Metabolic and transcriptional changes associated with the use of Ascophyllum nodosum extracts as tools to improve the quality of wine grapes (Vitis vinifera cv. Sangiovese) and their tolerance to biotic stress.


Journal

Journal of the science of food and agriculture
ISSN: 1097-0010
Titre abrégé: J Sci Food Agric
Pays: England
ID NLM: 0376334

Informations de publication

Date de publication:
Nov 2019
Historique:
received: 29 11 2018
revised: 05 06 2019
accepted: 03 07 2019
pubmed: 6 7 2019
medline: 2 11 2019
entrez: 6 7 2019
Statut: ppublish

Résumé

Recent studies report that Ascophyllum nodosum extracts, once applied on the canopy of different crops, deliver positive effects, increasing yield, inducing tolerance to biotic stress, and improving the quality of products. However, the mechanisms of action are still unclear. In this research, vines subjected to multiple foliar applications of an A. nodosum extract (ANE) at label doses were compared with untreated vines (NTV) in accordance with a comparative approach. The investigation coupled a field experiment with a second trial conducted under semi-controlled conditions, to clarify the mechanisms of action involved. The biostimulant did not affect soluble solids or the acidity of grapes; instead, it improved their anthocyanin and phenolic concentrations and the respective profiles. At the time of harvest, anthocyanin, and phenolic concentration were increased by 10.4% and 14.5%, respectively, when compared to the NTV. These effects correlated with a specific modulation of genes involved in the flavonoid metabolic pathways. Moreover, grapes from ANE vines witnessed a significant reduction in the spreading of gray mold when they were either assessed in field conditions or in vitro, compared to the grapes of NTV vines. This was related to a significant upregulation of the defense-related genes of the plant. Overall, the results showed that A. nodosum extracts can be valuable tools in viticulture considering the emergence of challenging environmental conditions; hence, the regulation of specific metabolic pathways is the mechanism of action that leads to an increased tolerance of biotic stress and of changes in the content of grape metabolites. © 2019 Society of Chemical Industry.

Sections du résumé

BACKGROUND BACKGROUND
Recent studies report that Ascophyllum nodosum extracts, once applied on the canopy of different crops, deliver positive effects, increasing yield, inducing tolerance to biotic stress, and improving the quality of products. However, the mechanisms of action are still unclear. In this research, vines subjected to multiple foliar applications of an A. nodosum extract (ANE) at label doses were compared with untreated vines (NTV) in accordance with a comparative approach. The investigation coupled a field experiment with a second trial conducted under semi-controlled conditions, to clarify the mechanisms of action involved.
RESULTS RESULTS
The biostimulant did not affect soluble solids or the acidity of grapes; instead, it improved their anthocyanin and phenolic concentrations and the respective profiles. At the time of harvest, anthocyanin, and phenolic concentration were increased by 10.4% and 14.5%, respectively, when compared to the NTV. These effects correlated with a specific modulation of genes involved in the flavonoid metabolic pathways. Moreover, grapes from ANE vines witnessed a significant reduction in the spreading of gray mold when they were either assessed in field conditions or in vitro, compared to the grapes of NTV vines. This was related to a significant upregulation of the defense-related genes of the plant.
CONCLUSIONS CONCLUSIONS
Overall, the results showed that A. nodosum extracts can be valuable tools in viticulture considering the emergence of challenging environmental conditions; hence, the regulation of specific metabolic pathways is the mechanism of action that leads to an increased tolerance of biotic stress and of changes in the content of grape metabolites. © 2019 Society of Chemical Industry.

Identifiants

pubmed: 31273796
doi: 10.1002/jsfa.9913
doi:

Substances chimiques

Anthocyanins 0
Flavonoids 0
Phenols 0
Plant Extracts 0
Plant Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

6350-6363

Subventions

Organisme : Acadian Seaplants Limited
Organisme : CBC Europe - Biogard Division

Informations de copyright

© 2019 Society of Chemical Industry.

