Short Communication

Complete Genome Sequencing of Three Clade-1 Xanthomonads Reveals Genetic Determinants for a Lateral Flagellin and the Biosynthesis of Coronatine-Like Molecules in Xanthomonas

Earth & Life Institute, UCLouvain, Louvain-la-Neuve, Belgium

Plant Health Institute of Montpellier (PHIM), University of Montpellier, Cirad, INRAE, Institut Agro, IRD, Montpellier, France

Search for more papers by this author

Daiva Burokienė

Nature Research Centre, Institute of Botany, Laboratory of Plant Pathology, Vilnius, Lithuania

Search for more papers by this author

Ildikó Katalin Nagy

Enviroinvest Corp., Pécs, Hungary

Search for more papers by this author

Marion Fischer-Le Saux

Univ. Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, France

Search for more papers by this author

Perrine Portier

Univ. Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, France

Search for more papers by this author

Alexis Dereeper

Plant Health Institute of Montpellier (PHIM), University of Montpellier, Cirad, INRAE, Institut Agro, IRD, Montpellier, France

Search for more papers by this author

Sébastien Cunnac

Plant Health Institute of Montpellier (PHIM), University of Montpellier, Cirad, INRAE, Institut Agro, IRD, Montpellier, France

Search for more papers by this author

Veronica Roman-Reyna

https://orcid.org/0000-0003-0072-8096

Department of Plant Pathology, The Ohio State University, Columbus, OH 43210, U.S.A.

Infectious Disease Institute, The Ohio State University, Columbus, OH 43210, U.S.A.

Search for more papers by this author

Jonathan M. Jacobs

https://orcid.org/0000-0002-1553-2013

Department of Plant Pathology, The Ohio State University, Columbus, OH 43210, U.S.A.

Infectious Disease Institute, The Ohio State University, Columbus, OH 43210, U.S.A.

Search for more papers by this author

Claude Bragard

Earth & Life Institute, UCLouvain, Louvain-la-Neuve, Belgium

Search for more papers by this author

, and

Ralf Koebnik

^†Corresponding author: R. Koebnik;

E-mail Address: [email protected]

https://orcid.org/0000-0002-4419-0542

Plant Health Institute of Montpellier (PHIM), University of Montpellier, Cirad, INRAE, Institut Agro, IRD, Montpellier, France

Search for more papers by this author

Affiliations

Authors and Affiliations

Chloé Peduzzi¹
Angeliki Sagia¹²
Daiva Burokienė³
Ildikó Katalin Nagy⁴
Marion Fischer-Le Saux⁵
Perrine Portier⁵
Alexis Dereeper²
Sébastien Cunnac²
Veronica Roman-Reyna⁶⁷
Jonathan M. Jacobs⁶⁷
Claude Bragard¹
Ralf Koebnik²^†

¹Earth & Life Institute, UCLouvain, Louvain-la-Neuve, Belgium
²Plant Health Institute of Montpellier (PHIM), University of Montpellier, Cirad, INRAE, Institut Agro, IRD, Montpellier, France
³Nature Research Centre, Institute of Botany, Laboratory of Plant Pathology, Vilnius, Lithuania
⁴Enviroinvest Corp., Pécs, Hungary
⁵Univ. Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, France
⁶Department of Plant Pathology, The Ohio State University, Columbus, OH 43210, U.S.A.
⁷Infectious Disease Institute, The Ohio State University, Columbus, OH 43210, U.S.A.

