Diversity of bacterial endophytes in 3 and 15 year-old grapevines of Vitis vinifera cv. Corvina and their potential for plant growth promotion and phytopathogen control

Microbiological Research

Volumn 183, Issue , 2016, Pages 42-52

  Andreolli, Marco ^a   Lampis, Silvia ^a   Zapparoli, Giacomo ^a   Angelini, Elisa ^b   Vallini, Giovanni ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b CREA VIT   (Italy)

Author keywords

Bacterial endophytes; Biocontrol; Grapevine; Plant growth promoting bacteria; Vitis vinifera cv. Corvina

Indexed keywords

BACTERIA; BIOCONTROL; PLANTS (BOTANY);

1 AMINOCYCLOPROPANE 1 CARBOXYLATES; ANTI-FUNGAL ACTIVITY; BACTERIAL ENDOPHYTES; GRAPEVINE; INDOLE-3-ACETIC ACID; PLANT GROWTH PROMOTING BACTERIUM; PLANT GROWTH PROMOTION; VITIS VINIFERA;

BACTERIOLOGY;

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOCONTROL AGENT; BIOTECHNOLOGY; ENDOPHYTE; GENOTYPE; GROWTH RATE; MICROBIAL COMMUNITY; PATHOGEN; PHYTOCHEMISTRY; SIDEROPHORE; VINE;

ACTINOBACTERIA; BACILLI (CLASS); BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA; PANTOEA; RHIZOBIUM; VITIS; VITIS VINIFERA;

1-AMINOCYCLOPROPANE-1-CARBOXYLATE DEAMINASE; AMMONIA; ANTIFUNGAL AGENT; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE; LYASE; PHOSPHATE; RNA 16S;

BACTERIUM; BIODIVERSITY; CLASSIFICATION; DNA SEQUENCE; ENDOPHYTE; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT DISEASE; PLANT ROOT; PREVENTION AND CONTROL; VITIS;

AMMONIA; ANTIFUNGAL AGENTS; BACTERIA; BASE SEQUENCE; BIODIVERSITY; CARBON-CARBON LYASES; CLONING, MOLECULAR; ENDOPHYTES; GENOTYPE; INDOLEACETIC ACIDS; PHOSPHATES; PHYLOGENY; PLANT DISEASES; PLANT ROOTS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; VITIS;

EID: 84957095174     PISSN: 09445013     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micres.2015.11.009     Document Type: Article

References (68)

