Whole Genome Resources of 17 Curtobacterium Flaccumfaciens Strains Including Pathotypes of C. Flaccumfaciens Pv. Betae, C. Flaccumfaciens Pv. Oortii, and C. Flaccumfaciens Pv. Poinsettiae

HomeMolecular Plant-Microbe Interactions®Vol. 35, No. 4Whole Genome Resources of 17 Curtobacterium flaccumfaciens Strains Including Pathotypes of C. flaccumfaciens pv. betae, C. flaccumfaciens pv. oortii, and C. flaccumfaciens pv. poinsettiae PreviousNext RESOURCE ANNOUNCEMENT OPENOpen Access licenseWhole Genome Resources of 17 Curtobacterium flaccumfaciens Strains Including Pathotypes of C. flaccumfaciens pv. betae, C. flaccumfaciens pv. oortii, and C. flaccumfaciens pv. poinsettiaeEbrahim Osdaghi, Geraldine Taghouti, Cecile Dutrieux, S. Mohsen Taghavi, Amal Fazliarab, Martial Briand, Marion Fischer-Le Saux, Perrine Portier, and Marie-Agnes JacquesEbrahim Osdaghi†Corresponding authors: E. Osdaghi; E-mail Address: eosdaghi@ut.ac.ir, P. Portier; E-mail Address: perrine.portier@inrae.fr, and M.-A. Jacques; E-mail Address: marie-agnes.jacques@inrae.frhttps://orcid.org/0000-0002-0359-0398Department of Plant Protection, College of Agriculture, University of Tehran, Karaj 31587-77871, IranSearch for more papers by this author, Geraldine TaghoutiUniversity of Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, FranceSearch for more papers by this author, Cecile DutrieuxUniversity of Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, FranceSearch for more papers by this author, S. Mohsen TaghaviDepartment of Plant Protection, School of Agriculture, Shiraz University, Shiraz 71441-65186, IranSearch for more papers by this author, Amal FazliarabIranian Sugarcane Research and Training Institute (ISCRTI), Ahvaz, Khuzestan, IranSearch for more papers by this author, Martial BriandUniversity of Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, FranceSearch for more papers by this author, Marion Fischer-Le SauxUniversity of Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, FranceSearch for more papers by this author, Perrine Portier†Corresponding authors: E. Osdaghi; E-mail Address: eosdaghi@ut.ac.ir, P. Portier; E-mail Address: perrine.portier@inrae.fr, and M.-A. Jacques; E-mail Address: marie-agnes.jacques@inrae.frUniversity of Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, FranceSearch for more papers by this author, and Marie-Agnes Jacques†Corresponding authors: E. Osdaghi; E-mail Address: eosdaghi@ut.ac.ir, P. Portier; E-mail Address: perrine.portier@inrae.fr, and M.-A. Jacques; E-mail Address: marie-agnes.jacques@inrae.frUniversity of Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, FranceSearch for more papers by this author AffiliationsAuthors and Affiliations Ebrahim Osdaghi1 † Geraldine Taghouti2 Cecile Dutrieux2 S. Mohsen Taghavi3 Amal Fazliarab4 Martial Briand2 Marion Fischer-Le Saux2 Perrine Portier2 † Marie-Agnes Jacques2 † 1Department of Plant Protection, College of Agriculture, University of Tehran, Karaj 31587-77871, Iran 2University of Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, CIRM-CFBP, F-49000 Angers, France 3Department of Plant Protection, School of Agriculture, Shiraz University, Shiraz 71441-65186, Iran 4Iranian Sugarcane Research and Training Institute (ISCRTI), Ahvaz, Khuzestan, Iran Published Online:14 Mar 2022https://doi.org/10.1094/MPMI-11-21-0282-AAboutSectionsPDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmailWechat Curtobacterium flaccumfaciens complex species in the family Microbacteriaceae encompasses a group of plant-pathogenic actinobacterial strains affecting annual crops and ornamental plants. The species includes five