Grapevine rootstock and soil microbiome interactions: Keys for a resilient viticulture

Romain Darriaut , Vincent Lailheugue , Isabelle Masneuf-Pomarède , Elisa Marguerit , Guilherme Martins , Stéphane Compant , Patricia Ballestra , Steven Upton , Nathalie Ollat , Virginie Lauvergeat

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac019

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Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac019 DOI: 10.1093/hr/uhac019
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Grapevine rootstock and soil microbiome interactions: Keys for a resilient viticulture
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Abstract

Soil microbiota has increasingly been shown to play an integral role in viticulture resilience. The emergence of new metagenomic and culturomic technologies has led to significant advances in the study of microbial biodiversity. In the agricultural sector, soil and plant microbiomes have been found to significantly improve resistance to environmental stressors and diseases, as well as influencing crop yields and fruit quality thus improving sustainability under shifting environments. Grapevines are usually cultivated as a scion grafted on rootstocks, which are selected according to pedoclimatic conditions and cultural practices, known as terroir. The rootstock connects the surrounding soil to the vine’s aerial part and impacts scion growth and berry quality. Understanding rootstock and soil microbiome dynamics is a relevant and important field of study, which may be critical to improve viticulture sustainability and resilience. This review aims to highlight the relationship between grapevine roots and telluric microbiota diversity and activity. In addition, this review explores the concept of core microbiome regarding potential applications of soil microbiome engineering with the goal of enhancing grapevine adaptation to biotic and abiotic stress.

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Romain Darriaut, Vincent Lailheugue, Isabelle Masneuf-Pomarède, Elisa Marguerit, Guilherme Martins, Stéphane Compant, Patricia Ballestra, Steven Upton, Nathalie Ollat, Virginie Lauvergeat. Grapevine rootstock and soil microbiome interactions: Keys for a resilient viticulture. Horticulture Research, 2022, 9 (1) : uhac019 DOI:10.1093/hr/uhac019

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References

[1]

Berg G, Rybakova D, Fischer D et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome. 2020; 8: 103.

[2]

Sarhan MS, Hamza MA, Youssef HH, Patz S . Culturomics of the plant prokaryotic microbiome and the dawn of plant-based culture media - a review. J Adv Res. 2019; 19: 15-27.

[3]

Hardoim PR, van Overbeek LS, Berg G et al. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev. 2015; 79: 293-320.

[4]

White RE . The value of soil knowledge in understanding wine terroir. Front Environ Sci. 2020; 8: 1-6.

[5]

Compant S, Samad A, Faist H, Sessitsch A . A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J Adv Res. 2019; 19: 29-37.

[6]

Fierer N . Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017; 15: 579-90.

[7]

Pascale A, Proietti S, Pantelides IS, Stringlis IA . Modulation of the root microbiome by plant molecules: the basis for targeted disease suppression and plant growth promotion. Front Plant Sci. 2020; 10: 1-23.

[8]

Ghatak A, Schindler F, Bachmann G et al. Root exudation of contrasting drought-stressed pearl millet genotypes conveys varying biological nitrification inhibition (BNI) activity. Biol Fertil Soils. 2021. https://doi.org/10.1007/s00374-021-01578-w.

[9]

Herz K, Dietz S, Gorzolka K et al. Linking root exudates to functional plant traits. PLoS One. 2018; 13: e0204128.

[10]

Williams B, Ahsan MU, Frank MH . Getting to the root of grafting-induced traits. Curr Opin Plant Biol. 2021; 59: 101988.

[11]

Marín D, Armengol J, Carbonell-Bejerano P et al. Challenges of viticulture adaptation to global change: tackling the issue from the roots. Aust J Grape Wine Res. 2021; 27: 8-25.

[12]

Ollat N, Bordenave L, Tandonnet JP et al. Grapevine rootstocks: origins and perspectives. Acta Hortic. 2016; 1136: 11-22.

[13]

Wei Y, Wu Y, Yan Y-Z et al. High-throughput sequencing of microbial community diversity in soil, grapes, leaves, grape juice and wine of grapevine from China. PLoS One. 2018; 13: e0193097.

[14]

Qu Q, Zhang Z, Peijnenburg WJGM et al. Rhizosphere microbiome assembly and its impact on plant growth. J Agric Food Chem. 2020; 68: 5024-38.

[15]

Marasco R, Rolli E, Fusi M et al. Grapevine rootstocks shape underground bacterial microbiome and networking but not potential functionality. Microbiome. 2018; 6: 3.