1. Ait Barka E., Gognies S., Nowak J., Audran J.-C., Belarbi A. Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol. Control 2002, 24:135-142.
2. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. Andreolli M., Lampis S., Zenaro E., Salkinoja-Salonen M., Vallini G. Burkholderia fungorum DBT1: a promising, bacterial strain for bioremediation of PAHs-contaminated soils. FEMS Microbiol. Lett. 2011, 319:11-18.
4. Andreolli M., Lampis S., Poli M., Gullner G., Biró B., Vallini G. Endophytic Burkholderia fungorum DBT1 can improve phytoremediation efficiency of polycyclic aromatic hydrocarbons. Chemosphere 2013, 92:688-694.
5. Baldan E., Nigris S., Populin F., Zottini M., Squartini A., Baldan B. Identification of culturable bacterial endophyte community isolated from tissues of Vitis vinifera Glera. Plant Biosyst. 2014, 148:508-516.
6. Bell C.R., Dickie G.A., Harvey W.L.G., Chan J.W.Y.F. Endophytic bacteria in grapevine. Can. J. Microbiol. 1995, 41:46-53.
7. Bohm M., Hurek T., Reinhold-Hurek B. Twitching motility is essential for endophytic rice colonization by the N-2-fixing endophyte Azoarcus sp. strain BH72. Mol. Plant Microbe Interact. 2007, 20:526-533.
8. Bulgari D., Casati P., Brusetti L., Quaglino F., Brasca M., Daffonchio D., Bianco P.A. Endophytic bacterial diversity in grapevine (Vitis vinifera L.) leaves described by 16S rRNA gene sequence analysis and length heterogeneity-PCR. J. Microbiol. 2009, 47:393-401.
9. Bulgari D., Casati P., Crepaldi P., Daffonchio D., Quaglino F., Brusetti L., Bianco P.A. Restructuring of endophytic bacterial communities in grapevine yellows-diseased and recovered Vitis vinifera L. plants. Appl. Environ. Microbiol. 2011, 77:5018-5022.
10. Cabanás C.G.-L., Schilirò E., Valverde-Corredor A., Mercado-Blanco J. The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots. Front. Microbiol. 2014, 5:427.
11. Campisano A., Antonielli L., Pancher M., Yousaf S., Pindo M., Pertot I. Bacterial endophytic communities in the grapevine depend on pest management. PLoS One 2014, 9:e112763.
12. Campisano A., Pancher M., Puopolo G., Puddu A., Lòpez-Fernàndez S., Biagini B., Yousaf S., Pertot I. Diversity in endophytic populations reveals functional and taxonomic diversity between wild and domesticated grapevines. Am. J. Enol. Vitic. 2015, 66:12-21.
13. Cappuccino J.C., Sherman N. Microbiology: A Laboratory Manual 1992, Benjamin/Cummings Pub. Co., New York. 3th edn.
14. Chun J., Lee J.H., Jung Y., Kim M., Kim S., Kim B.K., Lim Y.W. EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int. J. Syst. Evol. Microbiol. 2007, 57:2259-2261.
15. Compant S., Clement C., Sessitsch A. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 2010, 42:669-678.
16. Compant S., Mitter B., Colli-Mull J.G., Gangl H., Sessitsch A. 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, 62:188-197.
17. Crous P.W., Gams W. Phaeomoniella chlamydospora genet comb. nov., a causal organism of Petri grapevine decline and esca. Phytopathol. Mediterr. 2000, 39:112-118.
18. Dai Z.W., Ollat N., Gomès E., Decroocq S., Tandonnet J.-P., Bordenave L., Pieri P., Hilbert G., Kappel C., van Leeuwen C., Vivin P., Delrot S. Ecophysiological, genetic, and molecular causes of variation in grape berry weight and composition: a review. Am. J. Enol. Vitic. 2011, 62:413-425.
19. Datta B., Chakrabartty P.K. Siderophore biosynthesis genes of Rhizobium sp. isolated from Cicer arietinum L. 3 Biotech 2014, 4:391-401.
20. Di Carli M., Zamboni A., Pè M.E., Pezzotti M., Lilley K.S., Benvenuto E., Desiderio A. Two-dimensional differential in gel electrophoresis (2D-DIGE) analysis of grape berry proteome during postharvest withering. J. Proteome. Res. 2011, 10:429-446.
21. Dupont J., Laloui W., Magnin S., Larignon P., Roquebert M.F. Phaeoacremonium viticola, a new species associated with esca disease of grapevine in France. Mycologia 2000, 92:499-504.
22. FAOSTAT, 2011. http://faostat.fao.org.
23. Feliciano A.J., Gubler W.D. Histological investigations on infection of grape roots and shoots by Phaeoacremonium spp. Phytopathol. Mediterr. 2001, 40(Suppl):387-393.
24. Gordon S.-A., Weber R.P. Colorimetric estimation of indoleacetic acid. Plant Physiol. 1951, 26:192-195.
25. Grichko V.P., Filby B., Glick B.R. Increased ability of transgenic plants expressing the bacterial enzyme ACC deaminase to accumulate Cd, Co, Cu, Ni, Pb, and Zn. J. Biotechnol. 2000, 81:45-53.