Références

Jones GV, White MA, Cooper OR and Storchmann K, Climate change and global wine quality. Clim Change 73:319-343 (2005).
Palliotti A, Tombesi S, Silvestroni O, Lanari V, Gatti M and Poni S, Changes in vineyard establishment and canopy management urged by earlier climate-related grape ripening: a review. Sci Hortic 178:43-54 (2014).
Poni S, Gatti M, Palliotti A, Dai Z, Duchêne E, Truong TT et al., Grapevine quality: a multiple choice issue. Sci Hortic 234:445-462 (2018).
Calvo-Garrido C, Elmer PAG, Vinas I, Usall J, Bartra E and Teixidó N, Biological control of botrytis bunch rot in organic wine grapes with the yeast antagonist Candida sake CPA-1. Plant Pathol 62:510-519 (2013).
Du Jardin P, Plant biostimulants: definition, concept, main categories and regulation. Sci Hortic 196:3-14 (2015).
Colla G and Rouphael Y, Biostimulants in horticulture. Sci Hortic 196:1-2 (2015).
Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM et al., Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 28:386-399 (2009).
Povero G, Mejia JF, Di Tommaso D, Piaggesi A and Warrior P, A systematic approach to discover and characterize natural plant biostimulants. Front Plant Sci 7:435 (2016).
Battacharyya D, Babgohari MZ, Rathor P and Prithiviraj B, Seaweed extracts as biostimulants in horticulture. Sci Hortic 196:39-48 (2015).
Jayaraj J, Wan A, Rahman M and Punja ZK, Seaweed extract reduces foliar fungal diseases on carrot. Crop Prot 27:1360-1366 (2008).
Wally OS, Critchley AT, Hiltz D, Craigie JS, Han X, Zaharia LI et al., Regulation of phytohormone biosynthesis and accumulation in Arabidopsis following treatment with commercial extract from the marine macroalga Ascophyllum nodosum. J. Plant Growth Regul. 32:324-339 (2013).
Goñi O, Fort A, Quille P, McKeown PC, Spillane C and O'Connell S, Comparative transcriptome analysis of two Ascophyllum nodosum extract biostimulants: same seaweed but different. J Agr Food Chem 64:2980-2989 (2016).
Abkhoo J and Sabbagh SK, Control of Phytophthora melonis damping-off, induction of defense responses, and gene expression of cucumber treated with commercial extract from Ascophyllum nodosum. J. Appl. Phycol. 28:1333-1342 (2016).
Jayaraman J, Norrie J and Punja ZK, Commercial extract from the brown seaweed Ascophyllum nodosum reduces fungal diseases in greenhouse cucumber. J Appl Phycol 23:353-361 (2011).
Norrie J and Keathley JP, Benefits of Ascophyllum nodosum marine-plant extract applications to 'Thompson seedless' grape production. Acta Hortic 727:243-247 (2006).
Norrie J, Branson T and Keathley PE, Marine plant extracts impact on grape yield and quality. Acta Hortic. 594:315-319 (2002).
Fan D, Hodges DM, Critchley AT and Prithiviraj B, A commercial extract of brown macroalga (Ascophyllum nodosum) affects yield and the nutritional quality of spinach in vitro. Commun Soil Sci Plant Anal 44:1873-1884 (2013).
Fan D, Hodges DM, Zhang J, Kirby CW, Ji X, Locke SJ et al., Commercial extract of the brown seaweed Ascophyllum nodosum enhances phenolic antioxidant content of spinach (Spinacia oleracea L.) which protects Caenorhabditis elegans against oxidative and thermal stress. Food Chem 124:195-202 (2011).
Kocira A, Świeca M, Kocira S, Złotek U and Jakubczyk A, Enhancement of yield, nutritional and nutraceutical properties of two common bean cultivars following the application of seaweed extract (Ecklonia maxima). Saudi J Biol Sci 25:563-571 (2018).
Salvi L, Cataldo E, Secco S and Mattii GB, Use of natural biostimulants to improve the quality of grapevine production: first results. Acta Hortic. 1148:77-84 (2016).
Frioni T, Sabbatini P, Tombesi S, Norrie J, Poni S, Gatti M et al., Effects of a biostimulant derived from the brown seaweed Ascophyllum nodosum on ripening dynamics and fruit quality of grapevines. Sci Hortic 232:97-106 (2018).
Salvi L, Brunetti C, Cataldo E, Niccolai A, Centritto M, Ferrini F et al., Effects of Ascophyllum nodosum extract on Vitis vinifera: consequences on plant physiology, grape quality and secondary metabolism. Plant Physiol Biochem 139:21-32 (2019).
Coombe BG, Growth stages of the grapevine: adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res 1:104-110 (1995).
Hurtado AQ, Yunque DA, Tibubos K and Critchley AT, Use of Acadian marine plant extract powder from Ascophyllum nodosum in tissue culture of Kappaphycus varieties. J Appl Phycol 21:633-639 (2009).