[16]

Mezzasalma V, Sandionigi A, Guzzetti L et al. Geographical and cultivar features differentiate grape microbiota in northern Italy and Spain vineyards. Front Microbiol. 2018; 9: 1-13.

[17]

Samad A, Trognitz F, Compant S et al. Shared and host-specific microbiome diversity and functioning of grapevine and accompanying weed plants. Environ Microbiol. 2017; 19: 1407-24.

[18]

Zarraonaindia I, Owens SM, Weisenhorn P et al. The soil microbiome influences grapevine-associated microbiota. MBio. 2015; 6: 1-10.

[19]

Nerva L, Moffa L, Giudice G et al. Microscale analysis of soil characteristics and microbiomes reveals potential impacts on plants and fruit: vineyard as a model case study. Plant Soil. 2021; 462: 525-41.

[20]

Liu D, Howell K . Community succession of the grapevine fungal microbiome in the annual growth cycle. Environ Microbiol. 2021; 23: 1842-57.

[21]

Dries L, Bussotti S, Pozzi C et al. Rootstocks shape their microbiome-bacterial communities in the rhizosphere of different grapevine rootstocks. Microorganisms. 2021; 9: 822.

[22]

Aguilar MO, Gobbi A, Browne PD et al. Influence of vintage, geographic location and cultivar on the structure of microbial communities associated with the grapevine rhizosphere in vineyards of San Juan Province, Argentina. PLoS One. 2020; 15: e0243848.

[23]

Deyett E, Rolshausen PE . Endophytic microbial assemblage in grapevine. FEMS Microbiol Ecol. 2020; 96: fiaa053.

[24]

Berlanas C, Berbegal M, Elena G et al. The fungal and bacterial rhizosphere microbiome associated with grapevine rootstock genotypes in mature and young vineyards. Front Microbiol. 2019; 10: 1142.

[25]

Martínez-Diz M d P, Andrés-Sodupe M, Bujanda R et al. Soil-plant compartments affect fungal microbiome diversity and composition in grapevine. Fungal Ecol. 2019; 41: 234-44.

[26]

Novello G, Gamalero E, Bona E et al. The rhizosphere bacterial microbiota of Vitis vinifera cv. Pinot noir in an integrated pest management vineyard. Front Microbiol. 2017; 8.

[27]

Banerjee S, Schlaeppi K, van der Heijden MGA . Keystone taxa as drivers of microbiome structure and functioning. Nat. Rev. Microbiol. 2018; 16: 567-76.

[28]

Musilova L, Ridl J, Polivkova M et al. Effects of secondary plant metabolites on microbial populations: changes in community structure and metabolic activity in contaminated environments. Int J Mol Sci. 2016; 17: 1205.

[29]

Trivedi P, Leach JE, Tringe SG et al. Plant-microbiome interactions: from community assembly to plant health. Nat Rev Microbiol. 2020; 18: 607-21.

[30]

Pacifico D, Squartini A, Crucitti D et al. The role of the endophytic microbiome in the grapevine response to environmental triggers. Front Plant Sci. 2019; 10: 1256.

[31]

Zahid MS, Li D, Javed HU et al. Comparative fungal diversity and dynamics in plant compartments at different developmental stages under root-zone restricted grapevines. BMC Microbiol. 2021; 21: 317.

[32]

Ramírez M, López-Piñeiro A, Velázquez R et al. Analysing the vineyard soil as a natural reservoir for wine yeasts. Food Res Int. 2020; 129: 108845.

[33]

Belda I, Ruiz J, Esteban-Fernández A et al. Microbial contribution to wine aroma and its intended use for wine quality improvement. Molecules. 2017; 22: 189.

[34]

Abdelfattah A, Sanzani SM, Wisniewski M et al. Revealing cues for fungal interplay in the plant-air interface in vineyards. Front Plant Sci. 2019; 10: 1-10.

[35]

Martins G, Lauga B, Miot-Sertier C et al. Characterization of epiphytic bacterial communities from grapes, leaves, bark and soil of grapevine plants grown, and their relations. PLoS One. 2013; 8: e73013.

[36]

Mandl K, Schieck J, Silhavy-Richter K et al. Through the vine to the stem and skins of grapes. Ithaka J. 2015; 349-55.

[37]

Compant S, Mitter B, Colli-Mull JG et al. Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol. 2011; 62: 188-97.

[38]

Griggs RG, Steenwerth KL, Mills DA et al. Sources and assembly of microbial communities in vineyards as a functional component of winegrowing. Front Microbiol. 2021; 12: 673810.

[39]

Jiménez-Gómez A, Celador-Lera L, Fradejas-Bayón M, Rivas R . Plant probiotic bacteria enhance the quality of fruit and horticultural crops. AIMS Microbiol. 2017; 3: 483-501.

