Vol. 62 No. 1 (2023)
Articles

TaqMan qPCR assays improve Pseudomonas syringae pv. actinidiae biovar 3 and P. viridiflava (PG07) detection within the Pseudomonas sp. community of kiwifruit

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  • Sara CAMPIGLI,
  • Simone LUTI,
  • Tommaso MARTELLINI,
  • Domenico RIZZO,
  • Linda BARTOLINI,
  • Claudio CARRAI,
  • Jeyaseelan BASKARATHEVAN,
  • Luisa GHELARDINI,
  • Francesca PEDUTO HAND,
  • Guido MARCHI
Sara CAMPIGLI
Department of Agriculture, Food, Environment and Forestry, University of Florence, P.le delle Cascine 18, Florence, 50144
Simone LUTI
Department of Experimental and Clinical Biomedical Sciences, University of Florence, Viale Morgagni 50, Florence, 50134
Tommaso MARTELLINI
Department of Agriculture, Food, Environment and Forestry, University of Florence, P.le delle Cascine 18, Florence, 50144
Domenico RIZZO
Regione Toscana, Servizio Fitosanitario Regionale e di Vigilanza e Controllo Agroforestale, Via A. Manzoni 16, Florence, 50121
Linda BARTOLINI
Regione Toscana, Servizio Fitosanitario Regionale e di Vigilanza e Controllo Agroforestale, Via A. Manzoni 16, Florence, 50121
Claudio CARRAI
Regione Toscana, Servizio Fitosanitario Regionale e di Vigilanza e Controllo Agroforestale, Via A. Manzoni 16, Florence, 50121
Jeyaseelan BASKARATHEVAN
Plant Health & Environment Laboratory, Diagnostic and Surveillance Services, Biosecurity New Zealand, Ministry for Primary Industries, PO Box 2095, Auckland, 1140
Luisa GHELARDINI
Department of Agriculture, Food, Environment and Forestry, University of Florence, P.le delle Cascine 18, Florence, 50144
Francesca PEDUTO HAND
Department of Plant Pathology, The Ohio State University, Columbus, OH 43220
Guido MARCHI
Department of Agriculture, Food, Environment and Forestry, University of Florence, P.le delle Cascine 18, Florence, 50144
DOI: https://doi.org/10.36253/phyto-14400
Categories

Published 2023-05-08

Keywords

  • Actinidia sp.,
  • orchard variability,
  • Pseudomonas syringae species complex,
  • specificity

How to Cite

[1]
S. CAMPIGLI, “TaqMan qPCR assays improve Pseudomonas syringae pv. actinidiae biovar 3 and P. viridiflava (PG07) detection within the Pseudomonas sp. community of kiwifruit”, Phytopathol. Mediterr., vol. 62, no. 1, pp. 95–114, May 2023.

Copyright (c) 2023 Sara CAMPIGLI, Simone LUTI, Tommaso MARTELLINI, Domenico RIZZO, Linda BARTOLINI, Claudio CARRAI, Jeyaseelan BASKARATHEVAN, Luisa GHELARDINI, Francesca PEDUTO HAND, Guido MARCHI

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This work is licensed under a Creative Commons Attribution 4.0 International License.

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Abstract

Kiwifruit is inhabited by a heterogeneous community of bacteria belonging to the Pseudomonas syringae species complex (Pssc). Only a few of its members, such as the specialist Pseudomonas syringae pv. actinidiae biovar 3 (Psa3), are known as pathogens, but for most of the species, such as P. viridiflava (Pv), a generalist with high intraspecific variation, the nature of their relationship with kiwifruit is unclear. Currently, no culture independent molecular diagnostic assay is available for Pv. In this study we validated two TaqMan qPCR diagnostic assays adopting a strategy that for the first time widely focuses on the Pseudomonas sp. community associated to kiwifruit in Tuscany (Italy). Primers and probes were designed based on the sequence of the lscγ gene of Psa3 (qPCRPsa3) and the rpoD gene of Pv phylogroup 7 (qPCRPv7). Both qPCR assays have a LOD of 60 fg of DNA. By using reference strains along with 240 strains isolated from kiwifruit and characterized ad hoc as Pseudomonas sp., specificity was proven for members of six of the 13 Pssc phylogroups. Moreover, to evaluate the possible effects of seasonal variations in the Pseudomonas sp. community composition on assay specificity, the assays were tested on naturally infected leaves and canes sampled from different orchards throughout a growing season. At last, by proving qPCR’s capacity to detect latent infections in artificially inoculated leaves, their potential usefulness in surveillance programs and for epidemiological studies was verified.

