The Genomic Landscape Resource of Pseudomonas syringae pv. syringae Strains Isolated from Mango Trees.

HomeMolecular Plant-Microbe Interactions®Vol. 35, No. 12The Genomic Landscape Resource of Pseudomonas syringae pv. syringae Strains Isolated from Mango Trees PreviousNext RESOURCE ANNOUNCEMENT OPENOpen Access licenseThe Genomic Landscape Resource of Pseudomonas syringae pv. syringae Strains Isolated from Mango TreesJosé A. Gutiérrez-Barranquero, Zaira Heredia-Ponce, Lorena Aguilera-Cobos, Adrián Pintado, M. Gonzalo Claros, Cayo Ramos, Francisco M. Cazorla, and Antonio de VicenteJosé A. Gutiérrez-Barranquero†Corresponding author: J. A. Gutiérrez-Barranquero; E-mail Address: jagutierrez@uma.eshttps://orcid.org/0000-0003-1810-699XInstituto de Hortofruticultura Subtropical y Mediterránea La Mayora (IHSM-UMA-CSIC)Departamento de Microbiología, Facultad de Ciencias, Universidad de Málaga, Málaga, SpainSearch for more papers by this author, Zaira Heredia-PonceInstituto de Hortofruticultura Subtropical y Mediterránea La Mayora (IHSM-UMA-CSIC)Departamento de Microbiología, Facultad de Ciencias, Universidad de Málaga, Málaga, SpainSearch for more papers by this author, Lorena Aguilera-CobosPlataforma Andaluza de Bioinformática-SCBI, Universidad de Málaga, Málaga, SpainSearch for more papers by this author, Adrián PintadoInstituto de Hortofruticultura Subtropical y Mediterránea La Mayora (IHSM-UMA-CSIC)Departamento de Biología Celular, Genética y Fisiología, Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, SpainSearch for more papers by this author, M. Gonzalo Claroshttps://orcid.org/0000-0002-0112-3550Instituto de Hortofruticultura Subtropical y Mediterránea La Mayora (IHSM-UMA-CSIC)Plataforma Andaluza de Bioinformática-SCBI, Universidad de Málaga, Málaga, SpainDepartamento de Biología Molecular y Bioquímica, Facultad de Ciencias, Universidad de Málaga, Málaga, SpainSearch for more papers by this author, Cayo RamosInstituto de Hortofruticultura Subtropical y Mediterránea La Mayora (IHSM-UMA-CSIC)Departamento de Biología Celular, Genética y Fisiología, Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, SpainSearch for more papers by this author, Francisco M. CazorlaInstituto de Hortofruticultura Subtropical y Mediterránea La Mayora (IHSM-UMA-CSIC)Departamento de Microbiología, Facultad de Ciencias, Universidad de Málaga, Málaga, SpainSearch for more papers by this author, and Antonio de Vicentehttps://orcid.org/0000-0003-2716-9861Instituto de Hortofruticultura Subtropical y Mediterránea La Mayora (IHSM-UMA-CSIC)Departamento de Microbiología, Facultad de Ciencias, Universidad de Málaga, Málaga, SpainSearch for more papers by this authorAffiliationsAuthors and Affiliations José A. Gutiérrez-Barranquero1 2 † Zaira Heredia-Ponce1 2 Lorena Aguilera-Cobos3 Adrián Pintado1 4 M. Gonzalo Claros1 3 5 Cayo Ramos1 4 Francisco M. Cazorla1 2 Antonio de Vicente1 2 1Instituto de Hortofruticultura Subtropical y Mediterránea La Mayora (IHSM-UMA-CSIC) 2Departamento de Microbiología, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain 3Plataforma Andaluza de Bioinformática-SCBI, Universidad de Málaga, Málaga, Spain 4Departamento de Biología Celular, Genética y Fisiología, Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain 5Departamento de Biología Molecular y Bioquímica, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain Published Online:12 Dec 2022https://doi.org/10.1094/MPMI-05-22-0107-AAboutSectionsView articlePDFSupplemental ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmailWechat View articleGenome Resource AnnouncementPseudomonas syringae pv. syringae is the causal agent of bacterial apical necrosis (BAN) disease of mango trees (Cazorla et al. 1998). BAN disease is the most limiting factor of mango trees in the Mediterranean region because it severely affects mango yield in seasons when weather conditions are favorable to develop the infection by P. syringae pv. syringae (Gutiérrez-Barranquero et al. 2012). P. syringae pv. syringae isolates from mango possess a vast arsenal of virulence factors highlighting the production of the antimetabolite toxin mangotoxin (Arrebola et al. 2003). Other important adaptation traits were also present is P. syringae pv. syringae isolates from mango, such as the production of the exopolysaccharide (EPS) cellulose. The presence of different variants of copper resistance genes have been detected in plasmids belonging to the pPT23A family of plasmids, a family that appears to be indigenous to