[40]

Berger B, Baldermann S, Ruppel S . The plant growth-promoting bacterium Kosakonia radicincitans improves fruit yield and quality of Solanum lycopersicum. J Sci Food Agric. 2017; 97: 4865-71.

[41]

Aoki T, Aoki Y, Ishiai S et al. Impact of Bacillus cereus NRKT on grape ripe rot disease through resveratrol synthesis in berry skin. Pest Manag Sci. 2017; 73: 174-80.

[42]

Otoguro M, Suzuki S . Status and future of disease protection and grape berry quality alteration by micro-organisms in viticulture. Lett Appl Microbiol. 2018; 67: 106-12.

[43]

Verginer M, Leitner E, Berg G . Production of volatile metabolites by grape-associated microorganisms. J Agric Food Chem. 2010; 58: 8344-50.

[44]

Ji W, Han K, Cai Y et al. Characterization of rhizosphere bacterial community and berry quality of Hutai no. 8 (Vitis vinifera L.) with different ages, and their relations. J Sci Food Agric. 2019; 99: 4532-9.

[45]

Torres N, Goicoechea N, Zamarreño AM, Carmen Antolín M . Mycorrhizal symbiosis affects ABA metabolism during berry ripening in Vitis vinifera L. cv. Tempranillo grown under climate change scenarios. Plant Sci. 2018; 274: 383-93.

[46]

Gabriele M, Gerardi C, Longo V, Lucejko JJ . The impact of mycorrhizal fungi on Sangiovese red wine production: phenolic compounds and antioxidant properties. LWT - Food Sci Technol. 2016; 72: 310-6.

[47]

Torres N, Goicoechea N, Morales F, Antolín MC . Berry quality and antioxidant properties in Vitis vinifera cv. Tempranillo as affected by clonal variability, mycorrhizal inoculation and temperature. Crop Pasture Sci. 2016; 67: 961.

[48]

Antolín MC, Izurdiaga D, Urmeneta L et al. Dissimilar responses of ancient grapevines recovered in Navarra (Spain) to arbuscular mycorrhizal symbiosis in terms of berry quality. Agronomy. 2020; 10: 473.

[49]

Vink SN, Dini-Andreote F, Höfle R et al. Interactive effects of scion and rootstock genotypes on the root microbiome of grapevines (Vitis spp. L.). Appl Sci. 2021; 11: 1615.

[50]

Biget M, Mony C, Aubry M et al. The drivers of vine-plant root microbiota endosphere composition include both abiotic and plant-specific factors. OENO One. 2021; 55: 299-315.

[51]

Niem JM, Billones-Baaijens R, Stodart B, Savocchia S . Diversity profiling of grapevine microbial endosphere and antagonistic potential of endophytic pseudomonas against grapevine trunk diseases. Front Microbiol. 2020; 11: 1-19.

[52]

Bona E, Massa N, Novello G et al. Metaproteomic characterization of Vitis vinifera rhizosphere. FEMS Microbiol Ecol. 2018; 95: 1-16.

[53]

D’Amico F, Candela M, Turroni S et al. The rootstock regulates microbiome diversity in root and rhizosphere compartments of Vitis vinifera cultivar Lambrusco. Front Microbiol. 2018; 9: 1-11.

[54]

Trouvelot S, Bonneau L, Redecker D, van Tuinen D . Arbuscular mycorrhiza symbiosis in viticulture: a review. Agron Sustain Dev. 2015; 35: 1449-67.

[55]

Popescu GC . Arbuscular mycorrhizal fungi-an essential tool to sustainable vineyard development : a review. Curr Trends Nat Sci. 2016; 5: 107-16.

[56]

Likar M, Regvar M . Arbuscular mycorrhizal fungi and dark septate endophytes in grapevine: the potential for sustainable viticulture? In: Mycorrhiza - Function, Diversity, State of the Art.Springer International Publishing, 2017, 275-89.

[57]

Lanfranco L, Fiorilli V, Gutjahr C . Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis. New Phytol. 2018; 220: 1031-46.

[58]

Öpik M, Davison J . Uniting species- and community-oriented approaches to understand arbuscular mycorrhizal fungal diversity. Fungal Ecol. 2016; 24: 106-13.

[59]

Van Geel M, ErikVerbruggen MDB, Rennes G, BartLievens OH . High soil phosphorus levels overrule the potential benefits of organic farming on arbuscular mycorrhizal diversity in northern vineyards. Agric Ecosyst Environ. 2017; 248: 144-52.

