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Characterization of isolates of Xanthomonas arboricola pv. corylina, the causal agent of bacterial blight, from Oregon hazelnut orchards

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Abstract

Bacterial blight (Xanthomonas arboricola pv. corylina (Xac)) of hazelnut (Corylus avellana L.) was described first in Oregon in 1915 and is now recognized as a damaging disease of young hazelnut trees worldwide. Thousands of hectares of new hazelnut cultivars that are resistant to eastern filbert blight (Anisogramma anomala) are being planted in the Willamette Valley of Oregon, where 99% of the US hazelnut crop is grown. Reports of bacterial blight on young hazelnut trees have increased but information about the causal pathogen is limited. Isolates were recovered from tissues with bacterial blight symptoms that were then characterized for their ability to grow on semi-selective media, their nutrient utilization profiles using Biolog GN2, quinate metabolism, copper tolerance, hypersensitive response on tobacco, and pathogenicity on hazelnut. Additionally, isolates were identified with a duplex PCR assay (ftsX and qumA), 16S rRNA sequence, and multi-locus sequence analysis (MLSA) using rpoD and gyrB. Pathogenic isolates were identified as Xac using morphological, biochemical, molecular, and host assays. Using MLSA, Xac isolates from Oregon separated into two clades, one clade with the type strain and a second clade previously described using isolates from Europe. The phylogenetic diversity of Xac observed in other countries also is present in Oregon.

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References

  • Almeida NF, Yan S, Cai R, Clarke CR, Morris CE, Schaad NW, Schuenzel EL, Lacy GH, Sun X, Jones JB, Castillo JA, Bull CT, Leman S, Guttman DS, Setubal JC, Vinatzer BA (2010) PAMDB, a multi-locus sequence typing and analysis database and website for plant-associated microbes. Phytopathology 100:208–215. https://doi.org/10.1094/PHYTO-100-3-0208

    Article  CAS  PubMed  Google Scholar 

  • Andersen GL, Menkissoglou O, Lindow SE (1991) Occurrence and properties of copper-tolerant strains of Pseudomonas syringae isolated from fruit trees in California. Phytopathology 81:648–656

    Article  CAS  Google Scholar 

  • Barss HP (1915) Economic entomology. A new filbert disease in Oregon, Pamphlets

    Google Scholar 

  • Belisario A, Zoina A, Pezza L, Luongo L (1999) Susceptibility of species of Juglans to pathovars of Xanthomonas campestris. Eur J Plant Pathol 29:75–80

    Google Scholar 

  • Boudon S, Manceau C, Nottéghem J-L (2005) Structure and origin of Xanthomonas arboricola pv. pruni populations causing bacterial spot of stone fruit trees in Western Europe. Phytopathology 95:1081–1088

    Article  PubMed  Google Scholar 

  • Caballero JI, Zerillo MM, Snelling J, Boucher C, Tisserat N (2013) Genome sequence of Xanthomonas arboricola pv. corylina, isolated from Turkish filbert in Colorado. Genome Announc 1. https://doi.org/10.1128/genomeA.00246-13

  • Cesbron S, Briand M, Essakhi S, Gironde S, Boureau T, Manceau C, Fischer-Le Saux M, Jacques M-A (2015) Comparative genomics of pathogenic and nonpathogenic strains of Xanthomonas arboricola unveil molecular and evolutionary events linked to pathoadaptation. Front Plant Sci 6. https://doi.org/10.3389/fpls.2015.01126

  • EPPO (2004) EPPO quarantine pest ID Xanthomonas arboricola pv. corylina. Bull. OEPP/EPPO Bull 34:179–181

    Article  Google Scholar 

  • Fargier E, Fischer-Le Saux M, Manceau C (2011) A multi-locus sequence analysis of Xanthomonas campestris reveals a complex structure within crucifer-attacking pathovars of this species. Syst Appl Microbiol 34:156–165. https://doi.org/10.1016/j.syapm.2010.09.001

    Article  CAS  PubMed  Google Scholar 

  • Fischer-Le Saux M, Bonneau S, Essakhi S, Manceau C, Jacques M-A (2015) Aggressive emerging pathovars of Xanthomonas arboricola represent widespread epidemic clones distinct from poorly pathogenic strains, as revealed by multi-locus sequence typing. Appl Environ Microbiol 81:4651–4668. https://doi.org/10.1128/AEM.00050-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardan L, Devaux M (1987) La bactériose du noisetier (Xanthomonas campestris pv. corylina): biologie de la bactérie. EPPO Bull 17:241–250. https://doi.org/10.1111/j.1365-2338.1987.tb00034.x

