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BioControl

, Volume 61, Issue 3, pp 243–256 | Cite as

Vitis vinifera microbiome: from basic research to technological development

  • Cátia Pinto
  • Ana Catarina GomesEmail author
Article

Abstract

Plants naturally harbours a complex microbial ecosystem or plant microbiome, as neutral, beneficial or pathogens microorganisms, that are in a close interaction with the plant. The balance of these interactions is a key element for plant health, plant growth and productivity although several factors as ecological and environmental factors represents important drivers of the microorganism’s community. Herein, a review on plant microbiome is presented, and the case study of Vitis vinifera (grapevine) is presented as an example of the application of the study of a woody plant microbiome. Overall, new ecologically and sustainable strategies for agriculture are needed. The exploitation of the natural microbiome associated with plants and the identification of novel potential strains with plant benefits and biocontrol potential represent a challenge and a technological development for crops protection.

Keywords

Biological control agents Plant microbiome Grapevine microbiome 

Notes

Acknowledgments

This work has been funded by FCT – “Fundação para a Ciência e Tecnologia” under the HoliWine project (Ref FCOMP-01-0124-FEDER-02741). Cátia Pinto is supported by a PhD grant from FCT with the reference FRH/BD/84197/2012.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest for this publication.

Supplementary material

10526_2016_9725_MOESM1_ESM.xlsx (13 kb)
Supplementary table 1: General list of the bacterial communities associated with grapevine. General overview of the bacterial communities’ structure associated with grapevine and assessed using either independent or dependent- approach. The “X” at the independent or dependent-approach column indicates the methodology applied for the microbial community analysis, according to the mentioned study and “--“ indicates the lack of information available. *FD – Flavescence dorée. Supplementary material 1 (XLSX 12 kb)
10526_2016_9725_MOESM2_ESM.xlsx (12 kb)
Supplementary table 2: General list of the fungal communities associated with grapevine. General overview of the fungal communities’ structure associated with grapevine and assessed using either independent or dependent- approach. The “X” at the independent or dependent-approach column indicates the methodology applied for the microbial community analysis, according to the mentioned study and “--“ indicates the lack of information available. *FD – Flavescence dorée.. Supplementary material 2 (XLSX 11 kb)
10526_2016_9725_MOESM3_ESM.xlsx (11 kb)
Supplementary table 3: General overview of the effects of the viticulture managing practices on bacterial communities. Resume of the studies that analyse the effects of different viticulture management practices on bacterial communities. The “X” at the independent or dependent-approach column indicates the methodology applied for the microbial community analysis, according to the mentioned study and “--“ indicates the lack of information available. *IPM – Integrated Pest Management. Supplementary material 3 (XLSX 11 kb)
10526_2016_9725_MOESM4_ESM.xlsx (11 kb)
Supplementary table 4: General overview of the effects of the viticulture managing practices on fungal communities. Resume of the studies that analyse the effects of different viticulture management practices on fungal communities. The “X” at the independent or dependent-approach column indicates the methodology applied for the microbial community analysis, according to the mentioned study and “--“ indicates the lack of information available. *IPM – Integrated Pest Management. Supplementary material 4 (XLSX 11 kb)