P. syringae (Sesma et al. 1998). These adaptation traits enhance epiphytic fitness on mango tree surfaces (Gutiérrez-Barranquero et al. 2013a, 2017, 2019; Heredia-Ponce et al. 2020). P. syringae pv. syringae strains from mango form a specific phylotype within the pathovar syringae, strongly associated with the mango host and with mangotoxin production (Gutiérrez-Barranquero et al. 2013b, 2019). To date, genomic information of P. syringae pv. syringae belonging to this specific phylotype remain scarce, with only three genome sequences available in GenBank (Aprile et al. 2021; Martinez-García et al. 2015). Based on a previous phylogenetic distribution study performed within this specific phylotype, including strains from two groups isolated at different times (Aprile et al. 2021), the presence of various phylogenetic subgroups (PSGs) was observed.From these important PSGs, different strains were selected for genome sequencing, to obtain a comprehensive overview of the genomic landscape of the P. syringae pv. syringae mango phylotype. The main characteristics of the P. syringae pv. syringae strains that were selected are summarized in Supplementary Table S1. P. syringae pv. syringae strains were streaked onto King's B agar plates from −80°C frozen stocks and were grown for 48 h at 25°C. Single colonies from these plates were sampled using sterile toothpicks to inoculate 5 ml lysogenic broth (LB) tubes that were grown for 18 h at 25°C with shaking at 150 rpm. Total DNA extractions were performed using the DNAeasy UltraClean microbial kit (Qiagen) following manufacturer instructions. DNA libraries were prepared using the Nextera XT DNA library preparation kit for small genomes (Illumina, Inc.). Whole draft genome sequencing was performed by the Supercomputing and Bioinnovation Center of the University of Málaga, using the sequencing platform NextSeq 550 with paired-end reads, with a read length of 2 × 150 bp. To obtain high-quality reads for assembly, raw reads were pre-processed using SeqTrimBB, a modified software of SeqTrim (Falgueras et al. 2010), to eliminate low-quality reads and contaminants. The assembly of high-quality filtered reads was conducted using the A5-MiSeq pipeline with default parameters (Coil et al. 2015).Genome sequence annotation and gene identifications were obtained using two different approaches: i) the National Center for Biotechnology Information (NCBI) Prokaryotic Genome Annotation Pipeline (PGAP), using default parameters, and ii) Prokka (version 1.14.6), a command line software, to obtain a rapid prokaryotic genome annotation (Seemann 2014) with default parameters. The main features of the draft genome sequences obtained in this work, including their accession numbers, are listed in Table 1. The whole draft genome sizes ranged from 5.83 to 6.02 Mb, with a total number of coding DNA sequences ranging from 5,030 to 5,206 and G + C content from 59.1 to 59.3%, values that are typical for strains belonging to P. syringae species. The sequencing mean coverage of each genome sequence ranged from 605 to 1,118× and the content of transfer RNAs ranged from 57 to 63, based on PGAP results.Table 1. Accession numbers and genome assembly features of Pseudomonas syringae pv. syringae strains used in this studyaStrainsPSGGenBank accession no.Genome size (Mb)No. of scaffoldsN50 (bp)Coverage (×)No. of CDSNo. of tRNAsG + C content (%)UMAF2044PSG-IJAJPOB0000000005.8738809,1291,1185,0815959.3UMAF0049PSG-IIJAJPON0000000005.9524493,8859505,1395959.2UMAF0081PSG-IIJAJPOM0000000005.8724411,1701,0525,0305859.3UMAF0271PSG-IIJAJPOF0000000005.9520753,3529595,1336159.2UMAF7000PSG-IIIJAJPNY0000000005.9222669,5709635,0716159.2UMAF0176PSG-IVJAJPOK0000000005.8715907,0061,0415,0385959.2UMAF0297PSG-IVJAJPOD0000000005.9418819,9678705,1015659.2UMAF1013PSG-IVJAJPOC0000000005.9929663,1696815,2065959.2UMAF1029PSG-IVJAJPOI0000000006.0120820,0421,0355,1865859.2UMAF2801PSG-IVJAJPOH0000000005.9415564,1991,0175,0935759.1UMAF2815PSG-IVJAJPNZ0000000005.8912810,1341,0635,0976359.1EPS17APSG-VIJAJPOO0000000005.9125556,0857025,1115759.2UMAF1003PSG-VIJAJPOJ0000000006.0228551,3716315,2055859.2UMAF0170PSG-VIIJAJPOL0000000005.9265473,4116055,1105759.1UMAF0273PSG-VIIJAJPOE0000000005.83101,076,7719765,0725959.3UMAF2016PSG-VIIJAJPOG0000000005.8929414,3596285,1015759.2UMAF2600PSG-VIIJAJPOA0000000005.9227660,2828845,1636059.2DAR77789PSG-VIIJAJPOP0000000005.8722468,6186815,1025759.2aPSG = phylogenetic subgroup, CDS = coding DNA sequences, and tRNA = transfer RNA.Table 