Faurie B, Cluzet S, Corio-Costet MF and Mérillon JM, Methyl jasmonate/ethephon cotreatment synergistically induces stilbene production in "Vitis vinifera" cell suspensions but fails to trigger resistance to "Erysiphe necator". OENO One 43:99-110 (2009).
Iland P, Bruer N, Edwards G, Weeks S and Wilkes E, Chemical Analysis of Grapes and Wine: Techniques and Concepts. Patrick Iland Wine Promotions Pty. Ltd, Campbelltown (2004).
Livak KJ and Schmittgen TD, Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402-408 (2001).
Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E and Di Gaspero G, Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ 30:1381-1399 (2007).
Downey MO and Rochfort S, Simultaneous separation by reversed-phase high-performance liquid chromatography and mass spectral identification of anthocyanins and flavonols in shiraz grape skin. J Chrom A 1201:43-47 (2008).
Nicoletti I, Bello C, De Rossi A and Corradini D, Identification and quantification of phenolic compounds in grapes by HPLC-PDA-ESI-MS on a semimicro separation scale. J Agric Food Chem 56:8801-8808 (2008).
Santi S, De Marco F, Polizzotto R, Grisan S and Musetti R, Recovery from stolbur disease in grapevine involves changes in sugar transport and metabolism. Front Plant Sci 4:171 (2013).
Le Henanff G, Heitz T, Mestre P, Mutterer J, Walter B and Chong J, Characterization of Vitis vinifera NPR1 homologs involved in the regulation of pathogenesis-related gene expression. BMC Plant Biol 9:54 (2009).
Ramírez-Suero M, Bénard-Gellon M, Chong J, Laloue H, Stempien E, Abou-Mansour E et al., Extracellular compounds produced by fungi asscoiated with Botryosphaeria dieback induce differential defence gene expression patterns and necrosis in Vitis vinifera cv. Chardonnay cells. Protoplasma 251:1417-1426 (2014).
Mundy D and Beresford R, Susceptibility of grapes to Botrytis cinerea in relation to berry nitrogen and sugar concentration. N Z Plant Protect-SE 60:123-127 (2007).
Martínez-Romero D, Guillén F, Valverde JM, Bailén G, Zapata P, Serrano M et al., Influence of carvacrol on survival of Botrytis cinerea inoculated in table grapes. Int J Food Microbiol 115:144-148 (2007).
Moretti C, Quaglia M, Cerri M, Nicosia DE and Buonaurio R, A real-time PCR assay for detection and quantification of Botrytis cinerea in Pelargonium x hortorum plants and its use for evaluation of plant resistance. Eur J Plant Pathol 143:159-171 (2015).
Marois JJ, Bledsoe AM, Gubler WD and Luvisi DA, Control of Botrytis cinerea on grape berries during postharvest storage with reduced levels of Sulphur dioxide. Plant Dis 70:1050-1052 (1986).
McKinney HH, A new system of grading plant diseases. J Agric Res 26:195-218 (1923).
Winkler AJ, Cook JA, Kliewer WM and Lider LA, General viticulture. University of California Press, Berkeley, CA (1974).
Castellarin SD, Matthews MA, Di Gaspero G and Gambetta GA, Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 227:101-112 (2007).
Lola-Luz T, Hennequart F and Gaffney M, Effect on health promoting phytochemicals following seaweed application, in potato and onion crops grown under a low input agricultural system. Sci Hortic 170:224-227 (2014).
Lola-Luz T, Hennequart F and Gaffney M, Effect on yield total phenolic, total flavonoid and total isothiocyanate content of two broccoli cultivars (Brassica oleraceae var italica) following the application of a commercial brown seaweed (Ascophyllum nodosum). Agric Food Sci 23:28-37 (2014).
Lola-Luz T, Hennequart F and Gaffney M, Enhancement of phenolic and flavonoid compounds in cabbage (Brassica oleraceae) following application of commercial seaweed extracts of the brown seaweed (Ascophyllum nodosum). Agric Food Sci 22:288-295 (2013).
Winkel-Shirley B, Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485-493 (2001).
Falginella L, Castellarin SD, Testolin R, Gambetta GA, Morgante M and Di Gaspero G, Expansion and subfunctionalisation of flavonoid 3′,5′-hydroxylases in the grapevine lineage. BMC Genomics 11:562 (2010).
Fischer U and Noble AC, The effect of ethanol, catechin concentration, and pH on sourness and bitterness of wine. Am J Enol Viticult 45:6-10 (1994).
Boulton R, The copigmentation of anthocyanins and its role in the color of red wine: a critical review. Am. J. Enol. Viticult. 52:67-87 (2001).
Pérez MJ, Falqué E and Domínguez H, Antimicrobial action of compounds from marine seaweed. Mar Drugs 14:52 (2016).