[60]

Schreiner RP . Depth structures the community of arbuscular mycorrhizal fungi amplified from grapevine (Vitis vinifera L.) roots. Mycorrhiza. 2020; 30: 149-60.

[61]

Drain A, Bonneau L, Recorbet G, van Tuinen D . Characterization of arbuscular mycorrhizal communities in roots of vineyard plants. In: Reinhardt D, Sharma A, eds. Methods in Rhizosphere Biology Research.Springer: Singapore, 2019, 27-34.

[62]

Kryukov AA, Gorbunova AO, Machs EM et al. Perspectives of using Illumina MiSeq for identification of arbuscular mycorrhizal fungi. Vavilov J Genet Breed. 2020; 24: 158-67.

[63]

Radić T, Likar M, Hančević K et al. Occurrence of root endophytic fungi in organic versus conventional vineyards on the Croatian coast. Agric Ecosyst Environ. 2014; 192: 115-21.

[64]

Moukarzel R, Ridgway HJ, Guerin-Laguette A, Jones EE . Grapevine rootstocks drive the community structure of arbuscular mycorrhizal fungi in New Zealand vineyards. J Appl Microbiol. 2021; 131: 2941-56.

[65]

Nerva L, Giudice G, Quiroga G et al. Mycorrhizal symbiosis balances rootstock-mediated growth-defence tradeoffs. Biol Fertil Soils. 2022; 58: 17-34.

[66]

Song F, Pan Z, Bai F et al. The scion/rootstock genotypes and habitats affect arbuscular mycorrhizal fungal community in citrus. Front Microbiol. 2015; 6: 1-11.

[67]

Turnbaugh PJ, Ley RE, Hamady M et al. The human microbiome project. Nature. 2007; 449: 804-10.

[68]

Risely A . Applying the core microbiome to understand host- microbe systems. J Anim Ecol. 2020; 89: 1549-58.

[69]

Thakur MP, Geisen S . Trophic regulations of the soil microbiome. Trends Microbiol. 2019; 27: 771-80.

[70]

Swift JF, Hall ME, Harris ZN et al. Grapevine microbiota reflect diversity among compartments and complex interactions within and among root and shoot systems. Microorganisms. 2021; 9: 92.

[71]

Carbone MJ, Alaniz S, Mondino P et al. Drought influences fungal community dynamics in the grapevine rhizosphere and root microbiome. J Fungi. 2021; 7: 686.

[72]

Van Leeuwen C, Roby J-P, De Rességuier L . Soil-related terroir factors: a review. OENO One. 2018; 52: 173-88.

[73]

Louca S, Polz MF, Mazel F et al. Function and functional redundancy in microbial systems. Nat Ecol Evol. 2018; 2: 936-43.

[74]

Riou C, Agostini D, Aigrain P, Barthe M . Action plan against declining vineyards: an innovative approach. BIO Web Conf. 2016; 7: 01040.

[75]

Liu Q, Wang S, Li K et al. Responses of soil bacterial and fungal communities to the long-term monoculture of grapevine. Appl Microbiol Biotechnol. 2021; 105: 7035-50.

[76]

Westphal A, Browne GT, Schneider S . Evidence for biological nature of the grape replant problem in California. Plant Soil. 2002; 242: 197-203.

[77]

Sanmartin C, Venturi F, Taglieri I, Ferroni G . Restoration of an old vineyard by replanting of missing vines: effects on grape production and wine quality. Agrochimica. 2017; 61: 154-63.

[78]

Rolli E, Marasco R, Saderi S et al. Root-associated bacteria promote grapevine growth: from the laboratory to the field. Plant Soil. 2017; 410: 369-82.

[79]

Hrycan J, Hart M, Bowen P et al. Grapevine trunk disease fungi: their roles as latent pathogens and stress factors that favour disease development and symptom expression. Phytopathol Mediterr. 2020; 59: 395-424.

[80]

Orozco-Mosqueda M d C, Rocha-Granados MDC, Glick BR, Santoyo G . Microbiome engineering to improve biocontrol and plant growth-promoting mechanisms. Microbiol Res. 2018; 208: 25-31.

[81]

Berg G, Köberl M, Rybakova D et al. Plant microbial diversity is suggested as the key to future biocontrol and health trends. FEMS Microbiol Ecol. 2017; 93: 1-9.

[82]

Vega-Avila AD, Gumiere T, Andrade PAM et al. Bacterial communities in the rhizosphere of Vitis vinifera L. cultivated under distinct agricultural practices in Argentina. Antonie Van Leeuwenhoek. 2015; 107: 575-88.