26. Guerra B., Steenwerth K. Influence of floor management technique on grapevine growth, disease pressure, and juice and wine composition: a review. Am. J. Enol. Vitic. 2012, 63:149-164.
27. Hammer Ø., Harper D.A.T., Ryan P.D. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron 2001, 4-9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm.
28. Hardoim P.R., van Overbeek L.S., Berg G., Pirttilä A.M., Compant S., Campisano A., Döring M., Sessitsch A. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 2015, 79:293-320.
29. Kado C.I. Plant pathogenic bacteria. The Prokaryotes 1992, 660-662. Springerverlang, New York. A. Ballows, G.G. Truper, M. Dworkin, W. Harden, K.H. Schleifer (Eds.).
30. Kang Y.M., Lee C.K., Cho K.M. Diversity and antimicrobial activity of isolated endophytic bacteria from Deodeok (Codonopsis lanceolata) of different locations and ages. Afr. J. Microbiol. Res. 2013, 7:1015-1028.
31. Kumar S., Nei M., Dudley J., Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 2008, 9:299-306.
32. Larignon P., Dubos B. Fungi associated with esca disease in grapevine. Eur. J. Plant Pathol. 1997, 103:147-157.
33. Loaces I., Ferrando L., Scavino A.F. Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microbial. Ecol. 2011, 61:606-618.
34. Lorenzini M., Azzolini M., Tosi E., Zapparoli G. Postharvest grape infection of Botrytis cinerea and its interactions with other moulds under withering conditions to produce noble-rotten grapes. J. Appl. Microbiol. 2013, 114:762-770.
35. Ma L., Cao Y.H., Cheng M.H., Huang Y., Mo M.H., Wang Y., Yang J.Z., Yang F.X. Phylogenetic diversity of bacterial endophytes of Panax notoginseng with antagonistic characteristics towards pathogens of root-rot disease complex. Antonie Van Leeuwenhoek 2013, 103:299-312.
36. Madhaiyan M., Poonguzhali S., Sa T. Characterization of 1-aminocyclopropane-1-carboxylate (ACC) deaminase containing Methylobacterium oryzae and interactions with auxins and ACC regulation of ethylene in canola (Brassica campestris). Planta 2007, 226:867-876.
37. Masih E.I., Slezack Deschaumes S., Marmaras I., Barka E.A., Vernet G., Charpentier C., Adholeya A., Paul B. Characterization of the yeast Pichia membranifaciens and its possible use in the biological control of Botrytis cinerea causing the grey mould disease of grapevine. FEMS Microbiol. Lett. 2001, 202:227-232.
38. Mayer A.M. Determination of indole acetic acid by the Salkowsky reaction. Nature 1958, 182:1670-1671.
39. Melnick R.L., Suárez C., Bailey B.A., Backman P.A. Isolation of endophytic endospore-forming bacteria from Theobroma cacao as potential biological control agents of cacao diseases. Biol. Control 2011, 57:236-245.
40. Mostert L., Groenewald J.Z., Summerbell R.C., Robert V., Sutton D.A., Padhye A.A., Crous P.W. Species of Phaeoacremonium associated with infections in humans and environmental reservoirs in infected woody plants. J. Clin. Microbiol. 2005, 43:1752-1767.
41. Nabti E., Bensidhoum L., Tabli N., Dahel D., Weiss A., Rothballer M., Schmid M., Hartmann A. Growth stimulation of barley and biocontrol effect on plant pathogenic fungi by a Cellulosimicrobium sp. strain isolated from salt-affected rhizosphere soil in northwestern Algeria. Eur. J. Soil Biol. 2014, 61:20-26.
42. Nagarajkumar M., Bhaskaran R., Velazhahan R. Involvement of secondary metabolites and extracellular lytic enzymes produced by Pseudomonas fluorescens in inhibition of Rhizoctonia solani, the rice sheath blight pathogen. Microbiol. Res. 2004, 159:73-81.
43. Nascimento T.L., Oki Y., Lima D.M.M., Almeida-Cortez J.S., Fernandes G.W., Souza-Motta C.M. Biodiversity of endophytic fungi in different leaf ages of Calotropis procera and their antimicrobial activity. Fungal Ecol. 2015, 14:79-86.
44. Natul N., Sharma G.D., Barooah M. Screening of endophytic bacterial isolates of tea (Camellia sinensis L.) roots for their multiple plant growth promoting activities. Int. J. Agric. Environ. Biotechnol. 2013, 6:211-215.
45. Nautiyal C.S. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol. Lett. 1999, 170:265-270.
46. Naveed M., Mitter B., Yousaf S., Pastar M., Afzal M., Sessitsch A. The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol. Fert. Soils 2014, 50:249-262.