1. Accession numbers and genome assembly features of Pseudomonas syringae pv. syringae strains used in this studyaView as image HTML The Roary pipeline (Page et al. 2015) and the Bacterial Pan Genome Analysis Pipeline (BPGA) (Chaudhari et al. 2016) were both used to obtain the pangenome and core genomes. Based on Roary, the pangenome and core genomes (including the P. syringae pv. syringae B728a strain in our analysis) numbered 8,673 and 4,106 gene clusters, respectively, and using BPGA, the pangenome and core genomes were 8,202 and 3,963 protein-coding sequences, respectively. BGPA also uses curve fitting with Heaps’ law to estimate whether a pangenome is open or closed. Contrary to what was observed previously for the P. syringae complex (Dillon et al. 2019a), the pangenome of P. syringae pv. syringae isolates from mango was nearly closed, with a fitting parameter (γ) of 0.14, excluding the output P. syringae pv. syringae B728a strain (pangenome and core genomes by BPGA excluding P. syringae pv. syringae B728a were 7,590 and 4,273, respectively) (Supplementary Fig. S1A). A nearly closed pangenome was expected, as the 21 genomes of P. syringae pv. syringae strains isolated from mango would be suitable to capture most of the diversity of this genetically homogeneous group, in comparison to genomes of the entire P. syringae complex. The randomized axelerated maximum likelihood (RAxML, version 7.7.6) (Stamatakis 2014) method was used to analyze the phylogenetic distribution of the P. syringae pv. syringae strains based on the concatenated nucleotide sequences of genes belonging to the core genome obtained by the Roary pipeline. The RAxML phylogenetic tree was constructed using the GRT + gamma model with 1,000 fast bootstrap runs. The core genome phylogeny generated a rearrangement of certain P. syringae pv. syringae strains in comparison with the previous results, obtained using partial sequences of gyrB and rpoD genes (Aprile et al. 2021) (Fig. 1A). This result was considered more robust because of the inclusion of P. syringae pv. syringae strains isolated from pear in the same PSG. There is a correlation in the distribution of the strains, based on the area of isolation in some PSGs, in which old and new P. syringae pv. syringae strains isolated from related areas are part of the same PSGs (PSG-VIIa, PSG-I, PSG-II, and PSG-VI). In addition, there is a strong correlation based on their resistance or sensitivity to copper. Furthermore, the BLAST Atlas tool from the Gview server was used to perform a graphical genomic comparison, using the genome of P. syringae pv. syringae B728a as reference (Fig. 1B).Fig. 1. Core genome phylogeny and graphical comparative genomic analysis of Pseudomonas syringae pv. syringae strains isolated from mango. A, Phylogenetic analysis based on the multialigment of the concatenated nucleotide sequences belonging to the core genome of each P. syringae pv. syringae strain sequenced in this study (4,106 genes), including three other previously sequenced P. syringae pv. syringae strains isolated from mango (UMAF0158, UMAF0291, and UMAF3028). Strain P. syringae pv. syringae B728a was used as outgroup. Bootstrap values are included in the node of each branch. In addition, the year and location of isolation have been included. B, The BLAST Atlas tool was used for graphical comparative genomic analysis of P. syringae pv. syringae mango isolates, using the genome of P. syringae pv. syringae B728a as a reference. The different ring colors correspond to each P. syringae pv. syringae mango isolate belonging to different phylogenetic subgroups, with the same color code represented in A.Download as PowerPointGenome mining using BLAST searches revealed the presence of relevant genes associated with virulence or adaptation features essential for P. syringae pv. syringae lifestyle on mango tree surfaces. Regarding virulence factors, the mangotoxin generating operon (mgo operon) involved in the production of mangotoxin (Arrebola et al. 2007), an antimetabolite toxin very specific to P. syringae pv. syringae strains isolated from mango (Arrebola et al. 2003; Gutiérrez-Barranquero et al. 2013b), was present in the genome of all P. syringae pv. syringae strains isolated from mango. This operon has been recently described to synthesize the signaling molecule leudizen, a volatile molecule that controls mangotoxin production (Sieber et al. 2021). In addition, the mangotoxin biosynthetic operon (mbo operon) (Carrión et al. 2012) was also