Published Online:26 Aug 2023https://doi.org/10.1094/PHYTO-10-22-0373-SC

View article

Abstract

Evolutionarily, early-branching xanthomonads, also referred to as clade-1 xanthomonads, include major plant pathogens, most of which colonize monocotyledonous plants. Seven species have been validly described, among them the two sugarcane pathogens Xanthomonas albilineans and Xanthomonas sacchari, as well as Xanthomonas translucens, which infects small-grain cereals and diverse grasses but also asparagus and pistachio trees. Single-gene sequencing and genomic approaches have indicated that this clade likely contains more, yet-undescribed species. In this study, we sequenced representative strains of three novel species using long-read sequencing technology. Xanthomonas campestris pv. phormiicola strain CFBP 8444 causes bacterial streak on New Zealand flax, another monocotyledonous plant. Xanthomonas sp. strain CFBP 8443 has been isolated from common bean, and Xanthomonas sp. strain CFBP 8445 originated from banana. Complete assemblies of the chromosomes confirmed their unique phylogenetic position within clade 1 of Xanthomonas. Genome mining revealed novel genetic features, hitherto undescribed in other members of the Xanthomonas genus. In strain CFBP 8444, we identified genes related to the synthesis of coronatine-like compounds, a phytotoxin produced by several pseudomonads, which raises interesting questions about the evolution and pathogenicity of this pathogen. Furthermore, strain CFBP 8444 was found to contain a second, atypical flagellar gene cluster in addition to the canonical flagellar gene cluster. Overall, this research represents an important step toward better understanding the evolutionary history and biology of early-branching xanthomonads.