References

  1. Adesemoye A, Torbert H, Kloepper J (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929CrossRefPubMedGoogle Scholar
  2. Arber W (2008) Molecular mechanisms driving Darwinian evolution. Math Comput Model 47:666–674CrossRefGoogle Scholar
  3. Bakker P, Berendsen R, Doornbos R, Wintermans P, Piterse C (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4:165CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baldan E, Nigris S, Populin F, Zottini M, Squartini A, Baldan B (2014) Identification of culturable bacterial endophyte community isolated from tissues of Vitis vinifera Glera. Plant Biosyst 148:508–516CrossRefGoogle Scholar
  5. Barata A, Malfeito-Ferreira M, Loureiro V (2012) The microbial ecology of wine grape berries. Int J Food Microbiol 153:243–259CrossRefPubMedGoogle Scholar
  6. Bartoli C, Lamichhane J, Berge O, Guilbaud C, Varvaro L, Balestra G, Vinatzer B, Morris E (2014) A framework to gage the epidemic potential of plant pathogens in environmental reservoirs: the example of kiwifruit canker. Mol Plant Pathol 16:137–149CrossRefPubMedGoogle Scholar
  7. Baumgartner K (2006) The role of beneficial mycorrhizal fungi in grapevine nutrition. ASEV Tech Update 1:3Google Scholar
  8. Berendsen R, Pieterse C, Bakker P (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486CrossRefPubMedGoogle Scholar
  9. Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18CrossRefPubMedGoogle Scholar
  10. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13CrossRefPubMedGoogle Scholar
  11. Berg J, Tom-Petersen A, Nybroe O (2005) Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Lett Appl Microbiol 40:146–151CrossRefPubMedGoogle Scholar
  12. Berg G, Zachow C, Müller H, Philipps J, Tilcher R (2013) Next-generation bio-products sowing the seeds of success for sustainable agriculture. Agronomy 3:648–656CrossRefGoogle Scholar
  13. Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:1–7Google Scholar
  14. Bertsch C, Ramírez-Suero M, Magnin-Robert M, Larignon P, Chong J, Abou-Mansour E, Spagnolo A, Clément C, Fontaine F (2012) Grapevine trunk diseases: complex and still poorly understood. Plant Pathol 62:243–265CrossRefGoogle Scholar
  15. Bloemberg G, Lugtenberg B (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350CrossRefPubMedGoogle Scholar
  16. Bokulich N, Thorngate J, Richardson P, Mills D (2014) Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc Natl Acad Sci 111:E139–E148CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bruez E, Vallance J, Gerbore J, Lecomte P, Costa JP, Guerin-Dubrana L, Rey P (2014) Analyses of the temporal dynamics of fungal communities colonizing the healthy wood tissues of esca leaf-symptomatic and asymptomatic vines. PLoS ONE 9:e95928CrossRefPubMedPubMedCentralGoogle Scholar
  18. Bulgari D, Casati P, Brusetti L, Quaglino F, Brasca M, Daffonchio D, Bianco P (2009) Endophytic bacterial diversity in grapevine (Vitis vinifera L.) leaves described by 16S rRNA gene sequence analysis and length heterogeneity-PCR. J Microbiol 47:393–401CrossRefPubMedGoogle Scholar
  19. Bulgari D, Casati P, Quaglino F, Bianco P (2014) Endophytic bacterial community of grapevine leaves influenced by sampling date and phytoplasma infection process. BMC Microbiol 14:198–209CrossRefPubMedPubMedCentralGoogle Scholar
  20. Campisano A, Antonielli L, Pancher M, Yousaf S, Pindo M, Pertot I (2014) Bacterial endophytic communities in the grapevine depend on pest management. PLoS ONE 9:e112763CrossRefPubMedPubMedCentralGoogle Scholar
  21. Casieri L, Hofstetter V, Viret O, Gindro K (2009) Fungal communities living in the wood of different cultivars of young Vitis vinifera plants. Phytopathol Mediterr 48:73–83Google Scholar