    Article  Google Scholar 

  • Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, de Peer YV, Vandamme P, Thompson FL, Swings J (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739. https://doi.org/10.1038/nrmicro1236

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. https://doi.org/10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  • Johnson K, Mehlenbacher S, Stone J, Pscheidt J, Pinkerton J (1996) Eastern filbert blight of European hazelnut. Plant Dis 80:1308–1316

    Article  Google Scholar 

  • Johnson KB, Stockwell VO, Burgett DM, Sugar D, Loper JE (1993) Dispersal of Erwinia amylovora and Pseudomonas fluorescens by honey bees from hives to apple and pear blossoms. Phytopathology 83:995–1002

    Article  Google Scholar 

  • Kałużna M, Puławska J, Waleron M, Sobiczewski P (2014) The genetic characterization of Xanthomonas arboricola pv. juglandis, the causal agent of walnut blight in Poland. Plant Pathol 63:1404–1416. https://doi.org/10.1111/ppa.12211

    Article  CAS  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazempour MN, Ali B, Elahinia SA (2006) First report of bacterial blight of hazelnut caused by Xanthomonas arboricola pv. corylina in Iran. J Plant Pathol 88:340

    Google Scholar 

  • Lamichhane JR, Fabi A, Ridolfi R, Varvaro L (2013) Epidemiological study of hazelnut bacterial blight in Central Italy by using laboratory analysis and geostatistics. PLoS One 8:e56298. https://doi.org/10.1371/journal.pone.0056298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamichhane JR, Varvaro L (2014) Xanthomonas arboricola disease of hazelnut: current status and future perspectives for its management. Plant Pathol 63:243–254. https://doi.org/10.1111/ppa.12152

    Article  Google Scholar 

  • Lee YA, Hildebrand DC, Schroth MN (1992) Use of quinate metabolism as a phenotypic property to identify members of Xanthomonas campestris DNA homology group 6. Physiol Biochem 82:971–973

    CAS  Google Scholar 

  • Locke T, Barnes D (1979) New or unusual records of plant diseases and pests. Plant Pathol 28:53–53. https://doi.org/10.1111/j.1365-3059.1979.tb02620.x

    Article  Google Scholar 

  • Luisetti J, Jailloux F, Germain E, Prunier JP, Gardan L (1976) Caractérisation de Xanthomonas corylina responsable de la bactériose du noisetier récemment observée en France. Comptes Rendus des Seances de l’Academie d’Agriculture de France 61:845–849

    Google Scholar 

  • Mehlenbacher SA, Smith DC, McCluskey RL (2019) ‘PollyO’ hazelnut. HortScience 54:1429–1432. https://doi.org/10.21273/HORTSCI14089-19

    Article  Google Scholar 

  • Mehlenbacher SA, Smith DC, McCluskey RL (2016) ‘McDonald’ hazelnut. HortScience 51:757–760. https://doi.org/10.21273/HORTSCI.51.6.757

    Article  Google Scholar 

  • Mehlenbacher SA, Smith DC, McCluskey RL (2014) ‘Wepster’ hazelnut. HortScience 49:346–349. https://doi.org/10.21273/HORTSCI.49.3.346

    Article  Google Scholar 

  • Mehlenbacher SA, Smith DC, McCluskey RL (2013) ‘Dorris’ hazelnut. HortScience 48:796–799. https://doi.org/10.21273/HORTSCI.48.6.796

    Article  Google Scholar 

  • Mehlenbacher SA, Smith DC, McCluskey RL (2011) ‘Jefferson’ hazelnut. HortScience 46:662–664. https://doi.org/10.21273/HORTSCI.46.4.662

    Article  Google Scholar 

  • Mehlenbacher SA, Miller AN (1989) ‘Barcelona’ hazelnut. Fruit Varieties Journal 43:90–95

    Google Scholar 

  • Miller PW, Bollen WB, Simmons JE, Gross HN, Barss HP (1940) The pathogen of filbert bacteriosis compared with Phytomonas juglandis the cause of walnut blight. Phytopathology 30:713–733

    Google Scholar 

  • Miller PW, Bollen WB, Simmons JE (1949) Filbert bacteriosis and its control (technical report 16). Agricultural Experiment Station, Oregon State College, Corvallis

    Google Scholar 

  • Moore LW (1974) Stress predisposes young filbert trees to bacterial blight. Phytopathology 64:15–37. https://doi.org/10.1094/Phyto-64-1537

    Article  Google Scholar 

  • Olsen, J., 2013. Growing hazelnuts in the Pacific Northwest: orchard site selection. OSU Hazelnut Ext. Serv. 4

