A new inclusive MLVA assay to investigate genetic variability of Xylella fastidiosa with a specific focus on the Apulian outbreak in Italy

EFSA. Update of the Xylella spp. host plant database. EFSA J. 16, 5408. https://doi.org/10.2903/j.efsa.2018.5408 (2018).

Article  Google Scholar 

Almeida, R. P. P. & Nunney, L. How do plant diseases caused by Xylella fastidiosaXylella fastidiosa emerge?. Plant Dis. https://doi.org/10.1094/PDIS-02-15-0159-FE (2015).

Article  PubMed  Google Scholar 

Hopkins, D. L. Xylella fastidiosa: Xylem-limited bacterial pathogen of plants. Plant Dis. https://doi.org/10.1094/PDIS-02-15-0159-FE (1989).

Article  Google Scholar 

Baldi, P. & La Porta, N. Xylella fastidiosa: Host range and advance in molecular identification techniques. Front. Plant Sci. 8, 944. https://doi.org/10.3389/fpls.2017.00944 (2017).

Article  PubMed  PubMed Central  Google Scholar 

Purcell, A. Paradigms: Examples from the bacterium Xylella fastidiosa. Annu. Rev. Phytopathol. 51, 339–356. https://doi.org/10.1146/annurev-phyto-082712-102325 (2013).

CAS  Article  PubMed  Google Scholar 

Almeida, R. P. P. et al. Genetic structure and biology of Xylella fastidiosa strains causing disease in citrus and coffee in Brazil. Appl. Environ. Microbiol. 74, 3690–3701. https://doi.org/10.1128/AEM.02388-07 (2008).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Harris, J. L. & Balci, Y. Population structure of the bacterial pathogen Xylella fastidiosa among street trees in Washington DC. PLoS One 10, e0121297. https://doi.org/10.1371/journal.pone.0121297 (2015).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Nunney, L. et al. Recent evolutionary radiation and host plant specialization in the Xylella fastidiosa subspecies native to the United States. Appl. Environ. Microbiol. 79, 2189–2189. https://doi.org/10.1128/AEM.03208-12 (2013).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Schaad, N. W., Postnikova, E., Lacy, G., Fatmi, M. & Chang, C. J. Xylella fastidiosa subspecies: X. fastidiosa subsp. fastidiosa subsp. nov., X. fastidiosa subsp. multiplex subsp. nov., and X. fastidiosa subsp. pauca subsp. nov. Syst Appl Microbiol 27, 290–300. https://doi.org/10.1078/0723-2020-00263 (2004).

CAS  Article  PubMed  Google Scholar 

Denancé, N. et al. Several subspecies and sequence types are associated with the emergence of Xylella fastidiosa in natural settings in France. Plant Pathol. 66, 1054–1064. https://doi.org/10.1111/ppa.12695 (2017).

CAS  Article  Google Scholar 

Nunney, L., Schuenzel, E., Scally, M., Bromley, R. & Stouthamer, R. Large-scale intersubspecific recombination in the plant-pathogenic bacterium Xylella fastidiosa is associated with the host shift to mulberry. Appl. Environ. Microbiol. 80, 3025–3033. https://doi.org/10.1128/AEM.04112-13 (2014).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Randall, J. J. et al. Genetic analysis of a novel Xylella fastidiosa subspecies found in the southwestern United States. Appl. Environ. Microbiol. 75, 5631–5638. https://doi.org/10.1128/AEM.00609-09 (2009).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Su, C. et al. 2013 Pierce’s disease of grapevines in Taiwan: Isolation, cultivation and pathogenicity of Xylella fastidiosa. J. Phytopathol. 161, 389–396. https://doi.org/10.1111/jph.12075

CAS  Article  Google Scholar 

Saponari, M., Boscia, D., Nigro, F. & Martelli, G. Identification of DNA sequences related to Xylella fastidiosa in oleander, almond and olive trees exhibiting leaf scorch symptoms in Apulia (southern Italy). J. Plant Pathol. 95, 668–668 (2013).