  22. Chatelet D, Matthews M, Rost T (2006) Xylem structure and connectivity in grapevine (Vitis vinifera) shoots provides a passive mechanism for the spread of bacteria in grape plants. Ann Bot 98:483–494CrossRefPubMedPubMedCentralGoogle Scholar
  23. Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Barka E (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693CrossRefPubMedPubMedCentralGoogle Scholar
  24. Compant S, Kaplan H, Sessitsch A, Nowak J, Barka E, Clément C (2008) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63:84–93CrossRefPubMedGoogle Scholar
  25. Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678CrossRefGoogle Scholar
  26. Compant S, Mitter B, Colli-Mull J, Gangl H, Sessitsch A (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197CrossRefPubMedGoogle Scholar
  27. Compant S, Sessitsch A, Mathieu F (2012) The 125th anniversary of the first postulation of the soil origin of endophytic bacteria: a tribute to M.L.V. Galippe. Plant Soil 356:299–301CrossRefGoogle Scholar
  28. Compant S, Brader G, Muzammil S, Sessitsch A, Lebrihi A, Mathieu F (2013) Use of beneficial bacteria and their secondary metabolites to control grapevine pathogen diseases. BioControl 58:435–455CrossRefGoogle Scholar
  29. Corneo P, Pellegrini A, Cappellin L, Roncador M, Chierici M, Gessler C, Pertot I (2013) Microbial community structure in vineyard soils across altitudinal gradients and in different seasons. FEMS Microbiol Ecol 84:588–602CrossRefPubMedGoogle Scholar
  30. Cosoveanu A, Cabrera Y, Hernandez G, Cabrera R (2014) Endophytic fungi from grapevine cultivars in Canary Islands and their activity against phytopatogenic fungi. Intl J Agri Crop Sci 7:1497–1503Google Scholar
  31. DeAngelis K, Brodie E, DeSantis T, Andersen G, Lindow S, Firestone M (2009) Selective progressive response of soil microbial community to wild oat roots. ISME J 3:168–178CrossRefPubMedGoogle Scholar
  32. Delaunois B, Farace G, Jeandet P, Clément C, Baillieul F, Dorey S, Cordelier S (2014) Elicitors as alternative strategy to pesticides in grapevine? Current knowledge on their mode of action from controlled conditions to vineyard. Environ Sci Pollut Res Int 21:4837–4846CrossRefPubMedGoogle Scholar
  33. Dell’Amico E E, Mazzocchi M, Cavalca L, Allievi L, Andreoni V (2008) Assessment of bacterial community structure in a long-term copper-polluted ex-vineyard soil. Microbiol Res 163:671–683CrossRefPubMedGoogle Scholar
  34. Efsa, PLH Panel (EFSA Panel on Plant Health) (2015) Scientific opinion on the risks to plant health posed by Xylella fastidiosa in the EU territory, with the identification and evaluation of risk reduction options. EFSA J 13:3989Google Scholar
  35. Esparza M (2006) Copper content of grape and wine from Italian farms. Food Addit Contam 23:274–293CrossRefGoogle Scholar
  36. EUROSTAT (2014) European Statistics. Available via EUROSTAT. http://ec.europa.eu/eurostat
  37. FAO (2013) FAOSTAT database collections. Food and Agriculture Organization of the United Nations. Available via FAOSTAT. http://faostat3.fao.org/home/E
  38. Fernández D, Voss K, Bundschuh M, Zubrod J, Schäfer R (2015) Effects of fungicides on decomposer communities and litter decomposition in vineyard streams. Sci Total Environ 533:40–48CrossRefPubMedGoogle Scholar
  39. Fletcher J, Luster D, Bostock R, Burans J, Cardwell K, Gottwald T, McDaniel L, Royer M, Smith K (2010) Emerging infectious plant diseases. In: Scheld W, Grayson M, Hughes J (eds) Emerging infections. ASM Press, Washington DC, pp 337–366Google Scholar
  40. Fontaine F, Pinto C, Vallet J, Clément C, Gomes A, Spagnolo A (2015) The effects of grapevine trunk diseases (GTDs) on vine physiology. Eur J Plant Pathol. Available via Springer Link. http://link.springer.com/article/10.1007%2Fs10658-015-0770-0. Cited 21 Sept 2015