pathovars, namely C. flaccumfaciens pv. betae, C. flaccumfaciens pv. flaccumfaciens, C. flaccumfaciens pv. ilicis, C. flaccumfaciens pv. oortii, and C. flaccumfaciens pv. poinsettiae. Despite the economic importance of C. flaccumfaciens, its members have rarely been investigated for their phylogenetic relationships, molecular characteristics, and virulence repertories, due, in part, to the lack of whole-genome resources. Here, we present the whole-genome sequence of 17 C. flaccumfaciens strains representing members of four pathovars isolated from different plant species in a diverse geographical and temporal span. The genomic data presented in this study will pave the way for research on the comparative genomics, phylogenomics, and taxonomy of C. flaccumfaciens and extend our understanding of the virulence features of the species.Gram-positive actinobacterial plant pathogens in the family Microbacteriaceae comprise a series of economically important agents infecting several annual crops, ornamental plants, and vegetables (Dye and Kemp 1977; Jacques et al. 2012). Plant-pathogenic members in this group include Clavibacter spp., Rathayibacter spp., Leifsonia xyli, and Curtobacterium flaccumfaciens (Vidaver and Davis 1988). The latter species is a complex taxon comprising several pathovars as well as nonpathogenic, environmental, and, in some cases, clinical species (Francis et al. 2011). Among the gram-positive bacterial plant pathogens, C. flaccumfaciens is the least-studied member in terms of genomic features and pathogenicity determinants (Chen et al. 2021; Thapa et al. 2019). Plant-pathogenic members of C. flaccumfaciens are subdivided into five pathovars based on their host of isolation, pathogenicity, and host range (Collins and Jones 1983; Davis and Vidaver 2001; Davis 1986, 2001). Pathovars of the species include C. flaccumfaciens pv. flaccumfaciens, causing bacterial wilt of dry beans (Hedges 1922), C. flaccumfaciens pv. poinsettiae, causing bacterial canker of poinsettia (Pirone and Bender 1941), C. flaccumfaciens pv. betae, the agent of silvering disease of red beet (Keyworth et al. 1956), C. flaccumfaciens pv. ilicis, causing bacterial blight of American holly (Mandel et al. 1961; Young et al. 2004), and C. flaccumfaciens pv. oortii, the agent of bacterial wilt and spot of tulip (Saaltink and Maas Geesteranus 1969). Two additional pathovars including ‘C. flaccumfaciens pv. basellae’, the causal agent of bacterial leaf spot of malabar spinach (Basella alba or B. ruba) (Chen et al. 2000), and ‘C. flaccumfaciens pv. beticola’, the causal agent of bacterial leaf spot of sugar beet (Chen et al. 2007) were also proposed. However, the Committee on the Taxonomy of Plant Pathogenic bacteria (Bull et al. 2010) has not accepted them to date as valid taxa.Among these pathovars, bacterial wilt of dry beans caused by C. flaccumfaciens pv. flaccumfaciens and bacterial canker of poinsettia caused by C. flaccumfaciens pv. poinsettiae are economically important, the former one being included as a quarantine pathogen in the Annex II part A of European Regulation 2019/2072 and in the A2 list of the European and Mediterranean Plant Protection Organization and the latter one being included in the alert lists of EPPO (EPPO 2011; Osdaghi et al. 2020a). While molecular diagnostic tests are available to detect and identify C. flaccumfaciens pv. flaccumfaciens (Tegli et al. 2020), quarantined members of the species require considerable cost and effort to prevent the risk of global spread and introduction into areas yet free of the disease (Harveson et al. 2015; Osdaghi et al. 2020a). Members