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References

  1. Angelini E., Clair D., Borgo M., Bertaccini A., Boudon-Padieu E., 2001. Flavescence dorée in France and Italy-Occurrence of closely related phytoplasma isolates and their near relationships to Palatinate grapevine yellows and an alder yellows phytoplasma. Vitis. 40:79-86. https://doi.org/10.5073/vitis.2001.40.79-86
  2. Araki H., Tian D., Goss E. M., Jakob K., Halldorsdottir S. S.,… Bergelson J. 2006. Presence/absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava, a pathogen of Arabidopsis. Proceedings of the National Academy of Sciences. 103:5887-5892. https://doi.org/10.1073/pnas.0601431103 DOI: https://doi.org/10.1073/pnas.0601431103
  3. Balestra G. M., Mazzaglia A., Quattrucci A., Renzi M., Rossetti A., 2009. Occurrence of Pseudomonas syringae pv. actinidiae in Jin Tao kiwi plants in Italy. Phytopathologia Mediterranea. 48:299-301. DOI: 10.14601/Phytopathol_Mediterr-2821
  4. Balestra G. M., Varvaro L., 1998. Seasonal fluctuations in kiwifruit phyllosphere and ice nucleation activity of Pseudomonas viridiflava. Journal of Plant Pathology. 80: 151-156. http://dx.doi.org/10.4454/jpp.v80i2.812
  5. Baltrus D. A., McCann H. C., Guttman D. S., 2017. Evolution, genomics and epidemiology of Pseudomonas syringae: challenges in bacterial molecular plant pathology. Molecular plant pathology. 18:152-168. https://doi.org/10.1111/mpp.12506 DOI: https://doi.org/10.1111/mpp.12506
  6. Bartoli C., Berge O., Monteil C. L., Guilbaud C., Balestra G. M., … Morris C. E., 2014. The Pseudomonas viridiflava phylogroups in the P. syringae species complex are characterized by genetic variability and phenotypic plasticity of pathogenicity‐related traits. Environmental microbiology. 16:2301-2315. https://doi.org/10.1111/1462-2920.12433 DOI: https://doi.org/10.1111/1462-2920.12433
  7. Bartoli C., Lamichhane J. R., Berge O., Varvaro L., Morris C. E., 2015. Mutability in Pseudomonas viridiflava as a programmed balance between antibiotic resistance and pathogenicity. Molecular Plant Pathology. 16:860-869. https://doi.org/10.1111/mpp.12243 DOI: https://doi.org/10.1111/mpp.12243
  8. Bastardo A., Balboa S., Romalde J. L., 2017. From the Gene Sequence to the Phylogeography through the Population Structure: The Cases of Yersinia ruckeri and Vibrio tapetis. Genetic Diversity. http://dx.doi.org/10.5772/67182 DOI: https://doi.org/10.5772/67182
  9. Berge O., Monteil C. L., Bartoli C., Chandeysson C., Guilbaud C., … Morris C. E., 2014. A User’s Guide to a Data Base of the Diversity of Pseudomonas syringae and Its Application to Classifying Strains in This Phylogenetic Complex. PLoS ONE 9: e105547. doi:10.1371/journal.pone.0105547 DOI: https://doi.org/10.1371/journal.pone.0105547
  10. Billing E., 1970. Pseudomonas viridiflava (Burkholder, 1930; Clara 1934). Journal of Applied Microbiology. 33:492-500. https://doi.org/10.1111/j.1365-2672.1970.tb02225.x DOI: https://doi.org/10.1111/j.1365-2672.1970.tb02225.x
  11. Biondi E., Galeone A., Kuzmanović N., Ardizzi S., Lucchese C., Bertaccini A., 2013. Pseudomonas syringae pv. actinidiae detection in kiwifruit plant tissue and bleeding sap. Annals of Applied Biology. 162:60-70. https://doi.org/10.1111/aab.12001 DOI: https://doi.org/10.1111/aab.12001