  41. Francl L (2001) The disease triangle: a plant pathological paradigm revisited. The Plant Heal Instr. Available via APS. http://www.apsnet.org/edcenter/instcomm/TeachingArticles/Pages/DiseaseTriangle.aspx
  42. Galippe V (1887a) Note sur la présence de micro-organismes dans les tissus végétaux. CR Hebd Sci Mem Soc Biol 39:410–416Google Scholar
  43. Galippe V (1887b) Note sur la présence de micro-organismes dans les tissus végétaux (2ème note). CR Hebd Sci Mem Soc Biol 39:557–560Google Scholar
  44. Gardener B, Fravel D (2002) Biological control of plant pathogens: research, commercialization, and application in the USA. Plant Heal Prog. Available via APS. http://www.apsnet.org/publications/apsnetfeatures/Pages/biocontrol.aspx. Cited 3 May 2002
  45. González V, Tello M (2011) The endophytic mycota associated with V vinifera. Fungal Divers 47:29–42CrossRefGoogle Scholar
  46. Grube M, Schmid F, Berg G (2011) Black fungi and associated bacterial communities in the phyllosphere of grapevine. Fungal Biol 115:978–986CrossRefPubMedGoogle Scholar
  47. Guo B, Wang Y, Sun X, Tang K (2008) Bioactive natural products from endophytes: a review. Appl Biochem Microbiol 44:136–142CrossRefGoogle Scholar
  48. Hallmann J, Quadt-Hallmann A, Mahaffee W, Kloepper J (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914CrossRefGoogle Scholar
  49. Holland T, Bowen P, Bogdanoff C, Hart M (2013) How distinct are arbuscular mycorrhizal fungal communities associating with grapevines? Biol Fertil Soils 50:667–674CrossRefGoogle Scholar
  50. Hopkins D (2005) Biological control of Pierce’s disease in the vineyard with strains of Xylella fastidiosa benign to grapevine. Plant Dis 89:1348–1352CrossRefGoogle Scholar
  51. Lamb T, Tonkyn D, Kluepfel D (1996) Movement of Pseudomonas aureofaciens from the rhizosphere to aerial plant tissue. Can J Microbiol 42:1112–1120CrossRefGoogle Scholar
  52. Lamichhane J, Varvaro L, Parisi L, Audergon J, Morris C (2014) Disease and frost damage of woody plants caused by Pseudomonas syringae: seeing the forest for the trees. Adv Agron 126:235–295CrossRefGoogle Scholar
  53. Larignon P, Dubos B (1997) Fungi associated with Esca disease in grapevine. Eur J Plant Pathol 103:147–157CrossRefGoogle Scholar
  54. Lejon D, Martins J, Lévêque J, Spadini L, Pascault N, Landry D, Milloux M, Nowak V, Chaussod R, Ranjard L (2008) Copper dynamics and impact on microbial communities in soils of variable organic status. Environ Sci Technol 42:2819–2825CrossRefPubMedGoogle Scholar
  55. Leveau J, Tech J (2011) Grapevine microbiomics: bacterial diversity on grape leaves and berries revealed by high-throughput sequence analysis of 16S rRNA amplicons. Acta Hortic 905:31–42CrossRefGoogle Scholar
  56. Lindow S, Brandl M (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883CrossRefPubMedPubMedCentralGoogle Scholar
  57. Lodewyckx C, Vangronsveld J, Porteous F, Moore E, Taghavi S, Mezgeay M, Lelie D (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–596CrossRefGoogle Scholar
  58. Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12:2165–2179PubMedGoogle Scholar
  59. Magurno F, Balestrini R, Lumini E, Bianciotto V (2010) Outside and inside grapevine roots: arbuscular mycorrhizal fungal communities in a Nebbiolo vineyard. Quad Vitic Enol Univ Torino 31:91–95Google Scholar
  60. Marasco R, Rolli E, Fusi M, Cherif A, Abou-Hadid A, El-Bahairy U, Borin S, Sorlini C, Daffonchio D (2013) Plant growth promotion potential is equally represented in diverse grapevine root-associated bacterial communities from different biopedoclimatic environments. Biomed Res Int 2013:1–17CrossRefGoogle Scholar