[83]

Ostandie N, Giffard B, Bonnard O et al. Multi-community effects of organic and conventional farming practices in vineyards. Sci Rep. 2021; 11: 11979.

[84]

Karimi B, Cahurel J-Y, Gontier L et al. A meta-analysis of the ecotoxicological impact of viticultural practices on soil biodiversity. Environ Chem Lett. 2020; 18: 1947-66.

[85]

Pertot I, Giovannini O, Benanchi M, Caffi T . Combining biocontrol agents with different mechanisms of action in a strategy to control Botrytis cinerea on grapevine. Crop Prot. 2017; 97: 85-93.

[86]

Dagostin S, Schärer H-J, Pertot I, Tamm L . Are there alternatives to copper for controlling grapevine downy mildew in organic viticulture? Crop Prot. 2011; 30: 776-88.

[87]

Angeli D, Pellegrini E, Pertot I . Occurrence of Erysiphe necator Chasmothecia and their natural parasitism by Ampelomyces quisqualis. Phytopathology. 2009; 99: 704-10.

[88]

Andreazza R, Pieniz S, Okeke B, Camargo FA . Evaluation of copper resistant bacteria from vineyard soils and mining waste for copper biosorption. Brazilian J Microbiol. 2011; 42: 66-74.

[89]

Nally MC, Pesce VM, Maturano YP et al. Biocontrol of Botrytis cinerea in table grapes by non-pathogenic indigenous Saccharomyces cerevisiae yeasts isolated from viticultural environments in Argentina. Postharvest Biol Technol. 2012; 64: 40-8.

[90]

Salunkhe VP, Sawant IS, Banerjee K et al. Biodegradation of profenofos by Bacillus subtilis isolated from grapevines (Vitis vinifera). J Agric Food Chem. 2013; 61: 7195-202.

[91]

Thomidis T, Pantazis S, Konstantinoudis K . Evaluation of serenade max to control fruit rot of grapes. J Agric Sci. 2016; 8: 212.

[92]

Serrano L, Manker D, Brandi F, Cali T . The use of Bacillus subtilis QST 713 and Bacillus pumilus QST 2808 as protectant fungicides in conventional application programs for black leaf streak control. Acta Hortic. 2013; 986: 149-55.

[93]

Lahdenperä M-L, Simon E, Uoti J . Mycostop-a novel biofungicide based on Streptomyces bacteria. In: Developments in agricultural and managed forest ecology.Vol. 23. 1991, 258-63.

[94]

Hofstein R, Daoust RA, Aeschlimann JP . Constraints to the development of biofungicides: the example of “AQ10”, a new product for controlling powdery mildews. Entomophaga. 1996; 41: 455-60.

[95]

O’neill TM, Elad Y, Shtuenberg D, Cohen A . Control of grapevine Grey Mould with Trichoderma harzianum T39. Biocontrol Sci Tech. 1996; 6: 139-46.

[96]

Pertot I, Prodorutti D, Colombini A, Pasini L . Trichoderma atroviride SC1 prevents Phaeomoniella chlamydospora and Phaeoacremonium aleophilum infection of grapevine plants during the grafting process in nurseries. BioControl. 2016; 61: 257-67.

[97]

São-José C, Santos MA, Schmitt MJ . Viruses of wine-associated yeasts and bacteria. In: König H, Unden G, Fröhlich J, eds. Biology of Microorganisms on Grapes, in Must and in Wine.Springer International Publishing, 2017, 133-54.

[98]

Sipiczki M . Metschnikowia strains isolated from botrytized grapes antagonize fungal and bacterial growth by iron depletion. Appl Environ Microbiol. 2006; 72: 6716-24.

[99]

Calvo-Garrido C, Roudet J, Aveline N et al. Microbial antagonism toward botrytis bunch rot of grapes in multiple field tests using one bacillus ginsengihumi strain and formulated biological control products. Front Plant Sci. 2019; 10: 105.

[100]

Héloir M-C, Adrian M, Brulé D et al. Recognition of elicitors in grapevine: from MAMP and DAMP perception to induced resistance. Front Plant Sci. 2019; 10: 1-17.

[101]

Jeandet P, Hébrard C, Deville M-A et al. Deciphering the role of phytoalexins in plant-microorganism interactions and human health. Molecules. 2014; 19: 18033-56.

[102]

Yacoub A, Magnin N, Gerbore J et al. The biocontrol root oomycete, Pythium oligandrum, triggers grapevine resistance and shifts in the transcriptome of the trunk pathogenic fungus, Phaeomoniella chlamydospora. Int J Mol Sci. 2020; 21: 6876.