  12. Bophela K. N., Petersen Y., Bull C. T., Coutinho T. A., 2020. Identification of Pseudomonas isolates associated with bacterial canker of stone fruit trees in the Western Cape, South Africa. Plant disease. 104: 882-892. https://doi.org/10.1094/PDIS-05-19-1102-RE DOI: https://doi.org/10.1094/PDIS-05-19-1102-RE
  13. Borschinger B., Bartoli C., Chandeysson C., Guilbaud C., Parisi L., … Morris C.E., 2016. A set of PCRs for rapid identification and characterization of Pseudomonas syringae phylogroups. Journal of Applied Microbiology. 120:714-723. https://doi.org/10.1111/jam.13219 DOI: https://doi.org/10.1111/jam.13017
  14. Bull C. T., Koike S. T., 2015. Practical benefits of knowing the enemy: modern molecular tools for diagnosing the etiology of bacterial diseases and understanding the taxonomy and diversity of plant-pathogenic bacteria. Annual review of phytopathology. 53: 157-180. https://doi.org/10.1146/annurev-phyto-080614-120122 DOI: https://doi.org/10.1146/annurev-phyto-080614-120122
  15. Bustin S. A., Benes V., Garson J.A., Hellemans J., Huggett J., … Wittwer C. T., 2009. The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments. Clinical Chemistry. 55: 611-622. https://doi.org/10.1373/clinchem.2008.112797 DOI: https://doi.org/10.1373/clinchem.2008.112797
  16. Bustin S., Huggett J., 2017. qPCR primer design revisited. Biomolecular detection and quantification. 14:19-28. https://doi.org/10.1016/j.bdq.2017.11.001 DOI: https://doi.org/10.1016/j.bdq.2017.11.001
  17. Chapman J. R., Taylor R. K., Weir B. S., Romberg M. K., Vanneste J. L., … Alexander B. J. R. 2012. Phylogenetic relationships among global populations of Pseudomonas syringae pv. actinidiae. Phytopathology 102: 1034-1044. https://doi.org/10.1094/PHYTO-03-12-0064-R DOI: https://doi.org/10.1094/PHYTO-03-12-0064-R
  18. Conn K. E., Gubler W. D., Hasey J. K., 1993. Bacterial blight of kiwifruit in California. Plant disease. 77: 228-230. DOI: 10.1094/PD-77-0228. DOI: https://doi.org/10.1094/PD-77-0228
  19. Dillon M. M., Thakur S., Almeida R. N., Wang P. W., Weir B. S., Guttman D. S., 2019. Recombination of ecologically and evolutionarily significant loci maintains genetic cohesion in the Pseudomonas syringae species complex. Genome Biology. 20:1-28. https://doi.org/10.1186/s13059-018-1606-y DOI: https://doi.org/10.1186/s13059-018-1606-y
  20. Donati I., Cellini A., Sangiorgio D., Vanneste J. L., Scortichini M., … Spinelli F., 2020. Pseudomonas syringae pv. actinidiae: Ecology, infection dynamics and disease epidemiology. Microbial ecology. 80:81-102. https://doi.org/10.1007/s00248-019-01459-8 DOI: https://doi.org/10.1007/s00248-019-01459-8
  21. Dye D. W., Bradbury J., Goto M., Hayward A. C., Lelliott R. A., Schroth M. N., 1980. International standards for naming pathovars of phytopathogenic bacteria and a list of pathovar names and pathotype strains. Review of Plant pathology. 59:153-168.
  22. EPPO Bulletin 2021. Volume 51, Issue 3, PM 7/120 (2) Pseudomonas syringae pv. actinidiae. EPPO STANDARD – DIAGNOSTICS. DOI: 10.1111/epp.12782 DOI: https://doi.org/10.1111/epp.12782