  61. Martini M, Musetti R, Grisan S, Polizzotto R, Borselli S, Pavan F, Osler R (2009) DNA-dependent detection of the grapevine fungal endophytes Aureobasidium pullulans and Epicoccum nigrum. Plant Dis 93:993–998CrossRefGoogle Scholar
  62. Martins G, Lauga B, Miot-Sertier C, Mercier A, Lonvaud A, Soulas M, Soulas G, Masneuf-Pomarède I (2013) Characterization of epiphytic bacterial communities from grapes, leaves, bark and soil of grapevine plants grown, and their relations. PLoS ONE 8:e73013CrossRefPubMedPubMedCentralGoogle Scholar
  63. Martins G, Vallance J, Mercier A, Albertin W, Stamatopoulos P, Rey P, Lonvaud A, Masneuf-Pomarède I (2014) Influence of the farming system on the epiphytic yeasts and yeast-like fungi colonizing grape berries during the ripening process. Int J Food Microbiol 177:21–28CrossRefPubMedGoogle Scholar
  64. Mercado-Blanco J, Bakker P (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. A van Leeuw J Microb 92:367–389CrossRefGoogle Scholar
  65. Morens D, Folkers G, Fauci A (2004) The challenge of emerging and re-emerging infectious diseases. Nature 430:242–249CrossRefPubMedGoogle Scholar
  66. Morse S (1995) Factors in the emergence of infectious diseases. Emerg Infect Dis 1:7–15CrossRefPubMedPubMedCentralGoogle Scholar
  67. Müller T, Ruppel S (2014) Progress in cultivation-independent phyllosphere microbiology. FEMS Microbiol Ecol 87:2–17CrossRefPubMedPubMedCentralGoogle Scholar
  68. Newton A, Gravouil C, Fountaine J (2010) Managing the ecology of foliar pathogens: ecological tolerance in crops. Ann Appl Biol 157:343–359CrossRefGoogle Scholar
  69. Pancher M, Ceol M, Corneo P, Longa C, Yousaf S, Pertot I, Campisano A (2012) Fungal endophytic communities in grapevines (Vitis vinifera L.) respond to crop management. Appl Environ Microbiol 78:4308–4317CrossRefPubMedPubMedCentralGoogle Scholar
  70. Pautasso M, Döring T, Garbelotto M, Pellis L, Jeger M (2012) Impacts of climate change on plant diseases-opinions and trends. Eur J Plant Pathol 133:295–313CrossRefGoogle Scholar
  71. Philippot L, Raaijmakers J, Lemanceau P, van der Putten W (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799CrossRefPubMedGoogle Scholar
  72. Pietrzak U, McPhail D (2004) Copper accumulation, distribution and fractionation in vineyard soils of Victoria, Australia. Geoderma 122:151–166CrossRefGoogle Scholar
  73. Pinto C, Pinho D, Sousa S, Pinheiro M, Egas C, Gomes A (2014) Unravelling the diversity of grapevine microbiome. PLoS ONE 9:e85622CrossRefPubMedPubMedCentralGoogle Scholar
  74. Pinto C, Pinho D, Cardoso R, Custódio V, Fernandes J, Sousa S, Pinheiro M, Egas C, Gomes A (2015) Wine fermentation microbiome: a landscape from different Portuguese wine appellations. Front Microbiol 6:1–13CrossRefGoogle Scholar
  75. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315CrossRefPubMedGoogle Scholar
  76. Purcell A (1996) Fastidious xylem-limited bacterial plant pathogens. Annu Rev Phytopathol 34:131–151CrossRefPubMedGoogle Scholar
  77. Pusey P, Stockwell V, Rudell D (2008) Antibiosis and acidification by Pantoea agglomerans strain E325 may contribute to suppression of Erwinia amylovora. Phytopathology 98:1136–1143CrossRefPubMedGoogle Scholar
  78. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis M, Gandolfi C, Casati E, Previtali F, Gerbino R, Cei F, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331CrossRefPubMedGoogle Scholar
  79. Sabate J, Cano J, Esteve-Zarzoso B, Guillamón J (2002) Isolation and identification of yeasts associated with vineyard and winery by RFLP analysis of ribosomal genes and mitochondrial DNA. Microbiol Res 157:267–274CrossRefPubMedGoogle Scholar