[103]

Gramaje D, Armengol J . Fungal trunk pathogens in the grapevine propagation process: potential inoculum sources, detection, identification, and management strategies. Plant Dis. 2011; 95: 1040-55.

[104]

del Pilar Martínez-Diz M, Díaz-Losada E, Andrés-Sodupe M et al. Field evaluation of biocontrol agents against black-foot and petri diseases of grapevine. Pest Manag Sci. 2021; 77: 697-708.

[105]

Stempien E, Jean R, Pierron G, Jaarsveld WJVAN . Host defence activation and root colonization of grapevine rootstocks by the biological control fungus Trichoderma atroviride. Phytopathol Mediterr. 2020; 59: 615-26.

[106]

Jaarsveld WJ, Halleen F, Bester MC et al. Investigation of Trichoderma species colonization of nursery grapevines for improved management of black foot disease. Pest Manag Sci. 2021; 77: 397-405.

[107]

Aziz A, Verhagen B, Magnin-Robert M et al. Effectiveness of beneficial bacteria to promote systemic resistance of grapevine to gray mold as related to phytoalexin production in vineyards. Plant Soil. 2016; 405: 141-53.

[108]

Verhagen B, Trotel-Aziz P, Jeandet P et al. Improved resistance against Botrytis cinerea by grapevine-associated bacteria that induce a prime oxidative burst and phytoalexin production. Phytopathology. 2011; 101: 768-77.

[109]

Magnin-Robert M, Trotel-Aziz P, Quantinet D et al. Biological control of Botrytis cinerea by selected grapevine-associated bacteria and stimulation of chitinase and β-1,3 glucanase activities under field conditions. Eur J Plant Pathol. 2007; 118: 43-57.

[110]

Esmaeel Q, Jacquard C, Sanchez L et al. The mode of action of plant associated Burkholderia against grey mould disease in grapevine revealed through traits and genomic analyses. Sci Rep. 2020; 10: 19393.

[111]

Miotto-Vilanova L, Jacquard C, Courteaux B et al. Burkholderia phytofirmans PsJN confers grapevine resistance against Botrytis cinerea via a direct antimicrobial effect combined with a better resource mobilization. Front Plant Sci. 2016; 7: 1-15.

[112]

Lakkis S, Trotel-Aziz P, Rabenoelina F et al. Strengthening grapevine resistance by Pseudomonas fluorescens PTA-CT2 relies on distinct defense pathways in susceptible and partially resistant genotypes to downy mildew and gray mold diseases. Front Plant Sci. 2019; 10: 1-18.

[113]

Sawant IS, Wadkar PN, Ghule SB et al. Induction of systemic resistance in grapevines against powdery mildew by Trichoderma asperelloides strains. Australas Plant Pathol. 2020; 49: 107-17.

[114]

Yacoub A, Gerbore J, Magnin N et al. Ability of Pythium oligandrum strains to protect Vitis vinifera L., by inducing plant resistance against Phaeomoniella chlamydospora, a pathogen involved in esca, a grapevine trunk disease. Biol Control. 2016; 92: 7-16.

[115]

Leal C, Richet N, Guise J-F et al. Cultivar contributes to the beneficial effects of Bacillus subtilis PTA-271 and Trichoderma atroviride SC1 to protect grapevine against Neofusicoccum parvum. Front Microbiol. 2021; 12: 1-17.

[116]

Asghari S, Harighi B, Ashengroph M et al. Induction of systemic resistance to agrobacterium tumefaciens by endophytic bacteria in grapevine. Plant Pathol. 2020; 69: 827-37.

[117]

de la Fuente Cantó C, Simonin M, King E et al. An extended root phenotype: the rhizosphere, its formation and impacts on plant fitness. Plant J. 2020; 103: 951-64.

[118]

Caddell DF, Deng S, Coleman-Derr D . Role of the plant root microbiome in abiotic stress tolerance. In: Seed Endophytes.Springer International Publishing, 2019, 273-311.

[119]

Hawkes CV, Keitt TH . Resilience vs. historical contingency in microbial responses to environmental change. Ecol Lett. 2015; 18: 612-25.

[120]

Zolla G, Badri DV, Bakker MG et al. Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. Appl Soil Ecol. 2013; 68: 1-9.

[121]

Funes Pinter I, VictoriaSalomon M, Berli F et al. Plant growth promoting rhizobacteria alleviate stress by AsIII in grapevine. Agric Ecosyst Environ. 2018; 267: 100-8.

[122]

Rolli E, Marasco R, Vigani G et al. Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol. 2015; 17: 316-31.