  23. FAOSTAT, 2020. Food and Agriculture Organization of the United Nations. Available at: http://www.fao.org/faostat/en/#home. Accessed March 16, 2021.
  24. Firrao G., Torelli E., Polano C., Ferrante P., Ferrini F., ... Ermacora P., 2018. Genomic structural variations affecting virulence during clonal expansion of Pseudomonas syringae pv. actinidiae biovar 3 in Europe. Frontiers in Microbiology. 9:656. https://doi.org/10.3389/fmicb.2018.00656 DOI: https://doi.org/10.3389/fmicb.2018.00656
  25. Gallelli A., Talocci S., L'Aurora A., Loreti S., 2011. Detection of Pseudomonas syringae pv. actinidiae, causal agent of bacterial canker of kiwifruit, from symptomless fruits and twigs, and from pollen. Phytopathologia Mediterranea. 50: 462-472.
  26. Gardan L., Shafik H., Belouin S., Broch R., Grimont F., Grimont P. A. D., 1999. DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov.(ex Sutic and Dowson 1959). International Journal of Systematic and Evolutionary Microbiology. 49:469-478. https://doi.org/10.1099/00207713-49-2-469 DOI: https://doi.org/10.1099/00207713-49-2-469
  27. Gitaitis R., Sumner D., Gay D., Smittle D., McDonald G., … Hung Y., 1997. Bacterial streak and bulb rot of onion: I. A diagnostic medium for the semiselective isolation and enumeration of Pseudomonas viridiflava. Plant disease. 81:897-900. https://doi.org/10.1094/PDIS.1997.81.8.897 DOI: https://doi.org/10.1094/PDIS.1997.81.8.897
  28. Goss E. M., Kreitman M., Bergelson J., 2005. Genetic diversity, recombination and cryptic clades in Pseudomonas viridiflava infecting natural populations of Arabidopsis thaliana. Genetics 169:21-35. https://doi.org/10.1534/genetics.104.031351 DOI: https://doi.org/10.1534/genetics.104.031351
  29. Hirano S. S., Upper C. D., 2000. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae—a pathogen, ice nucleus, and epiphyte. Microbiology and molecular biology reviews. 64:624-653. DOI: 10.1128/MMBR.64.3.624-653.2000 DOI: https://doi.org/10.1128/MMBR.64.3.624-653.2000
  30. Hu F. P., Young J. M., Jones D. S., 1999. Evidence that bacterial blight of kiwifruit, caused by a Pseudomonas sp., was introduced into New Zealand from China. Journal of Phytopathology. 147: 89-97. DOI: https://doi.org/10.1111/j.1439-0434.1999.tb03813.x
  31. King E. O., Ward M. K., Raney D. E., 1954. Two simple media for the demonstration of pyocyanin and fluorescin. Journal of laboratory and clinical medicine. 44:301-307.
  32. Kumar S., Stecher G., Li M., Knyaz C., Tamura K., 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular biology and evolution. 35:1547-1549. https://doi.org/10.1093/molbev/msy096 DOI: https://doi.org/10.1093/molbev/msy096
  33. Lelliott R. A., Stead D. E., 1987. Methods for the diagnosis of bacterial diseases of plants. Methods in Plant Pathology. British Society for Plant Pathology, 162 pp.
  34. Lipps S. M., Samac D. A., 2022. Pseudomonas viridiflava: An internal outsider of the Pseudomonas syringae species complex. Molecular Plant Pathology. 23:3-15. https://doi.org/10.1111/mpp.13133 DOI: https://doi.org/10.1111/mpp.13133
