar 

  • Petit, A. N., Baillieul, F., Vaillant-Gaveau, N., Jacquens, L., Conreux, A., Jeandet, P., et al. (2009). Low responsiveness of grapevine flowers and berries at fruit set to UV-C irradiation. Journal of Experimental Botany, 60(4), 1155–1162. doi:10.1093/jxb/ern361.

    Article  CAS  PubMed  Google Scholar 

  • Philippe, I., Fallot, J., Petitprez, M., & Dargent, R. (1992). Effets de l’eutypiose sur les feuilles de Vitis vinifera cv. Cabernet Sauvignon. Etude cytologique. Vitis, 31, 45–53.

    Google Scholar 

  • Pouzoulet, J., Pivovaroff, A. L., Santiago, L. S., & Rolshausen, P. E. (2014). Can vessel dimension explain tolerance toward fungal vascular wilt diseases in woody plants? Lessons from Dutch elm disease and esca disease in grapevine. Frontiers in Plant Science, 5, doi: 10.3389/fpls.2014.00253.

  • Rifai, L. A., Koussa, T., Geny, L., Fassouane, A., Broquedis, M., & Dubos, B. (2005). Evolution des teneurs en polyamines libres et conjuguées dans les feuilles de vigne (Vitis vinifera ‘Cabernet Sauvignon’) saine et atteinte d’eutypiose. Canadian Journal of Botany, 83, 194–201.

    Article  CAS  Google Scholar 

  • Rojas, C. M., Senthil-Kumar, M., Tzin, V., & Mysore, K. S. (2014). Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defence. Frontiers in Plant Science, 5, doi:10.3389/fpls.2014.00017.

  • Roje, S. (2006). S-Adenosyl-L-methionine: Beyond the universal methyl group donor. Phytochemistry, 67(15), 1686–1698. doi:10.1016/j.phytochem.2006.04.019.

    Article  CAS  PubMed  Google Scholar 

  • Santos, C., Fragoeiro, S., & Phillips, A. (2005). Physiological response of grapevine cultivars and a rootstock to infection with Phaeoacremonium and Phaeomoniella isolates: an in vitro approach using plants and calluses. Scientia Horticulturae, 103(2), 187–198. doi:10.1016/j.scienta.2004.04.023.

    Article  CAS  Google Scholar 

  • Shigo, A. L. (1982). A codit view of tree cankers. Phytopathology, 72(2), 265–265.

    Google Scholar 

  • Spagnolo, A., Magnin-Robert, M., Alayi, T. D., Cilindre, C., Mercier, L., Schaeffer-Reiss, C., et al. (2012). Physiological changes in green stems of Vitis vinifera L. cv. Chardonnay in response to esca proper and apoplexy revealed by proteomic and transcriptomic analyses. Journal of Proteome Research, 11(1), 461–475. doi:10.1021/pr200892g.

    Article  CAS  PubMed  Google Scholar 

  • Spagnolo, A., Magnin-Robert, M., Alayi, T. D., Cilindre, C., Schaeffer-Reiss, C., Van Dorsselaer, A., Clément, C., Larignon, P., Suero-Ramirez, M., Chong, J., Bertsch, C., Abou-Mansour, E., & Fontaine, F. (2014a). Differential responses of three grapevine cultivars to Botryosphaeria dieback. Phytopathology. doi:10.1094/PHYTO-01-14-0007-R.

    PubMed  Google Scholar 

  • Spagnolo, A., Larignon, P., Magnin-Robert, M., Hovasse, A., Cilindre, C., Van Dorsselaer, A., Clément, C., Schaeffer-Reiss, C., & Fontaine, F. (2014b). Flowering as the most highly sensitive period of grapevine (Vitis vinifera L. cv Mourvèdre) to the Botryosphaeria dieback agents Neofusicoccum parvum and Diplodia seriata infection. International Journal of Molecular Sciences, 15, 9644–9669. doi:10.3390/ijms15069644.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Surico, G. (2009). Towards a redefinition of the disease within the esca complex of grapevine. Phytopathologia Mediterranea, 48, 5–10.

    Google Scholar 

  • Surico, G. M. L., & Marchi, G. (2006). Older and more recent observations on esca: a critical review. Phytopathologia Mediterranea, 45, S68–S86.

    Google Scholar 

  • Surico, G., Bandinelli, R., Braccinni, P., Marco, S., Marchi, G., Mugnai, L., & Parrini, C. (2004). On the factors that may have influenced the esca epidemic in Tuscany in the eighties. Phytopathologia Mediterranea, 43, 136–143.

    Google Scholar 

  • Surico, G., Mugnai, L., & Marchi, G. (2008). The esca disease complex. In A. Ciancio & K. Mukerji (Eds.), Integrated management of diseases caused by fungi, phytoplama and bacteria (pp. 119–136). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Thipyapong, P., Hunt, M. D., & Steffens, J. C. (1995). Systemic wound induction of potato (Solanum tuberosum) polyphenol oxidase. Phytochemistry, 40(3), 673–676. doi:10.1016/0031-9422(95)00359-f.