47. Park M.S., Jung S.R., Lee M.S., Kim K.O., Do J.O., Lee K.H., Kim S.B., Bae K.S. Isolation and characterization of bacteria associated with two sand dune plant species, Calystegia soldanella and Elymus mollis. J. Microbiol. 2005, 43:219-227.
48. Penrose D.M., Glick B.R. Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol. Plantarum 2003, 118:10.
49. Phillips A.J.L., Alves A., Abdollahzadeh J., Slippers B., Wingfield M.J., Groenewald J.Z., Crous P.W. The Botryosphaeriaceae: genera and species known from culture. Stud. Mycol. 2013, 76:51-167.
50. Qin S., Xing K., Jiang J.-H., Xu L.-H., Li W.-J. Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl. Microbiol. Biotechnol. 2011, 89:457-473.
51. Quecine M.C., Araújo W.L., Rossetto P.B., Ferreira A., Tsui S., Lacava P.T., Mondin M., Azevedo J.L., Pizzirani-Kleinera A.A. Sugarcane growth promotion by the endophytic bacterium Pantoea agglomerans 33.1. Appl. Environ. Microbiol. 2012, 78:7511-7518.
52. Rosenblueth M., Martínez-Romero E. Bacterial endophytes and their interaction with hosts. Mol. Plant-Microbe Interact. 2006, 19:827-837.
53. Schwyn B., Neilands J.B. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 1987, 160:47-56.
54. Shan H., Zhao M., Chen D., Cheng J., Li J., Feng Z., Ma Z., An D. Biocontrol of rice blast by the phenaminomethylacetic acid producer of Bacillus methylotrophicus strain BC79. Crop Protect. 2013, 44:29-37.
55. Singh R.K., Kumar D.P., Solanki M.K., Singh P., Srivastva A.K., Kumar S., Kashyap P.L., Saxena A.K., Singhal P.K., Arora D.K. Optimization of media components for chitinase production by chickpea rhizosphere associated Lysinibacillus fusiformis B-CM18. J. Basic Microbiol. 2013, 53:451-460.
56. Son J.-S., Sumayo M.H., wang Y.-J., Kim B.-S., Sa-Youl G., Ghim S.-Y. Screening of plant growth-promoting rhizobacteria as elicitor of systemic resistance against gray leaf spot disease in pepper. Appl. Soil Ecol. 2014, 73:1-8.
57. Taechowisan T., Lumyong S. Activity of endophytic actimomycetes from roots of Zingiber officinale and Alpinia galanga against phytopathogenic fungi. Ann. Microbiol. 2003, 53:291-298.
58. Taghavi S., Garafola C., Monchy S., Newman L., Hoffman A., Weyens N., Barac T., Vangronsveld J., van der Lelie D. Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of Poplar trees. Appl. Environ. Microbiol. 2009, 75:748-757.
59. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
60. Toffali K., Zamboni A., Anesi A., Stocchero M., Pezzotti M., Levi M., Guzzo F. Novel aspects of grape berry ripening and post-harvest withering revealed by untargeted LC-ESI-MS metabolomics analysis. Metabolomics 2011, 7:424-436.
61. Tumbarski Y., Valcheva-Zhekova N., Koleva I., Denkova Z. Antimicrobial activity against some saprophytic and pathogenic microorganisms of Bacillus species strains isolated from natural spring waters in Bulgaria. Br. Microbiol. Res. J. 2014, 4:1353-1369.
62. Úrbez-Torres J.R., Peláez H., Santiago Y., Martín C., Moreno C., Gubler W.D. Occurrence of Botryosphaeria obtusa, B. dothidea, and B. parva associated with grapevine trunk diseases in Castilla y León region, Spain. Plant Dis. 2006, 90:835.
63. Úrbez-Torres J.R., Haag P., Bowen P., O'Gorman D.T. Grapevine trunk diseases in British Columbia: incidence and characterization of the fungal pathogens associated with Esca and petri diseases of grapevine. Plant Dis. 2014, 98:469-482.
64. Van Belkum A., Sluijter M., de Groot R., Verbrugh H., Hermans P.W.M. Novel BOX repeat PCR assay for high-resolution typing of Streptococcus pneumoniae strains. J. Clin. Microbiol. 1996, 34:1176-1179.
65. Vendan R.T., Joon Yu Y.J., Lee S.H., Rhee Y.H. Diversity of endophytic bacteria in Ginseng and their potential for plant growth promotion. J. Microbiol. 2010, 48:559-565.
66. Venturini L., Ferrarini A., Zenoni S., Tornielli G.B., Fasoli M., Dal Santo S., Minio A., Buson G., Tononi P., Zago E.D., Zamperin G., Bellin D., Pezzotti M., Delledonne M. De novo transcriptome characterization of Vitis vinifera cv. Corvina unveils varietal diversity. BMC Genom. 2013, 14:41.
67. Weisburg W.G., Barns S.M., Pelletier D.A., Lane D.J. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 1991, 173:697-703.
68. West E.R., Cother E.J., Steel C.C., Ash G.J. The characterization and diversity of endophytes of grapevine. Can. J. Microbiol. 2010, 56:209-216.