Literature Cited

Aritua, V., Harrison, J., Sapp, M., Buruchara, R., Smith, J., and Studholme, D. J. 2015. Genome sequencing reveals a new lineage associated with lablab bean and genetic exchange between Xanthomonas axonopodis pv. phaseoli and Xanthomonas fuscans subsp. fuscans. Front. Microbiol. 6:1080. https://doi.org/10.3389/fmicb.2015.01080 Crossref, Medline, ISI, Google Scholar
Bansal, K., Kaur, A., Midha, S., Kumar, S., Korpole, S., and Patil, P. B. 2021. Xanthomonas sontii sp. nov., a non-pathogenic bacterium isolated from healthy basmati rice (Oryza sativa) seeds from India. Antonie Van Leeuwenhoek 114:1935-1947. https://doi.org/10.1007/s10482-021-01652-1 Crossref, Medline, Google Scholar
Bansal, K., Kumar, S., and Patil, P. B. 2020. Phylogenomic insights into diversity and evolution of nonpathogenic Xanthomonas strains associated with citrus. mSphere 5:e00087-20. https://doi.org/10.1128/mSphere.00087-20 Crossref, Medline, ISI, Google Scholar
Bender, C., Palmer, D., Peñaloza-Vázquez, A., Rangaswamy, V., and Ullrich, M. 1996. Biosynthesis of coronatine, a thermoregulated phytotoxin produced by the phytopathogen Pseudomonas syringae. Arch. Microbiol. 166:71-75. https://doi.org/10.1007/s002030050358 Crossref, ISI, Google Scholar
Bender, C. L., Alarcón-Chaidez, F., and Gross, D. C. 1999. Pseudomonas syringae phytotoxins: Mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 63:266-292. https://doi.org/10.1128/MMBR.63.2.266-292.1999 Crossref, Medline, ISI, Google Scholar
Bown, L., Li, Y., Berrué, F., Verhoeven, J. T. P., Dufour, S. C., and Bignell, D. R. D. 2017. Coronafacoyl phytotoxin biosynthesis and evolution in the common scab pathogen Streptomyces scabiei. Appl. Environ. Microbiol. 83:e01169-17. https://doi.org/10.1128/AEM.01169-17 Crossref, Medline, ISI, Google Scholar
Canals, R., Altarriba, M., Vilches, S., Horsburgh, G., Shaw, J. G., Tomás, J. M., and Merino, S. 2006. Analysis of the lateral flagellar gene system of Aeromonas hydrophila AH-3. J. Bacteriol. 188:852-862. https://doi.org/10.1128/JB.188.3.852-862.2006 Crossref, Medline, ISI, Google Scholar
Darrasse, A., Carrère, S., Barbe, V., Boureau, T., Arrieta-Ortiz, M. L., Bonneau, S., Briand, M., Brin, C., Cociancich, S., Durand, K., Fouteau, S., Gagnevin, L., Guérin, F., Guy, E., Indiana, A., Koebnik, R., Lauber, E., Munoz, A., Noël, L. D., Pieretti, I., Poussier, S., Pruvost, O., Robène-Soustrade, I., Rott, P., Royer, M., Serres-Giardi, L., Szurek, B., van Sluys, M. A., Verdier, V., Vernière, C., Arlat, M., Manceau, C., and Jacques, M. A. 2013. Genome sequence of Xanthomonas fuscans subsp. fuscans strain 4834-R reveals that flagellar motility is not a general feature of xanthomonads. BMC Genomics 14:761. https://doi.org/10.1186/1471-2164-14-761 Crossref, Medline, ISI, Google Scholar
Dia, N. C., Van Vaerenbergh, J., Van Malderghem, C., Blom, J., Smits, T. H. M., Cottyn, B., and Pothier, J. F. 2021. Xanthomonas hydrangeae sp. nov., a novel plant pathogen isolated from Hydrangea arborescens. Int. J. Syst. Evol. Microbiol. 71. https://doi.org/10.1099/ijsem.0.005163 Crossref, Medline, ISI, Google Scholar
Dowson, W. J. 1939. On the systematic position and generic names of the Gram-negative bacterial plant pathogens. Zentralbl. Bakteriol. Parasitenk. Infektionskr. Hyg. Abt. II (1939) 100:177-193. Google Scholar
Ferreira-Tonin, M., Rodrigues-Neto, J., Harakava, R., and Destéfano, S. A. 2012. Phylogenetic analysis of Xanthomonas based on partial rpoB gene sequences and species differentiation by PCR-RFLP. Int. J. Syst. Evol. Microbiol. 62:1419-1424. https://doi.org/10.1099/ijs.0.028977-0 Crossref, Medline, ISI, Google Scholar
