Ancestral chemotypes of cultivated grapevine with resistance to Botryosphaeriaceae-related dieback allocate metabolism towards bioactive stilbenes.
Neofusicoccum parvum
Vitis resistance
phenylpropanoid pathway
piceid chemotype
resveratrol-viniferin chemotype
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
21
04
2020
accepted:
24
08
2020
pubmed:
9
9
2020
medline:
15
5
2021
entrez:
8
9
2020
Statut:
ppublish
Résumé
Grapevine trunk diseases have devastating consequences on vineyards worldwide. European wild grapevines (Vitis vinifera subs. sylvestris) from the last viable population in Germany along the Rhine river showed variable degrees of resistance against Neofusicoccum parvum (strain Bt-67), a fungus associated with Botryosphaeriaceae-related dieback. Representative genotypes from different subclades of this population were mapped with respect to their ability to induce wood necrosis, as well as their defence responses in a controlled inoculation system. The difference in colonization patterns could be confirmed by cryo-scanning electron microscopy, while there was no relationship between vessel diameter and infection success. Resistant lines accumulated more stilbenes, that were in addition significantly partitioned to nonglycosylated viniferin trimers. By contrast, the susceptible genotypes accumulated less stilbenes with a significantly higher proportion of glycosylated piceid. We suggest a model in which in the resistant genotypes phenylpropanoid metabolism is channelled rapidly and specifically to the bioactive stilbenes. Our study specifies a resistant chemotype against grapevines trunk diseases and paves a way to breed for resistance against grapevine Botryosphaeriaceae-related dieback.
Substances chimiques
Stilbenes
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1133-1146Informations de copyright
© 2020 The Authors New Phytologist © 2020 New Phytologist Trust.
Références
Adrian M, Jeandet P. 2012. Effects of resveratrol on the ultrastructure of Botrytis cinerea conidia and biological significance in plant/pathogen interactions. Fitoterapia 83: 1345-1350.
Alonso-Villaverde V, Voinesco F, Viret O, Spring JL, Gindro K. 2011. The effectiveness of stilbenes in resistant Vitaceae: ultrastructural and biochemical events during Plasmopara viticola infection process. Plant Physiology and Biochemistry 49: 265-274.
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.
Arend M, Weisenseel MH, Brummer M, Osswald W, Fromm JH. 2002. Seasonal changes of plasma membrane H+-ATPase and endogenous ion current during cambial growth in poplar plants. Plant Physiology 129: 1651-1663.
Arroyo-García R, Ruiz-García L, Bolling L, Ocete R, López MA, Arnold C, Ergul A, Söylemezo'lu G, Uzun HI, Cabello F.et al. 2006. Multiple origins of cultivated grapevine (Vitis vinifera L. ssp. sativa) based on chloroplast DNA polymorphisms. Molecular Ecology 15: 3707-3714.
Bacete L, Mélida H, Miedes E, Molina A. 2018. Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. The Plant Journal 93: 614-636.
Barnes W, Anderson C. 2017. Acetyl bromide soluble lignin (ABSL) assay for total lignin quantification from plant biomass. Bio-Protocol 7: 1-11.
Baskarathevan J. 2011. Botryosphaeriaceous infection in New Zealand vineyards: identification, population structure and genetic diversity. PhD thesis, Lincoln University, New Zealand.
Bertsch C, Ramírez-Suero M, Magnin-Robert M, Larignon P, Chong J, Abou-Mansour E, Spagnolo A, Clément C, Fontaine F. 2013. Grapevine trunk diseases: complex and still poorly understood. Plant Pathology 62: 243-265.
Breuil AC, Jeandet P, Adrian M, Chopin F, Pirio N, Meunier P, Bessis R. 1999. Characterization of a pterostilbene dehydrodimer produced by laccase of Botrytis cinerea. Phytopathology 89: 298-302.
Coakley SM, Scherm H, Chakraborty S. 1999. Climate change and plant disease management. Annual Review of Phytopathology 37: 399-426.
European Commission. 2009. Regulation (EC) no 552/2009 of 22 June 2009 amending Regulation (EC) no 1907/2006 of the European Parliament and of the Council on the Registration, Evaluation, Authorisation and Restriction of Chemicals (REACH) as regards annex XVII. URL http://data.europa.eu/eli/reg/2009/552/oj. Brussels, Belgium: European Commission..
Cota-Sánchez JH, Remarchuk K, Ubayasena K. 2006. Ready-to-use DNA extracted with a CTAB method adapted for herbarium specimens and mucilaginous plant tissue. Plant Molecular Biology Reporter 24: 161-167.
Dai GH, Andary C, Mondolot-Cosson L, Boubals D. 1995. Histochemical studies on the interaction between three species of grapevine, Vitis vinifera, V. rupestris and V. rotundifolia and the downy mildew fungus, Plasmopara viticola. Physiological and Molecular Plant Pathology 46: 177-188.