Auteurs

Tommaso Frioni (T)

Department of Sustainable Crop Production (DI.PRO.VE.S.), Università Cattolica del Sacro Cuore, Piacenza, Italy.
Department of Agricultural, Food and Environmental Sciences (DSA3), Università degli Studi di Perugia, Perugia, Italy.

Sergio Tombesi (S)

Department of Sustainable Crop Production (DI.PRO.VE.S.), Università Cattolica del Sacro Cuore, Piacenza, Italy.

Mara Quaglia (M)

Department of Agricultural, Food and Environmental Sciences (DSA3), Università degli Studi di Perugia, Perugia, Italy.

Ornella Calderini (O)

Institute of Biosciences and Bioresources (IBBR), National Research Council of Italy (CNR), Perugia, Italy.

Chiaraluce Moretti (C)

Department of Agricultural, Food and Environmental Sciences (DSA3), Università degli Studi di Perugia, Perugia, Italy.

Stefano Poni (S)

Department of Sustainable Crop Production (DI.PRO.VE.S.), Università Cattolica del Sacro Cuore, Piacenza, Italy.

Matteo Gatti (M)

Department of Sustainable Crop Production (DI.PRO.VE.S.), Università Cattolica del Sacro Cuore, Piacenza, Italy.

Alessandro Moncalvo (A)

Department of Sustainable Crop Production (DI.PRO.VE.S.), Università Cattolica del Sacro Cuore, Piacenza, Italy.

Paolo Sabbatini (P)

Department of Horticulture, Michigan State University, East Lansing, MI, USA.

Julian Garcìa Berrìos (JG)

Departamento de Produccion Vexetal, Universidad de Santiago de Compostela, Escola Politecnica Superior, Lugo, Spain.

Alberto Palliotti (A)

Department of Agricultural, Food and Environmental Sciences (DSA3), Università degli Studi di Perugia, Perugia, Italy.

Articles similaires

Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family

Perceptions of the neighbourhood food environment and food insecurity of families with children during the Covid-19 pandemic.

Irene Carolina Sousa Justiniano, Matheus Santos Cordeiro, Hillary Nascimento Coletro et al.
1.00
Humans COVID-19 Food Insecurity Cross-Sectional Studies Female
Fragaria Light Plant Leaves Osmosis Stress, Physiological

Classifications MeSH