  35. Liu P., Xue S., He R., Hu J., Wang X., … Zhu L., 2016. Pseudomonas syringae pv. Actinidiae isolated from non-kiwifruit plant species in China. European Journal of Plant Pathology. 145:743-754. DOI 10.1007/s10658-016-0863-4 DOI: https://doi.org/10.1007/s10658-016-0863-4
  36. Loreti S., Cunty A., Pucci N., Chabirand A., Stefani E., … Poliakoff F., 2018. Performance of diagnostic tests for the detection and identification of Pseudomonas syringae pv. actinidiae (Psa) from woody samples. European Journal of Plant Pathology. 152:657-676. https://doi.org/10.1007/s10658-018-1509-5 DOI: https://doi.org/10.1007/s10658-018-1509-5
  37. Luti S., Campigli S., Ranaldi F., Paoli P., Pazzagli L., Marchi G., 2021. Lscβ and lscγ, two novel levansucrases of Pseudomonas syringae pv. actinidiae biovar 3, the causal agent of bacterial canker of kiwifruit, show different enzymatic properties. International Journal of Biological Macromolecules. 179:279–291. https://doi.org/10.1016/j.ijbiomac.2021.02.189 DOI: https://doi.org/10.1016/j.ijbiomac.2021.02.189
  38. McCann H. C., Li L., Liu Y., Li D., Pan H., … Huang H., 2017. Origin and evolution of the kiwifruit canker pandemic. Genome biology and evolution. 9: 932-944. https://doi.org/10.1093/gbe/evx055 DOI: https://doi.org/10.1093/gbe/evx055
  39. Mohan S. K., Schaad N.W., 1987. An improved agar plating assay for detecting Pseudomonas syringae pv. syringae and P. s. pv. phaseolicola in contaminated bean seed. Phytopathology 77:1390-1395. DOI: https://doi.org/10.1094/Phyto-77-1390
  40. Mohr T.J., Liu H., Yan S., Morris C. E., Castillo J. A., … Vinatzer B. A., 2008. Naturally occurring nonpathogenic isolates of the plant pathogen Pseudomonas syringae lack a type III secretion system and effector gene orthologues. Journal of bacteriology. 190:2858-2870. https://doi.org/10.1128/JB.01757-07 DOI: https://doi.org/10.1128/JB.01757-07
  41. Moore E., Arnscheidt A., Krüger A., Strömpl C., Mau M., 2004. Simplified protocols for the preparation of genomic DNA from bacterial cultures. Molecular microbial ecology manual. 1: 3-18.
  42. Morris C. E., Kinkel L. L., Xiao K., Prior P., Sands D. C., 2007. Surprising niche for the plant pathogen Pseudomonas syringae. Infection, Genetics and Evolution. 7:84-92. https://doi.org/10.1016/j.meegid.2006.05.002 DOI: https://doi.org/10.1016/j.meegid.2006.05.002
  43. Morris C. E., Sands D. C., Vinatzer B. A., Glaux C., Guilbaud C., … Thompson B.M., 2008. The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. The ISME journal. 2:321-334. DOI: 10.1038/ismej.2007.113 DOI: https://doi.org/10.1038/ismej.2007.113
  44. Morris C. E., Sands D. C., Vanneste J. L., Montarry J., Oakley B., … Glaux C., 2010. Inferring the evolutionary history of the plant pathogen Pseudomonas syringae from its biogeography in headwaters of rivers in North America, Europe, and New Zealand. MBio. 1:00107–00110. https://doi.org/10.1128/mBio.00107-10 DOI: https://doi.org/10.1128/mBio.00107-10
  45. Morris C. E., Lamichhane J. R., Nikolić I., Stanković S., Moury B., 2019. The overlapping continuum of host range among strains in the Pseudomonas syringae complex. Phytopathology Research. 1:1-16. https://doi.org/10.1186/s42483-018-0010-6 DOI: https://doi.org/10.1186/s42483-018-0010-6