[123]

Nikolaou N, Angelopoulos K, Karagiannidis N . Effects of drought stress on mycorrhizal and non-mycorrhizal cabernet sauvignon grapevine, grafted onto various rootstocks. Exp Agric. 2003; 39: 241-52.

[124]

Salomon MV, Purpora R, Bottini R, Piccoli P . Rhizosphere associated bacteria trigger accumulation of terpenes in leaves of Vitis vinifera L. cv. Malbec that protect cells against reactive oxygen species. Plant Physiol Biochem. 2016; 106: 295-304.

[125]

Cohen AC, Dichiara E, Jofré V et al. Carotenoid profile produced by bacillus licheniformis Rt4M10 isolated from grapevines grown in high altitude and their antioxidant activity. Int J Food Sci Technol. 2018; 53: 2697-705.

[126]

Jiao J, Ma Y, Chen S et al. Melatonin-producing endophytic bacteria from grapevine roots promote the abiotic stress-induced production of endogenous melatonin in their hosts. Front Plant Sci. 2016; 7: 1-13.

[127]

Ma Y, Jiao J, Fan X et al. Endophytic bacterium Pseudomonas fluorescens RG11 may transform tryptophan to melatonin and promote endogenous melatonin levels in the roots of four grape cultivars. Front Plant Sci. 2017; 07: 1-15.

[128]

Aragüés R, Medina ET, Zribi W et al. Soil salinization as a threat to the sustainability of deficit irrigation under present and expected climate change scenarios. Irrig Sci. 2015; 33: 67-79.

[129]

Khalil HA . Influence of vesicular-arbuscula mycorrhizal fungi (glomus spp.) on the response of grapevines rootstocks to salt stress. Asian J Crop Sci. 2013; 5: 393-404.

[130]

Rodriguez RJ, Henson J, Van Volkenburgh E et al. Stress tolerance in plants via habitat-adapted symbiosis. ISME J. 2008; 2: 404-16.

[131]

Gómez-Bellot MJ, Ortuño MF, Nortes PA et al. Protective effects of Glomus iranicum var. tenuihypharum on soil and Viburnum tinus plants irrigated with treated wastewater under field conditions. Mycorrhiza. 2015; 25: 399-409.

[132]

Bettenfeld P, Fontaine F, Trouvelot S et al. Woody plant declines. What’s wrong with the microbiome? Trends Plant Sci. 2020; 25: 381-94.

[133]

Verbruggen E, Heijden MGA, Rillig MC, Kiers ET . Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol. 2013; 197: 1104-9.

[134]

Chibeba AM, Kyei-Boahen S, Guimarães MF et al. Feasibility of transference of inoculation-related technologies: a case study of evaluation of soybean rhizobial strains under the agro-climatic conditions of Brazil and Mozambique. Agric Ecosyst Environ. 2018; 261: 230-40.

[135]

Velivelli SLS, De Vos P, Kromann P et al. Biological control agents: from field to market, problems, and challenges. Trends Biotechnol. 2014; 32: 493-6.

[136]

Keswani C, Prakash O, Bharti N et al. Re-addressing the biosafety issues of plant growth promoting rhizobacteria. Sci Total Environ. 2019; 690: 841-52.

[137]

Haidar R, Yacoub A, Vallance J et al. Bacteria associated with wood tissues of esca-diseased grapevines: functional diversity and synergy with Fomitiporia mediterranea to degrade wood components. Environ Microbiol. 2021; 23: 6104-21.

[138]

Compant S, Reiter B, Sessitsch A et al. Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol. 2005; 71: 1685-93.

[139]

Lòpez-Fernàndez S, Compant S, Vrhovsek U et al. Grapevine colonization by endophytic bacteria shifts secondary metabolism and suggests activation of defense pathways. Plant Soil. 2016; 405: 155-75.

[140]

Cook RJ. Plant health management: pathogen suppressive soils. In: Encyclopedia of Agriculture and Food Systems.Vol. 4. 2014, 441-55.

[141]

Richards A, Estaki M, Úrbez-Torres JR et al. Cover crop diversity as a tool to mitigate vine decline and reduce pathogens in vineyard soils. Diversity. 2020; 12: 128.

[142]

Nerva L, Zanzotto A, Gardiman M et al. Soil microbiome analysis in an ESCA diseased vineyard. Soil Biol Biochem. 2019; 135: 60-70.

[143]

Smits LP, Bouter KEC, de Vos WM et al. Therapeutic potential of fecal microbiota transplantation. Gastroenterology. 2013; 145: 946-53.