Fyans, J. K., Altowairish, M. S., Li, Y., and Bignell, D. R. 2015. Characterization of the coronatine-like phytotoxins produced by the common scab pathogen Streptomyces scabies. Mol. Plant-Microbe Interact. 28:443-454. https://doi.org/10.1094/MPMI-09-14-0255-R Link, ISI, Google Scholar
Gavín, R., Rabaan, A. A., Merino, S., Tomás, J. M., Gryllos, I., and Shaw, J. G. 2002. Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Mol. Microbiol. 43:383-397. https://doi.org/10.1046/j.1365-2958.2002.02750.x Crossref, Medline, ISI, Google Scholar
Giblot-Ducray, D., Marefat, A., Gillings, M. R., Parkinson, N. M., Bowman, J. P., Ophel-Keller, K., Taylor, C., Facelli, E., and Scott, E. S. 2009. Proposal of Xanthomonas translucens pv. pistaciae pv. nov., pathogenic to pistachio (Pistacia vera). Syst. Appl. Microbiol. 32:549-557. https://doi.org/10.1016/j.syapm.2009.08.001 Crossref, Medline, ISI, Google Scholar
Gilchrist, C. L. M., and Chooi, Y. H. 2021. Clinker & clustermap.js: Automatic generation of gene cluster comparison figures. Bioinformatics 37:2473-2475. https://doi.org/10.1093/bioinformatics/btab007 Crossref, Medline, ISI, Google Scholar
Gimenez-Ibanez, S., Boter, M., and Solano, R. 2015. Novel players fine-tune plant trade-offs. Essays Biochem. 58:83-100. https://doi.org/10.1042/bse0580083 Crossref, Medline, ISI, Google Scholar
Goettelmann, F., Roman-Reyna, V., Cunnac, S., Jacobs, J. M., Bragard, C., Studer, B., Koebnik, R., and Kölliker, R. 2022. Complete genome assemblies of all Xanthomonas translucens pathotype strains reveal three genetically distinct clades. Front. Microbiol. 12:817815. https://doi.org/10.3389/fmicb.2021.817815 Crossref, Medline, ISI, Google Scholar
Gonçalves, E. R., and Rosato, Y. B. 2002. Phylogenetic analysis of Xanthomonas species based upon 16S-23S rDNA intergenic spacer sequences. Int. J. Syst. Evol. Microbiol. 52:355-361. https://doi.org/10.1099/00207713-52-2-355 Crossref, Medline, ISI, Google Scholar
Goris, J., Konstantinidis, K. T., Klappenbach, J. A., Coenye, T., Vandamme, P., and Tiedje, J. M. 2007. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol. 57:81-91. https://doi.org/10.1099/ijs.0.64483-0 Crossref, Medline, ISI, Google Scholar
Gowda, K., Ping, D., Mani, M., and Kuehn, S. 2022. Genomic structure predicts metabolite dynamics in microbial communities. Cell 185:530-546.e25. https://doi.org/10.1016/j.cell.2021.12.036 Crossref, Medline, ISI, Google Scholar
Hauben, L., Vauterin, L., Swings, J., and Moore, E. R. 1997. Comparison of 16S ribosomal DNA sequences of all Xanthomonas species. Int. J. Syst. Bacteriol. 47:328-335. https://doi.org/10.1099/00207713-47-2-328 Crossref, Medline, Google Scholar
Jacobs, J. M., Pesce, C., Lefeuvre, P., and Koebnik, R. 2015. Comparative genomics of a cannabis pathogen reveals insight into the evolution of pathogenicity in Xanthomonas. Front. Plant Sci. 6:431. https://doi.org/10.3389/fpls.2015.00431 Crossref, Medline, ISI, Google Scholar
Jacques, M. A., Arlat, M., Boulanger, A., Boureau, T., Carrère, S., Cesbron, S., Chen, N. W., Cociancich, S., Darrasse, A., Denancé, N., Saux, M. F.-L., Gagnevin, L., Koebnik, R., Lauber, E., Noëll, L. D., Pieretti, I., Portier, P., Pruvost, O., Rieux, A., Robène, I., Royer, M., Szurek, B., Verdier, V., and Vernière, C. 2016. Using ecology, physiology, and genomics to understand host specificity in Xanthomonas. Annu. Rev. Phytopathol. 54:163-187. https://doi.org/10.1146/annurev-phyto-080615-100147 Crossref, Medline, ISI, Google Scholar
Jain, C., Rodriguez, R. L., Phillippy, A. M., Konstantinidis, K. T., and Aluru, S. 2018. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 9:5114. https://doi.org/10.1038/s41467-018-07641-9 Crossref, Medline, ISI, Google Scholar
Khenfous-Djebari, B., Kerkoud, M., Fischer-Le Saux, M., Benhassine, T., Bouznad, Z., Koebnik, R., and Bragard, C. 2019. Isolation of atypical wheat-associated xanthomonads in Algeria. Phytopathologia Mediterranea 58:497-506. ISI, Google Scholar