of C. flaccumfaciens are well-known for variability in colony pigmentation and morphology possessing a wide range of colony variants including orange, pink, purple, red, and yellow phenotypes in either fluidal, mucoid, or dry form on culture media (Harveson and Vidaver 2008; Osdaghi and Lak 2015; Osdaghi et al. 2016). As a complex species, population structure and taxonomy of C. flaccumfaciens has rarely been examined using high throughput genomics techniques, leaving the phylogenetic relationships of different pathovars to each other uninvestigated. Further, due to the lack of whole-genome resources from different pathovars of C. flaccumfaciens, pathogenicity-associated genomic features and virulence strategies of its members are still almost entirely unknown. Unlike the other plant-pathogenic actinobacteria, for which the nucleotide sequence data from a wide range of strains are available (Ansari et al. 2019; Jacques et al. 2012; Osdaghi et al. 2020b), whole-genome sequence data of only a few C. flaccumfaciens strains are published in the literature (Chen et al. 2021). Among the pathotype strains of the species, C. flaccumfaciens pv. flaccumfaciens is the only one for which a whole-genome sequence is available (Gonçalves et al. 2019).DNA fingerprinting-based investigations (Agarkova et al. 2012; Osdaghi et al. 2018a) and multilocus sequence analysis (MLSA) (Gonçalves et al. 2019: Osdaghi et al. 2018b) suggested high genetic diversity among plant pathogenic members of C. flaccumfaciens either in an intrapathovar or interpathovar level. For instance, it has been noted that yellow-pigmented strains of the dry bean pathogen C. flaccumfaciens pv. flaccumfaciens are genetically and phylogenetically distinct from those of red- and orange-pigmented strains of the same pathovar (Osdaghi et al. 2018a, b). Interestingly, MLSA-based results showed that the red- and orange-pigmented strains of the latter pathogen are phylogenetically more related to the poinsettia pathogen C. flaccumfaciens pv. poinsettiae than to the pathotype strain of C. flaccumfaciens pv. flaccumfaciens. All these findings led us to conclude that an inclusive genome sequencing effort is warranted to shed light on the taxonomic structure, phylogenetic relationships, and genomic repertoires of C. flaccumfaciens members. Thus, the main objective of this study was to provide whole-genome resources for 17 C. flaccumfaciens strains, covering nearly the entire genetic diversity of the species, including the pathotype strains of C. flaccumfaciens pv. betae, C. flaccumfaciens pv. oortii, and C. flaccumfaciens pv. poinsettiae.C. flaccumfaciens strains representing members of different pathovars with various colony morphology (pigmentation) and diverse geographic origins were obtained from the French Collection for Plant-Associated Bacteria CIRM-CFBP (Table 1). The strains were streaked onto yeast-extract peptone glucose agar medium, were resuspended in sterile distilled water and stored at 4°C for further use, and were stored in 15% glycerol at −70°C for long-term purposes. Bacterial DNAs were extracted using the Wizard genomic DNA purification kit (Promega, Madison WI, U.S.A.). The 17 strains were sequenced using NovaSeq 6000 Illumina with Nextera XT Preparation kit and paired-end 150 bp (Institut du Cerveau, CHU Pitié-Salpêtrière, Paris). Genome assembly was performed using SPAdes 1 (Bankevich et al. 2012) after a quality filtration with CheckM (Parks et al. 2015). For each strain, sequencing coverage, genome size, number of contigs, and G+C percentage are summarized in Table 1. Genome annotation was performed