  • Pacific Agricultural Survey LLC [WWW Document] (2019). Pac. AG Surv. URL http://www.pacificagsurvey.com/ (accessed 5.14.19)

  • Parkinson N (2007) Phylogenetic analysis of Xanthomonas species by comparison of partial gyrase B gene sequences. Int J Syst Evol Microbiol 2881–2887

  • Parkinson N, Elphinstone J (2010) Species and infra-species phylogenetic discrimination of Pseudomonad and Xanthomonad pathogens of stone fruit and nuts. J Plant Pathol 92:S1.15–S1.19. https://doi.org/10.4454/jpp.v92i1sup.2502

    Article  Google Scholar 

  • Pisetta M, Albertin I, Petriccione M, Scortichini M (2016) Effects of hot water treatment to control Xanthomonas arboricola pv. corylina on hazelnut (Corylus avellana L.) propagative material. Sci Hortic 211:187–193. https://doi.org/10.1016/j.scienta.2016.08.019

    Article  Google Scholar 

  • Pothier JF, Pagani MC, Pelludat C, Ritchie DF, Duffy B (2011) A duplex-PCR method for species- and pathovar-level identification and detection of the quarantine plant pathogen Xanthomonas arboricola pv. pruni. J Microbiol Methods 86:16–24. https://doi.org/10.1016/j.mimet.2011.03.019

    Article  CAS  PubMed  Google Scholar 

  • Prokić A, Gašić K, Ivanović MM, Kuzmznović N, Šević M, Puławska J, Obradović A (2012) Detection and identification methods and new tests as developed and used in the framework of cost873 for bacteria pathogenic to stone fruits and nuts Xanthomonas arboricola pv. corylina. J Plant Pathol 94:S1.127–S1.133 https://doi.org/10.4454/jpp.v94i1sup.020

    Google Scholar 

  • Pulawska J, Kaluzna M, Kolodziejska A, Sobiczewski P (2010) Identification and characterization of Xanthomonas arboricola pv. corylina causing bacterial blight of hazelnut: a new disease in Poland. J Plant Pathol 92:803–806

    Google Scholar 

  • Rothleutner JJ, Contreras RN, Stockwell VO, Owen JS (2014) Screening cotoneaster for resistance to fire blight by artificial inoculation. HortScience 49:1480–1485

    Article  Google Scholar 

  • Scortichini M, Rossi MP, Marchesi U (2002) Genetic, phenotypic and pathogenic diversity of Xanthomonas arboricola pv. corylina strains question the representative nature of the type strain. Plant Pathol 51:374–381

    Article  Google Scholar 

  • Stockwell VO, Johnson KB, Loper JE (1998) Establishment of bacterial antagonists of Erwinia amylovora on pear and apple blossoms as influenced by inoculum preparation. Phytopathology 88:506–513

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2019). R: a language and environment for statistical computing. 2013

  • U.S. Department of Agriculture, Economic Research Service (USDA, ERS). 2019. Fruit and Tree Nut Data 2018

  • Vauterin L, Hoste B, Kersters K, Swings J (1995) Reclassification of Xanthomonas. Int J Syst Evol Microbiol 45:472–489

    CAS  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wimalajeewa DL, Washington WS (1980) New diseases: bacterial blight of hazelnut. Australas Plant Pathol 9:112–113

    Article  Google Scholar 

  • Wiman, N., Pscheidt, J.W., Moretti, M., 2019. 2019 Hazelnut pest management guide for the Willamette Valley. Or. State Univ. Ext. EM8328

  • Young JM, Park D-C, Shearman HM, Fargier E (2008) A multi-locus sequence analysis of the genus Xanthomonas. Syst Appl Microbiol 31:366–377. https://doi.org/10.1016/j.syapm.2008.06.004

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Oregon hazelnut growers and field agents that allowed us to survey their orchards, reported disease symptoms, and supplied infected plant material. We specifically thank Jeff Newton and Christensen Farms for access to their orchard for pathogenicity testing. Sincere thanks to Brenda Shaffer and Gayle McGhee of the USDA ARS Horticultural Crops Research Unit for excellent technical assistance.

Funding

This research was funded in part by Jan and Linda Wepster, the Oregon Hazelnut Commission, and Birkemeier Nursery, Canby, Oregon.

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Correspondence to Virginia O. Stockwell.

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Webber, J.B., Putnam, M., Serdani, M. et al. Characterization of isolates of Xanthomonas arboricola pv. corylina, the causal agent of bacterial blight, from Oregon hazelnut orchards. J Plant Pathol 102, 799–812 (2020). https://doi.org/10.1007/s42161-020-00505-6

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