Kobayashi, M., Konishi, H., Maruyama, Y., Murata, K., and Hashimoto, W. 2016. Lateral-typed flagellin responsible for formation of a polar flagellum but not of lateral flagella in Sphingomonas sp. strain A1. Microbiology (Reading) 162:2042-2052. https://doi.org/10.1099/mic.0.000385 Crossref, Medline, ISI, Google Scholar
Koebnik, R., Burokiene, D., Bragard, C., Chang, C., Saux, M. F.-L., Kölliker, R., Lang, J. M., Leach, J. E., Luna, E. K., Portier, P., Sagia, A., Ziegle, J., Cohen, S. P., and Jacobs, J. M. 2021. The complete genome sequence of Xanthomonas theicola, the causal agent of canker on tea plants, reveals novel secretion systems in clade-1 xanthomonads. Phytopathology 111:611-616. https://doi.org/10.1094/PHYTO-07-20-0273-SC Link, ISI, Google Scholar
Kolmogorov, M., Yuan, J., Lin, Y., and Pevzner, P. A. 2019 Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 37:540-546. https://doi.org/10.1038/s41587-019-0072-8 Crossref, Medline, ISI, Google Scholar
Kühn, M. J., Edelmann, D. B., and Thormann, K. M. 2022. Polar flagellar wrapping and lateral flagella jointly contribute to Shewanella putrefaciens environmental spreading. Environ. Microbiol. 24:5911-5923. https://doi.org/10.1111/1462-2920.16107 Crossref, Medline, ISI, Google Scholar
Letunic, I., and Bork, P. 2019. Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res. 47:W256-W259. https://doi.org/10.1093/nar/gkz239 Crossref, Medline, ISI, Google Scholar
Li, T., Mann, R., Sawbridge, T., Kaur, J., Auer, D., and Spangenberg, G. 2020. Novel Xanthomonas species from the perennial ryegrass seed microbiome – assessing the bioprotection activity of non-pathogenic relatives of pathogens. Front. Microbiol. 11:1991. https://doi.org/10.3389/fmicb.2020.01991 Crossref, Medline, ISI, Google Scholar
Li, W., O'Neill, K. R., Haft, D. H., DiCuccio, M., Chetvernin, V., Badretdin, A., Coulouris, G., Chitsaz, F., Derbyshire, M. K., Durkin, A. S., Gonzales, N. R., Gwadz, M., Lanczycki, C. J., Song, J. S., Thanki, N., Wang, J., Yamashita, R. A., Yang, M., Zheng, C., Marchler-Bauer, A., and Thibaud-Nissen, F. 2021. RefSeq: Expanding the Prokaryotic Genome Annotation Pipeline reach with protein family model curation. Nucleic Acids Res. 49:D1020-D1028. https://doi.org/10.1093/nar/gkaa1105 Crossref, Medline, ISI, Google Scholar
Liu, L., Li, Y., Xu, Z., Chen, H., Zhang, J., Manion, B., Liu, F., Zou, L., Fu, Z. Q., and Chen, G. 2022. The Xanthomonas type III effector XopAP prevents stomatal closure by interfering with vacuolar acidification. J. Integr. Plant Biol. 64:1994-2008. https://doi.org/10.1111/jipb.13344 Crossref, Medline, ISI, Google Scholar
López, M. M., Lopez-Soriano, P., Garita-Cambronero, J., Beltrán, C., Taghouti, G., Portier, P., Cubero, J., Fischer-Le Saux, M., and Marco-Noales, E. 2018. Xanthomonas prunicola sp. nov., a novel pathogen that affects nectarine (Prunus persica var. nectarina) trees. Int. J. Syst. Evol. Microbiol. 68:1857-1866. https://doi.org/10.1099/ijsem.0.002743 Crossref, Medline, ISI, Google Scholar
Mafakheri, H., Taghavi, S. M., Zarei, S., Portier, P., Dimkić, I., Koebnik, R., Kuzmanović, N., and Osdaghi, E. 2022. Xanthomonas bonasiae sp. nov. and Xanthomonas youngii sp. nov., isolated from crown gall tissues. Int. J. Syst. Evol. Microbiol. 72. https://doi.org/10.1099/ijsem.0.005418 Crossref, Medline, ISI, Google Scholar
Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., Dow, M., Verdier, V., Beer, S. V., Machado, M. A., Toth, I., Salmond, G., and Foster, G. D. 2012. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13:614-629. https://doi.org/10.1111/j.1364-3703.2012.00804.x Crossref, Medline, ISI, Google Scholar