using the GeneMarkS+ suite implemented in the National Center for Biotechnology Information (NCBI) Prokaryotic Genome Annotation Pipeline with default settings (Borodovsky and Lomsadze 2014). Total number of genes and coding sequences were determined for all the genomes (Table 1).Table 1. Source, place, and date of isolation, and genomic information of the Curtobacterium flaccumfaciens strains used in this studyStrainOther namesTaxonHostYearCountryColony color (pigmentation)Genome size (bp)No. ofG+C% contentCoverage ×Plasmid/phagebGenBank accession numberCDSsaGenesContigsPlasmid FinderSourceFinderPhagecPlasmidCFBP 2402PTICMP 2594PT, LMG 3596PT, NCPPB 374PTC. flaccumfaciens pv. betaeBeta vulgaris1955U.K.Yellow-Dry3,768,0773,5343,5895070.9219ND45, 49, 50NDJAHEXD000000000CFBP 1384PTNCPPB 2113PT, ATCC 25283PT, ICMP 2632PT, LMG 3702PTC. flaccumfaciens pv. oortiiTulipa gesneriana1967NetherlandsYellow-Fluidal4,024,4223,8213,8786470.7249ND7, 54, 59, 61, 63, 64NDJAHEXC000000000CFBP 2403PTICMP 2566PT, ATCC 9682PT, NCPPB 854PTC. flaccumfaciens pv. poinsettiaeEuphorbia pulcherrimaMissingU.S.A.Orange-Dry3,616,0773,3963,4505471.0219ND39, 53NDJAHEXB000000000CFBP 3400PD 1751C. flaccumfaciens pv. oortiiZantedeschia aethiopica1990NetherlandsYellow-Dry3,773,5923,5593,6144871.0249NDNDNDJAHEXA000000000CFBP 3423NCPPB 2344, ATCC 23827C. flaccumfaciens pv. flaccumfaciensPhaseolus vulgaris1957U.S.A.Yellow-Fluidal3,906,8943,6823,7395270.5204ND25, 41, 43, 46, 51, 5240, 44, 45JAHEWZ000000000CFBP 3422NCPPB 2343, ATCC 12813C. flaccumfaciens pv. flaccumfaciensPhaseolus vulgaris1956U.S.A.Orange-Dry3,587,1233,3493,4044571.0234ND2, 44NDJAHEWY000000000CFBP 3417NCPPB 558C. flaccumfaciens pv. flaccumfaciensPhaseolus vulgaris1958U.S.A.Orange-Fluidal3,731,9363,5493,6044870.8264ND15, 22, 40, 46, 47, 4836JAHEWX000000000CFBP 3401LMG 7238, PDDCC 4735C. flaccumfaciens pv. betaeBeta vulgarisMissingU.K.Yellow-Dry3,771,8933,5403,5955270.9310ND9, 17, 19, 40, 42, 43, 46, 47, 48, 49, 50NDJAHEWW000000000CFBP 3415LMG 7321C. flaccumfaciens pv. poinsettiaeEuphorbia pulcherrimaMissingU.S.A.Orange-Fluidal3,693,8183,4643,5184370.9332ND40, 42, 43NDJAHEWU000000000CFBP 8818Tom50, ICMP 22062C. flaccumfaciens pv. flaccumfaciensSolanum lycopersicum2015IranRed-Dry3,718,2763,4973,5537370.9189ND19, 56, 59, 63, 67NDJAHEWT000000000CFBP 881950R, ICMP 22071C. flaccumfaciens pv. flaccumfaciensPhaseolus vulgaris2014IranRed-Fluidal3,722,5623,5043,5566370.8219ND24, 44, 48, 53, 57, 60NDJAHEWS000000000CFBP 8820P990, ICMP 22053C. flaccumfaciens pv. flaccumfaciensCapsicum annuum2015IranYellow-Fluidal3,841,5553,6183,6735670.9234ND24, 52, 55, 56NDJAHEWR000000000CFBP 8821Cmmeg20, ICMP 22056C. flaccumfaciensSolanum melongena2014IranYellow-Fluidal3,667,5573,4173,4704771.0189ND46, 47NDJAHEWQ000000000CFBP 8822Xeu15, ICMP 21400C. flaccumfaciensCapsicum annuum2013IranYellow-Fluidal3,715,9763,4953,5494771.0219ND46, 47NDJAHEWP000000000CFBP 8823Cff156C. flaccumfaciens pv. flaccumfaciensPhaseolus vulgaris2015IranOrange-Fluidal3,749,4033,5193,5766570.8227ND12, 23, 53, 56, 59, 64NDJAHEWO000000000CFBP 8824G105, ICMP 22064C. flaccumfaciensSolanum lycopersicum2015IranRed-Fluidal3,603,5413,3693,4223571.0287ND8, 33, 35NDJAHEWN000000000CFBP 8825Tom827, ICMP 22084C. flaccumfaciensSolanum lycopersicum2015IranYellow-Fluidal3,707,673 3,4873,5424771.0189ND25, 45, 46NDJAHEWM000000000aCDS = coding sequences.bPresence of plasmids was evaluated using both PlasmidFinder and SourceFinder services, while the presence of phages was evaluated using SourceFinder. ND = Not detected.cThe numbers indicate the contig number in the FASTA files (in the GenBank database) in which the