  46. Parisi L., Morgaint B., Blanco‐Garcia J., Guilbaud C., Chandeysson C., … Morris C. E., 2019. Bacteria from four phylogroups of the Pseudomonas syringae complex can cause bacterial canker of apricot. Plant Pathology. 68:1249-1258. https://doi.org/10.1111/ppa.13051 DOI: https://doi.org/10.1111/ppa.13051
  47. Parkinson N., Bryant R., Bew, J., Elphinstone J., 2011. Rapid phylogenetic identification of members of the Pseudomonas syringae species complex using the rpoD locus. Plant Pathology. 60:338-344. https://doi.org/10.1111/j.1365-3059.2010.02366.x DOI: https://doi.org/10.1111/j.1365-3059.2010.02366.x
  48. Petriccione M., Salzano A. M., Di Cecco I., Scaloni A., Scortichini M., 2014. Proteomic analysis of the Actinidia deliciosa leaf apoplast during biotrophic colonization by Pseudomonas syringae pv. actinidiae. Journal of proteomics. 101:43-62. https://doi.org/10.1016/j.jprot.2014.01.030 DOI: https://doi.org/10.1016/j.jprot.2014.01.030
  49. Renzi M., Copini P., Taddei A. R., Rossetti A., Gallipoli L., … Balestra G. M., 2012. Bacterial canker on kiwifruit in Italy: anatomical changes in the wood and in the primary infection sites. Phytopathology 102:827-840. https://doi.org/10.1094/PHYTO-02-12-0019-R DOI: https://doi.org/10.1094/PHYTO-02-12-0019-R
  50. Riffaud C. H., Morris C. E., 2002. Detection of Pseudomonas syringae pv. aptata in irrigation water retention basins by immunofluorescence colony-staining. European Journal of Plant Pathology. 108:539-545. https://doi.org/10.1023/A:1019919627886 DOI: https://doi.org/10.1023/A:1019919627886
  51. Sarkar S. F., Guttman D. S., 2004. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Applied and environmental microbiology. 70:1999-2012. DOI:10.1128/AEM.02553-07 DOI: https://doi.org/10.1128/AEM.70.4.1999-2012.2004
  52. Sawada H., Fujikawa T., 2019. Genetic diversity of Pseudomonas syringae pv. actinidiae, pathogen of kiwifruit bacterial canker. Plant Pathology. 68: 1235-1248. https://doi.org/10.1111/ppa.13040 DOI: https://doi.org/10.1111/ppa.13040
  53. Schaad N. W., Cheong S. S., Tamaki S., Hatziloukas E., Panopoulas N. J., 1995. A combined biological amplification (BIO-PCR) technique to detect Pseudomonas syringae pv. phaseolicola in bean seed extracts. Phytopathology 85:243-248. DOI: 10.1094/Phyto-85-243 DOI: https://doi.org/10.1094/Phyto-85-243
  54. Schaad N. W., Berthier-Schaad Y., Sechler A., Knorr D., 1999. Detection of Clavibacter michiganensis subsp. sepedonicus in potato tubers by BIO-PCR and an automated real-time fluorescence detection system. Plant disease. 83:1095-1100. DOI: 10.1094/PDIS.1999.83.12.1095 DOI: https://doi.org/10.1094/PDIS.1999.83.12.1095
  55. Schaad N. W., Jones J. B., Chun W., 2001. Laboratory guide for the identification of plant pathogenic bacteria. 3th ed. American Phytopathological Society (APS Press), USA, 373 pp.
  56. Serizawa S., Ichikawa T., Takikawa Y., Tsuyumu S., Goto M., 1989. Occurrence of bacterial canker of kiwifruit in japan. Japanese Journal of Phytopathology 55:427-436 (in Japanese) https://doi.org/10.3186/jjphytopath.55.427 DOI: https://doi.org/10.3186/jjphytopath.55.427