found in the genome of all the P. syringae pv. syringae strains. Interestingly, two different type III secretion systems were also found in all P. syringae pv. syringae mango genomes, as were previously identified in the complete genome sequence of P. syringae pv. syringae UMAF0158 (Martínez-García et al. 2015). The pool of predicted type III effectors was analyzed using the BastionHUb platform (Wang et al. 2021), a webserver that integrates and analyzes substrates secreted by gram-negative bacteria. The output from this database was revised to include the new reassignment of several type III effector families reported by Dillon et al. (2019b). The pan and core type III effectors numbered 21 and 16, respectively (Supplementary Fig. S1B).Regarding adaptation mechanisms, all P. syringae pv. syringae strains from mango harbored the biosynthetic genes of cellulose (wss operon), Psl-like, and alginate EPS. Cellulose and Psl-like EPS have been described to be crucial for adhesion and biofilm formation and to function as switches between epiphytic and pathogenic lifestyles (Arrebola et al. 2015; Heredia-Ponce et al. 2020). Interestingly, and similar to what was observed previously for mangotoxin, the wss operon is a very specific feature of the P. syringae pv. syringae mango phylotype. Another important adaption mechanism is the presence of different variants of copper resistance genes, mainly associated with 62-kb pPT23A plasmids. From the 18 P. syringae pv. syringae draft genomes sequenced in this study, 11 P. syringae pv. syringae strains harbored different variants of copper resistance genes (Supplementary Table S1), which could improve their survival against copper treatments (Aprile et al. 2021; Cazorla et al. 2002; Gutiérrez-Barranquero et al. 2019). Finally, to analyze the genetic diversity of our P. syringae pv. syringae mango genomes, the FastANI method (Jain et al. 2018) was performed using the 21 P. syringae pv. syringae strains from mango, nine P. syringae pv. syringae strains isolated from others hosts, and strain P. syringae pv. tomato DC3000 (Feil et al. 2005) (Supplementary Fig. S2). The highest and average ANI values exclusively for P. syringae pv. syringae mango genomes were 99.98 and 99.09%, respectively. The highest and average ANI values for all P. syringae pv. syringae genomes included in this analysis were 99.98% (between mango P. syringae pv. syringae strains UMAF0158 and UMAF0273) and 96.90%, respectively. P. syringae pv. syringae HS191 showed the highest ANI value in comparison with all the P. syringae pv. syringae strains, reaching values in all cases higher than 95%.The increase of genomic data of P. syringae pv. syringae strains from mango provides a comprehensive overview of the genomic landscape of this specific phylotype, providing important clues to understanding the evolution of molecular mechanisms, especially with respect to their specific virulence and adaptation features. Understanding in depth this genomic information will provide an advantage in the fight against bacterial phytopathogens, improving disease management strategies.Data AvailabilityThe draft genome sequences are deposited in the NCBI GenBank database under BioProject PRJNA786963. 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Nucleic Acids Res. 49:D651-D659. https://doi.org/10.1093/nar/gkaa899 Crossref, Medline, ISI, Google ScholarFunding: This work was supported by grants from CICE-Junta de Andalucía, Proyecto de Excelencia (P12-AGR-1473) from Junta de Andalucía, Proyecto Spanish Plan Nacional I+D+I (AGL2017-83368-C2-1-R) and Proyecto UMA18-FEDERJA-046, all cofinanced by FEDER grants.The author(s) declare no conflict of interest. Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.DetailsFiguresLiterature CitedRelated Vol. 35, No. 12 December 2022ISSN:0894-0282e-ISSN:1943-7706 Download Metrics Article History Issue Date: 19 Dec 2022Published: 12 Dec 2022Accepted: 30 Aug 2022 Pages: 1109-1114 InformationCopyright © 2022 The Author(s).This is an open access article distributed under the CC BY-NC-ND 4.0 International license.Funding CICE-Junta de Andalucía, Proyecto de ExcelenciaGrant/Award Number: P12-AGR-1473 Junta de Andalucía, Proyecto Spanish Plan Nacional I+D+IGrant/Award Number: AGL2017-83368-C2-1-R Junta de Andalucía, ProyectoGrant/Award Number: UMA18-FEDERJA-046 Keywordsexopolysaccharidesgenomicsmango treesPseudomonas syringae pv. syringaevirulence associated genesThe author(s) declare no conflict of interest.PDF download