corresponding sequence was detected.Table 1. Source, place, and date of isolation, and genomic information of the Curtobacterium flaccumfaciens strains used in this studyView as image HTML Whole-genome sequences of the 17 C. flaccumfaciens strains obtained in this study were assembled in contigs varying in number from 35 to 73, while sequencing coverage was between 189× and 332× (Table 1). Genome size of the strains ranged from 3,587,123 bp in C. flaccumfaciens pv. flaccumfaciens CFBP 3422 to 4,024,422 bp in the pathotype strain of C. flaccumfaciens pv. oortii CFBP 1384PT, while G+C% content was between 70.5 and 71.0% (Table 1). It has previously been shown that a number of C. flaccumfaciens strains possess plasmids harboring various biological functions (Chen et al. 2021; Hendrick et al. 1984; Vaghefi et al. 2021). Hence, the genome sequences obtained in this study were investigated for the presence of plasmid and phage sequences via online services PlasmidFinder 2.0 and SourceFinder 1.0 (Carattoli et al. 2014). While PlasmidFinder did not find any plasmid in the genome sequences, SourceFinder suggested the presence of plasmid in the C. flaccumfaciens pv. flaccumfaciens strains CFBP 3423 and CFBP 3417. Phage fragments were also frequently detected in all the genomes except C. flaccumfaciens pv. oortii CFBP 3400, as detailed in Table 1. Agarose gel–based plasmid profiling is recommended to decipher the precise plasmid profile of the strains sequenced in this study. Furthermore, a preliminary average nucleotide identity (ANI) and digital DNA-DNA hybridization calculation among the strains sequenced in this study suggest a need for an in-depth taxonomic investigation on the phylogenetic relationships of the C. flaccumfaciens members. For instance, ANI between the type strain of C. flaccumfaciens CFBP 3418T and the pathotype strain of C. flaccumfaciens pv. poinsettiae CFBP 2403PT was 93.5%, which was below the accepted threshold (95 to 96%) for definition of prokaryotic species (Kim et al. 2014). A comprehensive multiphasic taxonomic study is ongoing to re-evaluate the taxonomy of C. flaccumfaciens complex species.Data AvailabilityThe whole-genome shotgun sequences obtained in this study are deposited at the NCBI GenBank database under the accession numbers shown in Table 1. Furthermore, a pure culture of the 17 strains is available in CIRM-CFBP culture collection.AcknowledgmentsWe thank C. Dutrieux and A. Lathus at CIRM-CFBP for preservation of the bacterial strains.The author(s) declare no conflict of interest.Literature CitedAgarkova, I. V., Lambrecht, P. A., Vidaver, A. K., and Harveson, R. M. 2012. Genetic diversity among Curtobacterium flaccumfaciens pv. flaccumfaciens populations in the American high plains. 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This is an open access article distributed under the CC BY-NC-ND 4.0 International license.DetailsFiguresLiterature CitedRelated Vol. 35, No. 4 April 2022ISSN:0894-0282e-ISSN:1943-7706 Download Metrics Downloaded 867 times Article History Issue Date: 12 Apr 2022Published: 14 Mar 2022First Look: 12 Jan 2022Accepted: 10 Jan 2022 Pages: 352-356 InformationCopyright © 2022 The Author(s).This is an open access article distributed under the CC BY-NC-ND 4.0 International license.FundingInstitut National de la Recherche AgronomiqueGrant/Award Number: CIRM 2020College of Agriculture Natural Resources, University of TehranGrant/Award Number: CA16107Keywordsactinobacteriabacterial wilt of beanscoryneform bacteriaMicrobacteriaceaequarantine pathogenbacterial pathogenesisThe author(s) declare no conflict of interest.PDF download