Google Scholar 

Amanifar, N., Taghavi, M., Izadpanah, K. & Babaei, G. Isolation and pathogenicity of Xylella fastidiosa from grapevine and almond in Iran. Phytopathol. Mediterr. https://doi.org/10.14601/Phytopathol_Mediterr-12647 (2014).

Article  Google Scholar 

Olmo, D. et al. First detection of Prunus avium infecting cherry (Prunus avium) and Polygala myrtifolia plants, in Mallorca Island, Spain. Plant Dis. 101, 1820–1820. https://doi.org/10.1094/PDI5-04-17-0590-PDN (2017).

Article  Google Scholar 

EPPO. First report of Xylella fastidiosa subsp. multiplex in Portugal. Report, European Plant Protection Organization (2019).

EPPO. First report of Xylella fastidiosa in Israel. Report, European Plant Protection Organization (2019).

Mehta, A., Pereira Leite, R. & Bomura Rosato, Y. Assessment of the genetic diversity of Xylella fastidiosa isolated from citrus in Brazil by PCR–RFLP of the 16s r DNA and 16 S-23 S intergenic spacer and rep-PCR fingerprinting. Antonie Van Leeuwenhoek 79, 53–59. https://doi.org/10.1023/A:1010219811555 (2001).

Article  Google Scholar 

Lacava, P., Araújo, W., Maccheroni, W. Jr. & Azevedo, J. RAPD profile and antibiotic susceptibility of Xylella fastidiosa, causal agent of citrus variegated chlorosis. Lett. Appl. Microbiol. 33, 302–306. https://doi.org/10.1046/j.1472-765X.2001.01000.x (2001).

CAS  Article  PubMed  Google Scholar 

Kishi, L., Wickert, E. & de Macedo Lemos, E. Evaluation of Xylella fastidiosa genetic diversity by fAFPL markers. Rev. Bras. Fruticult. 30, 202–208, https://doi.org/10.1590/S0100-29452008000100037 (2008).

Article  Google Scholar 

Nunney, L., Ortiz, B., Russell, S., Sanchez, R. & Stouthamer, R. The complex biogeography of the plant pathogen Xylella fastidiosa: Genetic evidence of introductions and subspecific introgression in Central America. Plos One. https://doi.org/10.1371/journal.pone.0112463 (2014).

Article  PubMed  PubMed Central  Google Scholar 

Yuan, X. et al. Multilocus sequence typing of Xylella fastidiosa causing Pierce’s Disease and oleander leaf scorch in the United States. Phytopathology https://doi.org/10.1094/PHYTO-100-6-0601 (2010).

Article  PubMed  Google Scholar 

Elbaino, T. et al. Multilocus sequence typing of Xylella fastidiosa, isolated from olive affected by ‘ Olive Quick Decline Syndrome’ in Italy. Phytopathol. Mediterr. 53, 533–542. https://doi.org/10.14601/Phytopathol_Mediterr-15000 (2014).

Google Scholar 

Loconsole, G. et al. Intercepted isolates of Xylella fastidiosa in Europe reveal novel genetic diversity. Eur. J. Plant Pathol. 146, 85–94. https://doi.org/10.1007/s10658-016-0894-x (2016).

CAS  Article  Google Scholar 

Coletta-Filho, H. D., Francisco, C. S., Lopes, J. R. S., Muller, C. & Almeida, R. P. P. Homologous recombination and Xylella fastidiosa host-pathogen associations in South America. Phytopathology 107, 305–312. https://doi.org/10.1094/PHYTO-09-16-0321-R (2017).

Article  PubMed  Google Scholar 

Marcelletti, S. & Scortichini, M. Genome-wide comparison and taxonomic relatedness of multiple Xylella fastidiosa strains reveal the occurrence of three subspecies and a new xylella species. Arch. Microbiol. 198, 803–812. https://doi.org/10.1007/s00203-016-1245-1 (2016).

CAS  Article  PubMed  Google Scholar 

Li, W., Raoult, D. & Fournier, P. Bacterial strain typing in the genomic era. Fems Microbiol. Rev. 33, 892–916. https://doi.org/10.1111/j.1574-6976.2009.00182.x (2009).