  57. Serizawa S., Ichikawa T., 1993. Epidemiology of bacterial canker of kiwifruit. 2. The most suitable times and environments for infection on new canes. Annals of the Phytopathological Society of Japan. 59:460-468 (in Japanese). DOI 10.3186/jjphytopath.59.460 DOI: https://doi.org/10.3186/jjphytopath.59.460
  58. Straub C., Colombi E., Li L., Huang H., Templeton M. D., … Rainey P. B. , 2018. The ecological genetics of Pseudomonas syringae from kiwifruit leaves. Environmental microbiology. 20:2066-2084. https://doi.org/10.1111/1462-2920.14092 DOI: https://doi.org/10.1111/1462-2920.14092
  59. Tyson J. L., Rees-George J., Curtis C. L., Manning M. A., Fullerton R. A., 2012. Survival of Pseudomonas syringae pv actinidiae on the orchard floor over winter. New Zealand Plant Protection. 65:25-28. https://doi.org/10.30843/nzpp.2012.65.5420 DOI: https://doi.org/10.30843/nzpp.2012.65.5420
  60. Tyson J. L., Horner I.J., Curtis C. L., Blackmore A., Manning M. A., 2015. Influence of leaf age on infection of Actinidia species by Pseudomonas syringae pv actinidiae. New Zealand Plant Protection. 68:328-331. https://doi.org/10.30843/nzpp.2015.68.5829 DOI: https://doi.org/10.30843/nzpp.2015.68.5829
  61. Vanneste J. L., Yu J., Cornish D. A., Max S., Clark G., 2011. Presence of Pseudomonas syringae pv actinidiae the causal agent of bacterial canker of kiwifruit on symptomatic and asymptomatic tissues of kiwifruit. New Zealand Plant Protection. 64:241-245. https://doi.org/10.30843/nzpp.2011.64.5948 DOI: https://doi.org/10.30843/nzpp.2011.64.5948
  62. Vanneste J. L., 2017. The scientific, economic, and social impacts of the New Zealand outbreak of bacterial canker of kiwifruit (Pseudomonas syringae pv. actinidiae). Annual Review of Phytopathology. 55:377-399. https://doi.org/10.1146/annurev-phyto-080516-035530 DOI: https://doi.org/10.1146/annurev-phyto-080516-035530
  63. Visnovsky S. B., Marroni M. V., Pushparajah S., Everett K. R., Taylor, R. K., … Pitman A. R., 2019. Using multilocus sequence analysis to distinguish pathogenic from saprotrophic strains of Pseudomonas from stone fruit and kiwifruit. European Journal of Plant Pathology. 155:643-658. https://doi.org/10.1007/s10658-019-01799-8 DOI: https://doi.org/10.1007/s10658-019-01799-8
  64. Wilkie J. P., Dye D. W., Watson D. R. W., 1973. Further hosts of Pseudomonas viridiflava. New Zealand Journal of Agricultural Research. 16:315-323. https://doi.org/10.1080/00288233.1973.10421110 DOI: https://doi.org/10.1080/00288233.1973.10421110
  65. Young J. M., Cheesmur G. J., Welham F. V., Henshall W. R., 1988. Bacterial blight of kiwifruit. Annals of applied Biology. 112:91-105. https://doi.org/10.1111/j.1744-7348.1988.tb02044.x DOI: https://doi.org/10.1111/j.1744-7348.1988.tb02044.x
  66. Young J. M., Gardan L., Ren X. Z., Hu F. P., 1997. Genomic and phenotypic characterization of the bacterium causing blight of kiwifruit in New Zealand. Plant Pathology. 46:857-864. https://doi.org/10.1046/j.1365-3059.1997.d01-72.x DOI: https://doi.org/10.1046/j.1365-3059.1997.d01-72.x
  67. Zar J. H., 1999. Biostatistical Analysis, 4th ed. Prentice-Hall International, London, UK, 663pp.

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