    Article  CAS  Google Scholar 

  • Thipyapong, P., Stout, M. J., & Attajarusit, J. (2007). Functional analysis of polyphenol oxidases by antisense/sense technology. Molecules, 12(8), 1569–1595. doi:10.3390/12081569.

    Article  CAS  PubMed  Google Scholar 

  • Tsunezuka, H., Fujiwara, M., Kawasaki, T., & Shimamoto, K. (2005). Proteome analysis of programmed cell death and defence signaling using the rice lesion mimic mutant cdr2. Molecular Plant-Microbe Interactions, 18(1), 52–59. doi:10.1094/mpmi-18-0052.

    Article  CAS  PubMed  Google Scholar 

  • Tuzun, S., & Somanchi, A. (2006). The possible role of PR proteins in multigenic and induced systemic resistance. In S. Tuzun & E. Bent (Eds.), Multigenic and induced systemic resistance in plants (pp. 112–142). New York: Springer.

    Chapter  Google Scholar 

  • Úrbez-Torres, J. R. (2011). The status of Botryosphaeriaceae species infecting grapevines. Phytopathologia Mediterranea, 50, S5–S45.

    Google Scholar 

  • Úrbez-Torres, J. R., Haag, P., Bowen, P., & O’Gorman, D. T. (2014). Grapevine trunk diseases in British Columbia: incidence and characterization of the fungal pathogens associated with esca and petri diseases of grapevine. Plant Disease, 98(4), 469–482. doi:10.1094/pdis-05-13-0523-re.

    Article  Google Scholar 

  • Valtaud, C. F. C., Fleurat-Lessard, P., & Bourbouloux, A. (2009a). Systemic effects on leaf glutathione metabolism and defence protein expression caused by esca infection in grapevines. Function Plant Biology, 36(3), 260–279.

    Article  CAS  Google Scholar 

  • Valtaud, C., Larignon, P., Roblin, G., & Fleurat-Lessard, P. (2009b). Developmental and ultrastructural features of Phaeomoniella chlamydospora and Phaeoacremonium aleophilum in relation to xylem degradation in esca disease of the grapevine. Journal of Plant Pathology, 91(1), 37–51.

    CAS  Google Scholar 

  • Valtaud, C., Thibault, F., Larignon, P., Berstch, C., Fleurat-Lessard, P., & Bourbouloux, A. (2011). Systemic damage in leaf metabolism caused by esca infection in grapevines. Australian Journal of Grape and Wine Research, 17(1), 101–110. doi:10.1111/j.1755-0238.2010.00122.x.

    Article  Google Scholar 

  • van Loon, L. C., Rep, M., & Pieterse, C. M. J. (2006). Significance of inducible defence-related proteins in infected plants. In Annual Review of Phytopathology (Vol. 44, pp. 135–162, Annual Review of Phytopathology). Palo Alto: Annual Reviews.

  • van Niekerk, J. M., Crous, P. W., Groenewald, J. Z., Fourie, P. H., & Halleen, F. (2004). DNA phylogeny, morphology and pathogenicity of Botryosphaeria species on grapevines. Mycologia, 96(4), 781–798. doi:10.2307/3762112.

    Article  PubMed  Google Scholar 

  • Waters, E. R., Lee, G. J., & Vierling, E. (1996). Evolution, structure and function of the small heat shock proteins in plants. Journal of Experimental Botany, 47(296), 325–338. doi:10.1093/jxb/47.3.325.

    Article  CAS  Google Scholar 

  • White, C. L. (2010). The characterization of the Basidiomycetes and other fungi asscoiated with esca of grapevines in South Africa. Thesis, Stelleboch University, South Africa.

  • Yan, J. Y., Xie, Y., Zhang, W., Wang, Y., Liu, J. K., Hyde, K. D., et al. (2013). Species of Botryosphaeriaceae involved in grapevine dieback in China. Fungal Diversity, 61(1), 221–236. doi:10.1007/s13225-013-0251-8.

    Article  Google Scholar 

  • Yang, L. T., Lin, H., Takahashi, Y., Chen, F., Walker, M. A., & Civerolo, E. L. (2011). Proteomic analysis of grapevine stem in response to Xylella fastidiosa inoculation. Physiological and Molecular Plant Pathology, 75(3), 90–99. doi:10.1016/j.pmpp.2010.11.002.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financed by the CASDAR programme V1301 (Compte d’Affectation Spécial au Développement Agricole et Rural), the Interprofessionnal institute “Interloire”, FranceAgriMer, FEDER – COMPETE, through “Quadro de Referência Estratégico Nacional” - QREN, with the reference FCOMP-01-0202-FEDER-011498, and within the project FCOMP-01-0124-FEDER-008749, which is financed with funds from FEDER through the “Programa Operacional Factores de Competitividade” – COMPETE, FCT. We thank Richard Smart, a native speaker and a vine consultant, to revise and improve the English of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Florence Fontaine.

Additional information

This article is part of Topical Collection on Special Issue on Fungal Grapevine Diseases

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fontaine, F., Pinto, C., Vallet, J. et al. The effects of grapevine trunk diseases (GTDs) on vine physiology. Eur J Plant Pathol 144, 707–721 (2016). https://doi.org/10.1007/s10658-015-0770-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-015-0770-0

Keywords

Navigation