CAS  Article  PubMed  Google Scholar 

Kremer, K. et al. Comparison of methods based on different molecular epidemiological markers for typing of mycobacterium tuberculosis complex strains: Interlaboratory study of discriminatory power and reproducibility. J. Clin. Microbiol.J. Clin. Microbiol.37, 2607–2618 (1999).

CAS  Article  Google Scholar 

van Belkum, A. Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA). Fems Immunol. Med. Microbiol. 49, 22–27. https://doi.org/10.1111/j.1574-695X.2006.00173.x (2007).

CAS  Article  PubMed  Google Scholar 

Lindstedt, B. Multiple-locus variable number tandem repeats analysis for genetic fingerprinting of pathogenic bacteria. Electrophoresis 26, 2567–2582. https://doi.org/10.1002/elps.200500096 (2005).

CAS  Article  PubMed  Google Scholar 

Coletta-Filho, H. D. et al. Differentiation of strains of Xylella fastidiosa by a variable number of tandem repeat analysis. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.67.9.4091-4095.2001 (2001).

Article  PubMed  PubMed Central  Google Scholar 

Lin, H. et al. Multilocus simple sequence repeat markers for differentiating strains and evaluating genetic diversity of Xylella fastidiosa. Appl. Environ. Microbiol. 71, 4888–4892. https://doi.org/10.1128/AEM.71.8.4888-4892.2005 (2005).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Montero-Astúa, M. et al. Isolation and molecular characterization of Xylella fastidiosa from coffee plants in Costa Rica. J. Microbiol. https://doi.org/10.1007/s12275-008-0072-8 (2008).

Article  PubMed  Google Scholar 

Coletta-Filho, H. D., Francisco, C. S. & Almeida, R. P. P. Temporal and spatial scaling of the genetic structure of a vector-borne plant pathogen. Phytopathology. https://doi.org/10.1094/PHYTO-06-13-0154-R (2014).

Article  PubMed  Google Scholar 

Lin, H., Islam, M., Cabrera-La Rosa, J., Civerolo, E. & Groves, R. Population structure of Xylella fastidiosa associated with almond leaf scorch disease in the San Joaquin Valley of California. Phytopathology 105, 825–832. https://doi.org/10.1094/PHYTO-09-14-0254-R (2015).

Article  Google Scholar 

Montes-Borrego, M., Lopes, J. R. S., Jiménez-Díaz, R. M. & Landa, B. B. Combined use of a new snp-based assay and multilocus SSR markers to assess genetic diversity of Xylella fastidiosa subsp. pauca infecting citrus and coffee plants. Int. Microbiol. https://doi.org/10.2436/20.1501.01.230 (2015).

Article  PubMed  Google Scholar 

Francisco, C. S., Ceresini, P. C., Almeida, R. P. P. & Coletta-Filho, H. D. Spatial genetic structure of coffee-associated Xylella fastidiosa populations indicates that cross infection does not occur with sympatric citrus orchards. Phytopathology 107, 395–402. https://doi.org/10.1094/PHYTO-08-16-0300-R (2017).

CAS  Article  PubMed  Google Scholar 

Cariddi, C. et al. Isolation of a Xylella fastidiosa strain infecting olive and oleander in Apulia Italy. J. Plant Pathol. https://doi.org/10.4454/JPP.V96I2.024 (2014).

Article  Google Scholar 

Saponari, M. et al. Isolation and pathogenicity of Xylella fastidiosa associated to the olive quick decline syndrome in southern Italy. Sci. Rep.Sci. Rep.. https://doi.org/10.1038/s41598-017-17957-z (2017).

Article  PubMed  PubMed Central  Google Scholar 

Bergsma-Vlami, M. et al. Assessment of the genetic diversity of Xylella fastidiosa in imported ornamental coffea arabica plants. Plant Pathol. 66, 1065–1074. https://doi.org/10.1111/ppa.12696 (2017).