[144]

Siegel-Hertz K, Edel-Hermann V, Chapelle E et al. Comparative microbiome analysis of a fusarium wilt suppressive soil and a fusarium wilt conducive soil from the Châteaurenard region. Front Microbiol. 2018; 9: 1-16.

[145]

Bertini E, Tornielli GB, Pezzotti M, Zenoni S . Regeneration of plants from embryogenic callus-derived protoplasts of Garganega and Sangiovese grapevine (Vitis vinifera L.) cultivars. Plant Cell Tissue Organ Cult. 2019; 138: 239-46.

[146]

Gaziea SM, Shereen MAH, Laila HF, Eman EHS . Efficiency of biological control of root-knot nematodes in infected grapevines seedling by genetic improved bacteria. Plant Arch. 2020; 20: 951-61.

[147]

Abdel-Salam MS, Ameen HH, Soliman GM et al. Improving the nematicidal potential of bacillus amyloliquefaciens and Lysinibacillus sphaericus against the root-knot nematode Meloidogyne incognita using protoplast fusion technique. Egypt J Biol Pest Control. 2018; 28: 31.

[148]

Lakhani HN, Vakharia DN . Influence of protoplast fusion in Trichoderma Spp. on controlling some soil borne diseases. J Plant Pathol Microbiol. 2016; 7.

[149]

Zhang Y-X, Perry K, Vinci VA et al. Genome shuffling leads to rapid phenotypic improvement in bacteria. Nature. 2002; 415: 644-6.

[150]

Pollock J, Glendinning L, Wisedchanwet T, Watson M . The madness of microbiome: attempting to find consensus “best practice” for 16S microbiome studies. Appl Environ Microbiol. 2018; 84: e02627-17.

[151]

Dawkins R, Barnett SA . The Extended Phenotype . Vol. 18. Oxford Univ Press; 1982: 253-9.

[152]

Pratama AA, van Elsas JD . The ‘neglected’ soil virome - potential role and impact. Trends Microbiol. 2018; 26: 649-62.

[153]

Martelli GP . An overview on grapevine viruses, viroids, and the diseases they cause. In: Grapevine Viruses: Molecular Biology, Diagnostics and Management . Springer International Publishing, 2017, 31-46.

[154]

Vitulo N, Lemos WJF Jr, Calgaro M et al. Bark and grape microbiome of Vitis vinifera: influence of geographic patterns and agronomic management on bacterial diversity. Front Microbiol. 2019; 9.

[155]

Faist H, Keller A, Hentschel U, Deeken R . Grapevine (Vitis vinifera) crown galls host distinct microbiota. Appl Environ Microbiol. 2016; 82: 5542-52.

[156]

Portillo M d C, Franquès J, Araque I et al. Bacterial diversity of Grenache and Carignan grape surface from different vineyards at Priorat wine region (Catalonia, Spain). Int J Food Microbiol. 2016; 219: 56-63.

[157]

Bokulich NA, Thorngate JH, Richardson PM, Mills DA . Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc Natl Acad Sci. 2014; 111: 139-48.

[158]

Perazzolli M, Antonielli L, Storari M et al. Resilience of the natural phyllosphere microbiota of the grapevine to chemical and biological pesticides. Appl Environ Microbiol. 2014; 80: 3585-96.

[159]

Pinto C, Pinho D, Sousa S et al. Unravelling the diversity of grapevine microbiome. PLoS One. 2014; 9: e85622.

[160]

Gramaje D, Eichmeier A, Spetik M et al. Exploring the temporal dynamics of the fungal microbiome in rootstocks, the lesser-known half of the grapevine crop. Res Sq. 2021.

[161]

Kraus C, Voegele RT, Fischer M . Temporal development of the culturable, endophytic fungal community in healthy grapevine branches and occurrence of GTD-associated fungi. Microb Ecol. 2019; 77: 866-76.

[162]

Carmichael PC, Siyoum N, Chidamba L, Korsten L . Exploring the microbial communities associated with Botrytis cinerea during berry development in table grape with emphasis on potential biocontrol yeasts. Eur J Plant Pathol. 2019; 154: 919-30.

[163]

Dissanayake AJ, Purahong W, Wubet T et al. Direct comparison of culture-dependent and culture-independent molecular approaches reveal the diversity of fungal endophytic communities in stems of grapevine (Vitis vinifera). Fungal Divers. 2018; 90: 85-107.

[164]

Eichmeier A, Pečenka J, Peňázová E et al. High-throughput amplicon sequencing-based analysis of active fungal communities inhabiting grapevine after hot-water treatments reveals unexpectedly high fungal diversity. Fungal Ecol. 2018; 36: 26-38.

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