Djoukeng JD, Polli S, Larignon P, Abou-Mansour E. 2009. Identification of phytotoxins from Botryosphaeria obtusa, a pathogen of black dead arm disease of grapevine. European Journal of Plant Pathology 124: 303-308.
Duan D, Fischer S, Merz P, Bogs J, Riemann M, Nick P. 2016. An ancestral allele of grapevine transcription factor MYB14 promotes plant defence. Journal of Experimental Botany 67: 1795-1804.
Duan D, Halter D, Baltenweck R, Tisch C, Tröster V, Kortekamp A, Hugueney P, Nick P. 2015. Genetic diversity of stilbene metabolism in Vitis sylvestris. Journal of Experimental Botany 66: 3243-3257.
Fontaine F, Gramaje D, Armengol J, Smart R, Nagy ZA, Borgo M, Rego C, Corio-Costet M-F. 2016. Grapevine trunk diseases. A review. International Organisation of Vine and Wine (OIV), (December), 25. [WWW document] URL http://www.oiv.int/public/medias/4650/trunk-diseases-oiv-2016.
Gerlach D. 1977. Botanische Mikrotechnik Eine Einführung. 2, überarbeitete und erweiterte Auflage. XII + 311 S., 45 Abb. Georg Thieme Verlag. Stuttgart, ISBN 3-13-444902-1. Feddes Repertorium 89: 99-100.
Gómez P, Báidez AG, Ortuño A, Del Río JA. 2016. Grapevine xylem response to fungi involved in trunk diseases. Annals of Applied Biology 169: 116-124.
Guan P, Schmidt F, Riemann M, Fischer J, Thines E, Nick P. 2020. Hunting modulators of plant defence: the grapevine trunk disease fungus Eutypa lata secretes an amplifier for plant basal immunity. Journal of Experimental Botany 71: 3710-3724.
Guan X, Essakhi S, Laloue H, Nick P, Bertsch C, Chong J. 2016. Mining new resources for grape resistance against Botryosphaeriaceae: a focus on Vitis vinifera subsp. sylvestris. Plant Pathology 65: 273-284.
Jiao Y, Xu W, Duan D, Wang Y, Nick P. 2016. A stilbene synthase allele from a Chinese wild grapevine confers resistance to powdery mildew by recruiting salicylic acid signalling for efficient defence. Journal of Experimental Botany 67: 5841-5856.
Jones J, Dangl J. 2006. The plant immune system. Nature 444: 323-329.
Kelloniemi J, Trouvelot S, Heloir M-C, Simon A, Dalmais B, Frettinger P, Cimerman A, Fermaud M, Roudet J, Baulande Set al. 2015. Analysis of the molecular dialogue between Gray Mold (Botrytis cinerea) and Grapevine (Vitis vinifera) reveals a clear shift in defense mechanisms during berry ripening. Molecular Plant-Microbe Interactions 28: 1167-1180.
Keylor MH, Matsuura BS, Stephenson CRJ. 2015. Chemistry and biology of resveratrol-derived natural products. Chemical Reviews 115: 8976-9027.
Kumar SN, Nambisan B. 2014. Antifungal activity of diketopiperazines and stilbenes against plant pathogenic fungi in vitro. Applied Biochemistry and Biotechnology 172: 741-754.
Langcake P. 1981. Disease resistance of Vitis spp. and the production of the stress metabolites resveratrol, ε-viniferin, α-viniferin and pterostilbene. Physiological Plant Pathology 18: 213-226.
Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
Liang Z, Duan S, Sheng J, Zhu S, Ni X, Shao J, Liu C, Nick P, Du F, Fan P et al. 2019. Whole-genome resequencing of 472 Vitis accessions for grapevine diversity and demographic history analyses. Nature Communications 10: 1-12.
Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408.
Massonnet M, Figueroa-Balderas R, Galarneau ERA, Miki S, Lawrence DP, Sun Q, Wallis CM, Baumgartner K, Cantu D. 2017. Neofusicoccum parvum colonization of the grapevine woody stem triggers asynchronous host responses at the site of infection and in the leaves. Frontiers Plant Science 8. doi: 10.3389/fpls.2017.01117.
Nick P. 2014. Schützen und nützen - von der Erhaltung zur Anwendung. Fallbeispiel Europäische Wildrebe. Hoppea Denkschrift 159-173.
Parage C, Tavares R, Rety S, Baltenweck-Guyot R, Poutaraud A, Renault L, Heintz D, Lugan R, Marais GAB, Aubourg S et al. 2012. Structural, functional, and evolutionary analysis of the unusually large stilbene synthase gene family in grapevine. Plant Physiology 160: 1407-1419.
Paterson AH, Kim C, Guo H, Wang X, Lee T-H. 2014. SNPhylo: a pipeline to construct a phylogenetic tree from huge SNP data. BMC Genomics 15: 162.