CAS  Article  Google Scholar 

Martelli, G., Boscia, D., Porcelli, F. & Saponari, M. The olive quick decline syndrome in south-east Italy: A threatening phytosanitary emergency. Eur. J. Plant Pathol.144, 235–243. https://doi.org/10.1007/s10658-015-0784-7 (2016).

Article  Google Scholar 

Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580. https://doi.org/10.1093/nar/27.2.573 (1999).

CAS  Article  PubMed  PubMed Central  Google Scholar 

EPPO. Pm 7/24 (4) Pm 7/24 (4) Xylella fastidiosa. EPPO Bull.49, 175–227. https://doi.org/10.1111/epp.12575 (2019).

Article  Google Scholar 

Maiden, M. et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95, 3140–3145. https://doi.org/10.1073/pnas.95.6.3140 (1998).

ADS  CAS  Article  PubMed  Google Scholar 

Safady, N., Lopes, J., Francisco, C. & Della Coletta, H. Distribution and genetic diversity of Xylella fastidiosa subsp. pauca associated with olive quick syndrome symptoms in southeastern Brazil. Phytopathology 109, 257–264. https://doi.org/10.1094/PHYTO-07-18-0273-FI (2019).

Article  PubMed  Google Scholar 

EFSA. Statement on diversity of Xylella fastidiosa subsp. pauca in Apulia. EFSA J. 14, 4542. https://doi.org/10.2903/j.efsa.2016.4542 (2016).

Article  Google Scholar 

Lin, H. et al. Genetic variation of Xylella fastidiosa associated with grapevines in two major viticultural regions in the united states: California and Texas. J. Plant Pathol.95, 329–337 (2013).

Google Scholar 

Bruvo, R., Michiels, N., D’Souza, T. & Schulenburg, H. A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol. Ecol. 13, 2101–2106. https://doi.org/10.1111/j.1365-294X.2004.02209.x (2004).

CAS  Article  PubMed  Google Scholar 

Clark, L. & Jasieniuk, M. POLYSAT: An R package for polyploid microsatellite analysis. Mol. Ecol. Resour. 11, 562–566. https://doi.org/10.1111/j.1755-0998.2011.02985.x (2011).

Article  PubMed  Google Scholar 

Kamvar, Z. N., Tabima, J. F. & Grunwald, N. J. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 1, 1–14. https://doi.org/10.7717/peerj.281 (2014).

Article  Google Scholar 

Meirmans, P. & Van Tienderen, P. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4, 792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x (2004).

Article  Google Scholar 

Francisco, A., Bugalho, M., Ramirez, M. & Carrico, J. Global optimal e BURST analysis of multilocus typing data using a graphic matroid approach. BMC Bioinf. 10, https://doi.org/10.1186/1471-2105-10-152 (2009).

Article  Google Scholar 

Feil, E., Li, B., Aanensen, D., Hanage, W. & Spratt, B. e BURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 186, 1518–1530. https://doi.org/10.1128/JB.186.5.1518-1530.2004 (2004).

CAS  Article  PubMed  PubMed Central  Google Scholar 

code by Richard A. Becker, O. S., version by Ray Brownrigg. Enhancements by Thomas P Minka, A. R. W. R. & Deckmyn., A. maps: Draw Geographical Maps (2018). R package version 3.3.0.

Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Spring, New York, 2016).

Google Scholar 

Harper, S., Ward, L. & Clover, G. Development of LAMP and real-time PCR methods for the rapid detection of Xylella fastidiosa for quarantine and field applications. Phytopathology 100, 1282–1288. https://doi.org/10.1094/PHYTO-06-10-0168 (2010).

CAS  Article  PubMed  Google Scholar 

Kassambara, A. & Mundt, F. Factoextra: Extract and visualize the results of multivariate data analyses [R package Factoextra version 1.0.5] (2016).

Nascimento, M. et al. Phyloviz 2.0: Providing scalable data integration and visualization for multiple phylogenetic inference methods. Bioinformatics 33, 128–129, https://doi.org/10.1093/bioinformatics/btw582 (2017).

CAS  Article  PubMed  Google Scholar