Martins, L., Fernandes, C., Blom, J., Dia, N. C., Pothier, J. F., and Tavares, F. 2020. Xanthomonas euroxanthea sp. nov., a new xanthomonad species including pathogenic and non-pathogenic strains of walnut. Int. J. Syst. Evol. Microbiol. 70:6024-6031. https://doi.org/10.1099/ijsem.0.004386 Crossref, Medline, ISI, Google Scholar
Maruyama, Y., Kobayashi, M., Murata, K., and Hashimoto, W. 2015. Formation of a single polar flagellum by two distinct flagellar gene sets in Sphingomonas sp. strain A1. Microbiology (Reading) 161:1552-1560. https://doi.org/10.1099/mic.0.000119 Crossref, Medline, ISI, Google Scholar
McCarter, L., and Silverman, M. 1989. Iron regulation of swarmer cell differentiation of Vibrio parahaemolyticus. J. Bacteriol. 171:731-736. https://doi.org/10.1128/jb.171.2.731-736.1989 Crossref, Medline, ISI, Google Scholar
Meier-Kolthoff, J. P., Auch, A. F., Klenk, H.-P., and Göker, M. 2013. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. 14:60. https://doi.org/10.1186/1471-2105-14-60 Crossref, Medline, ISI, Google Scholar
Meier-Kolthoff, J. P., Carbasse, J. S., Peinado-Olarte, R. L., and Göker, M. 2022. TYGS and LPSN: A database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res. 50:D801-D807. https://doi.org/10.1093/nar/gkab902 Crossref, Medline, ISI, Google Scholar
Meier-Kolthoff, J. P., and Göker, M. 2019. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat. Commun. 10:2182. https://doi.org/10.1038/s41467-019-10210-3 Crossref, Medline, ISI, Google Scholar
Melotto, M., Underwood, W., Koczan, J., Nomura, K., and He, S. Y. 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969-980. https://doi.org/10.1016/j.cell.2006.06.054 Crossref, Medline, ISI, Google Scholar
Mitchell, R. E. 1991. Coronatine analogues produced by Xanthomonas campestris pv phormiicola. Phytochemistry 30:3917-3920. https://doi.org/10.1016/0031-9422(91)83434-M Crossref, ISI, Google Scholar
Parkinson, N., Aritua, V., Heeney, J., Cowie, C., Bew, J., and Stead, D. 2007. Phylogenetic analysis of Xanthomonas species by comparison of partial gyrase B gene sequences. Int. J. Syst. Evol. Microbiol. 57:2881-2887. https://doi.org/10.1099/ijs.0.65220-0 Crossref, Medline, ISI, Google Scholar
Parkinson, N., Cowie, C., Heeney, J., and Stead, D. 2009. Phylogenetic structure of Xanthomonas determined by comparison of gyrB sequences. Int. J. Syst. Evol. Microbiol. 59:264-274. https://doi.org/10.1099/ijs.0.65825-0 Crossref, Medline, ISI, Google Scholar
Parte, A. C., Sardà Carbasse, J., Meier-Kolthoff, J. P., Reimer, L. C., and Göker, M. 2020. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int. J. Syst. Evol. Microbiol. 70:5607-5612. https://doi.org/10.1099/ijsem.0.004332 Crossref, Medline, ISI, Google Scholar
Pieretti, I., Cociancich, S., Bolot, S., Carrère, S., Morisset, A., Rott, P., and Royer, M. 2015. Full genome sequence analysis of two isolates reveals a novel Xanthomonas species close to the sugarcane pathogen Xanthomonas albilineans. Genes (Basel) 6:714-733. https://doi.org/10.3390/genes6030714 Crossref, Medline, ISI, Google Scholar
Pieretti, I., Royer, M., Barbe, V., Carrere, S., Koebnik, R., Cociancich, S., Couloux, A., Darrasse, A., Gouzy, J., Jacques, M. A., Lauber, E., Manceau, C., Mangenot, S., Poussier, S., Segurens, B., Szurek, B., Verdier, V., Arlat, M., and Rott, P. 2009. The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 10:616. https://doi.org/10.1186/1471-2164-10-616 Crossref, Medline, ISI, Google Scholar
Raffeiner, M., Üstün, S., Guerra, T., Spinti, D., Fitzner, M., Sonnewald, S., Baldermann, S., and Börnke, F. 2022. The Xanthomonas type-III effector XopS stabilizes CaWRKY40a to regulate defense responses and stomatal immunity in pepper (Capsicum annuum). Plant Cell 34:1684-1708. https://doi.org/10.1093/plcell/koac032 Crossref, Medline, ISI, Google Scholar