Pezet R, Gindro K, Viret O, Spring JL. 2004. Glycosylation and oxidative dimerization of resveratrol are respectively associated to sensitivity and resistance of grapevine cultivars to downy mildew. Physiological and Molecular Plant Pathology 65: 297-303.
Pierron RJG, Pouzoulet J, Couderc C, Judic E, Compant S, Jacques A. 2016. Variations in early response of grapevine wood depending on wound and inoculation combinations with Phaeoacremonium aleophilum and Phaeomoniella chlamydospora. Frontiers in Plant Science 7: 1-14.
Pouzoulet J, Jacques A, Besson X, Dayde J, Mailhac N. 2013. Histopathological study of response of Vitis vinifera cv. Cabernet Sauvignon to bark and wood injury with and without inoculation by Phaeomoniella chlamydospora. Phytopathologia Mediterranea 52: 313-323.
Pouzoulet J, Pivovaroff AL, Santiago LS, Rolshausen PE. 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: 1-11.
Pouzoulet J, Scudiero E, Schiavon M, Rolshausen PE. 2017. Xylem vessel diameter affects the compartmentalization of the vascular pathogen Phaeomoniella chlamydospora in grapevine. Frontiers in Plant Science 8: 1-13.
Romanazzi G, Murolo S, Pizzichini L, Nardi S. 2009. Esca in young and mature vineyards, and molecular diagnosis of the associated fungi. European Journal of Plant Pathology 125: 277-290.
Schellenberger R, Touchard M, Clément C, Baillieul F, Cordelier S, Crouzet J, Dorey S. 2019. Apoplastic invasion patterns triggering plant immunity: plasma membrane sensing at the frontline. Molecular Plant Pathology 20: 1602-1616.
Schröder S, Kortekamp A, Heene E, Daumann J, Valea L, Nick P. 2015. Crop wild relatives as genetic resources - the case of the European wild grape. Canadian Journal of Plant Science 95: 905-912.
Slippers B, Wingfield MJ. 2007. Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biology Reviews 21: 90-106.
Sosnowski MR, Creaser ML, Wicks TJ, Lardner R, Scott ES. 2008. Protection of grapevine pruning wounds from infection by Eutypa lata. Australian Journal of Grape and Wine Research 14: 134-142.
Spagnolo A, Mondello V, Larignon P, Villaume S, Rabenoelina F, Clément C, Fontaine F. 2017. Defense responses in grapevine (Cv. Mourvèdre) after inoculation with the Botryosphaeria dieback pathogens Neofusicoccum parvum and Diplodia seriata and their relationship with flowering. International Journal of Molecular Sciences 18: 1-12.
Stael S, Kmiecik P, Willems P, Van Der Kelen K, Coll NS, Teige M, Van Breusegem F. 2015. Plant innate immunity - sunny side up? Trends in Plant Science 20: 3-11.
Stempien E, Goddard ML, Wilhelm K, Tarnus C, Bertsch C, Chong J. 2017. Grapevine Botryosphaeria dieback fungi have specific aggressiveness factor repertory involved in wood decay and stilbene metabolization. PLoS ONE 12: 1-22.
Svyatyna K, Jikumaru Y, Brendel R, Reichelt M, Mithöfer A, Takano M, Kamiya Y, Nick P, Riemann M. 2014. Light induces jasmonate-isoleucine conjugation via OsJAR1-dependent and -independent pathways in rice. Plant, Cell & Environment 37: 827-839.
Tassoni A, Fornalè S, Franceschetti M, Musiani F, Michael AJ, Perry B, Bagni N. 2005. Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv. Barbera cell cultures. New Phytologist 166: 895-905.
Úrbez-Torres JR. 2011. The status of Botryosphaeriaceae species infecting grapevines José. Phytopathologia Mediterranea 50.
Úrbez-Torres JR, Haag P, Bowen P, O’Gorman DT. 2013. Grapevine trunk diseases in British Columbia: incidence and characterization of the fungal pathogens associated with black foot disease of grapevine. Plant Disease 98: 456-468.
Vannozzi A, Dry IB, Fasoli M, Zenoni S, Lucchin M. 2012. Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses. BMC Plant Biology 12: doi: 10.1186/1471-2229-12-130.
Wagschal I, Abou-Mansour E, Petit A-N, Clement C, Fontaine F. 2008. Wood diseases of grapevine: A review on eutypa dieback and esca. In: Barka EA, Clément C, eds. Plant-microbe interactions. Kerala, India: Research Signpost, 37, 661-686.
Walker SE, Lorsch. 2013. RNA purification - Precipitation methods. In: Lorsch J, ed. Laboratory methods in enzymology: RNA. Methods in enzymology. New York, NY, USA: Academic Press Inc., 530, 337-343.
Wang L, Sadeghnezhad E, Riemann M, Nick P. 2019. Microtubule dynamics modulate sensing during cold acclimation in grapevine suspension cells. Plant Science 280: 18-30.