  80. Schmid F, Moser G, Müller H, Berg G (2011) Functional and structural microbial diversity in organic and conventional viticulture: organic farming benefits natural biocontrol agents. Appl Environ Microbiol 77:2188–2191CrossRefPubMedPubMedCentralGoogle Scholar
  81. Schreiner R, Mihara K (2009) The diversity of arbuscular mycorrhizal fungi amplified from grapevine roots (Vitis vinifera L.) in Oregon vineyards is seasonally stable and influenced by soil and vine age. Mycologia 101:599–611CrossRefPubMedGoogle Scholar
  82. Setati M, Jacobson D, Andong U, Bauer F (2012) The vineyard yeast microbiome, a mixed model microbial map. PLoS ONE 7:e52609CrossRefPubMedPubMedCentralGoogle Scholar
  83. Setati M, Jacobson D, Bauer F (2015) Sequence-based analysis of the Vitis vinifera L. cv Cabernet Sauvignon grape must mycobiome in three South African vineyards employing distinct agronomic systems. Front Microbiol 6:1–12CrossRefGoogle Scholar
  84. Steenwerth K, Drenovsky R, Lambert J, Kluepfel D, Scow K, Smart D (2008) Soil morphology, depth and grapevine root frequency influence microbial communities in a Pinot Noir vineyard. Soil Biol Biochem 40:1330–1340CrossRefGoogle Scholar
  85. Strange N (2003) The causal agents of plant disease: identity and impact. In: Strange N (ed) Introduction to plant pathology. Wiley, New York, pp 1–30Google Scholar
  86. Tarbah F, Goodman R (1987) Systemic spread of Agrobacterium tumefaciens biovar 3 in the vascular system of grapes. Phytopathology 77:915–920CrossRefGoogle Scholar
  87. Thorne E, Young B, Young G, Stevenson J, Labavitch J, Matthews M, Rost T (2006) The structure of xylem vessels in grapevine (vitaceae) and a possible passive mechanism for the systemic spread of bacterial disease. Am J Bot 93:497–504CrossRefPubMedGoogle Scholar
  88. Turner T, James E, Poole P (2013) The plant microbiome. Genome Biol 14:209–218CrossRefPubMedPubMedCentralGoogle Scholar
  89. Vandenkoornhuyse P, Quaiser A, Duhamel M, Le van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 4:1–11Google Scholar
  90. Vega-Avila D, Gumiere T, Andrade P, Lima-perim J, Durrer A, Baigori M, Vazquez F, Andreote F (2015) Bacterial communities in the rhizosphere of Vitis vinifera L. cultivated under distinct agricultural practices in Argentina. A van Leeuw J Microb 107:575–588CrossRefGoogle Scholar
  91. Verginer M, Leitner E, Berg G (2010) Production of volatile metabolites by grape-associated microorganisms. J Agric Food Chem 58:8344–8350CrossRefPubMedGoogle Scholar
  92. Vurro M, Bonciani B, Vannacci G (2010) Emerging infectious diseases of crop plants in developing countries: impact on agriculture and socio-economic consequences. Food Secur 2:113–132CrossRefGoogle Scholar
  93. West E, Cother E, Steel C, Ash G (2010) The characterization and diversity of bacterial endophytes of grapevine. Can J Microbiol 56:209–216CrossRefPubMedGoogle Scholar
  94. Whipps J (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511CrossRefPubMedGoogle Scholar
  95. Whipps J, Hand P, Pink D, Bending G (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755CrossRefPubMedGoogle Scholar
  96. Yousaf S, Bulgari D, Bergna A, Pancher M, Quaglino F, Casati P, Campisano A (2014) Pyrosequencing detects human and animal pathogenic taxa in the grapevine endosphere. Front Microbiol 5:1–9CrossRefGoogle Scholar
  97. Zarraonaindia I, Gilbert J (2014) Probing the microbial mysteries of wine. Microbe 9:442–447Google Scholar
  98. Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Bokulich N, Mills D, Martin G, Taghavi S, Lelie D, Gilbert J (2015) The soil microbiome influences grapevine-associated microbiota. MBio 6:1–10CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2016

Authors and Affiliations

  1. 1.Genomics UnitBiocant-technology Transfer AssociationCantanhedePortugal

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