Rana, R., Madhavan, V. N., Saroha, T., Bansal, K., Kaur, A., Sonti, R. V., Patel, H. K., and Patil, P. B. 2022. Xanthomonas indica sp. nov., a novel member of non-pathogenic Xanthomonas community from healthy rice seeds. Curr. Microbiol. 79:304. https://doi.org/10.1007/s00284-022-03001-5 Crossref, Medline, ISI, Google Scholar
Richter, M., and Rosselló-Móra, R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. U. S. A. 106:19126-19131. https://doi.org/10.1073/pnas.0906412106 Crossref, Medline, ISI, Google Scholar
Roux, D., Schaefers, M., Clark, B. S., Weatherholt, M., Renaud, D., Scott, D., LiPuma, J. J., Priebe, G., Gerard, C., and Yoder-Himes, D. R. 2018. A putative lateral flagella of the cystic fibrosis pathogen Burkholderia dolosa regulates swimming motility and host cytokine production. PLoS One 13:e0189810. https://doi.org/10.1371/journal.pone.0189810 Crossref, Medline, ISI, Google Scholar
Slawiak, M., and Lojkowska, E. 2009. Genes responsible for coronatine synthesis in Pseudomonas syringae present in the genome of soft rot bacteria. Eur. J. Plant Pathol. 124:353-361. https://doi.org/10.1007/s10658-008-9418-7 Crossref, ISI, Google Scholar
Smirnova, A. V., Wang, L., Rohde, B., Budde, I., Weingart, H., and Ullrich, M. S. 2002. Control of temperature-responsive synthesis of the phytotoxin coronatine in Pseudomonas syringae by the unconventional two-component system CorRPS. J. Mol. Microbiol. Biotechnol. 4:191-196. Medline, ISI, Google Scholar
Sneath, P. H. A., and Sokal, R. R. 1973. Numerical Taxonomy. Freeman, San Francisco, CA. Google Scholar
Stecher, G., Tamura, K., and Kumar, S. 2020. Molecular Evolutionary Genetics Analysis (MEGA) for macOS. Mol. Biol. Evol. 37:1237-1239. https://doi.org/10.1093/molbev/msz312 Crossref, Medline, ISI, Google Scholar
Studholme, D. J., Wasukira, A., Paszkiewicz, K., Aritua, V., Thwaites, R., Smith, J., and Grant, M. 2011. Draft genome sequences of Xanthomonas sacchari and two banana-associated xanthomonads reveal insights into the Xanthomonas group 1 clade. Genes (Basel) 2:1050-1065. https://doi.org/10.3390/genes2041050 Crossref, Medline, ISI, Google Scholar
Takimoto, S. 1933. Bacterial diseases of New Zealand flax. Byogaichu zasshi 20:774-778. Google Scholar
Tamura, K., Stecher, G., and Kumar, S. 2021. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38:3022-3027. https://doi.org/10.1093/molbev/msab120 Crossref, Medline, ISI, Google Scholar
Tamura, K., Takikawa, Y., Tsuyumu, S., Goto, M., and Kijima, T. 1987. Coronatine-like substance produced by Xanthomonas campestris pv. phormiicola. Ann. Phytopathol. Soc. Jpn. 53:72-73. Google Scholar
Tamura, K., Takikawa, Y., Tsuyumu, S., Goto, M., and Watanabe, M. 1992. Coronatine production by Xanthomonas campestris pv. phormiicola. Ann. Phytopathol. Soc. Jpn. 58:276-281. https://doi.org/10.3186/jjphytopath.58.276 Crossref, Google Scholar
Vicente, J. G., Rothwell, S., Holub, E. B., and Studholme, D. J. 2017. Pathogenic, phenotypic and molecular characterisation of Xanthomonas nasturtii sp. nov. and Xanthomonas floridensis sp. nov., new species of Xanthomonas associated with watercress production in Florida. Int. J. Syst. Evol. Microbiol. 67:3645-3654. https://doi.org/10.1099/ijsem.0.002189 Crossref, Medline, ISI, Google Scholar
Wang, S., Li, S., Wang, J., Li, Q., Xin, X. F., Zhou, S., Wang, Y., Li, D., Xu, J., Luo, Z. Q., He, S. Y., and Sun, W. 2021. A bacterial kinase phosphorylates OSK1 to suppress stomatal immunity in rice. Nat. Commun. 12:5479. https://doi.org/10.1038/s41467-021-25748-4 Crossref, Medline, ISI, Google Scholar
Zain, B. S., and Roberts, R. J. 1977. A new specific endonuclease from Xanthomonas badrii. J. Mol. Biol. 115:249-255. https://doi.org/10.1016/0022-2836(77)90101-2 Crossref, Medline, ISI, Google Scholar