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Article ; Online: Exploring the Emergence and Evolution of Plant Pathogenic Microbes Using Historical and Paleontological Sources.

Malmstrom, Carolyn M / Martin, Michael D / Gagnevin, Lionel

2022 Volume 60, Page(s) 187–209

Abstract: Biotechnological advances now permit broad exploration of past microbial communities preserved in diverse substrates. Despite biomolecular degradation, high-throughput sequencing of preserved materials can yield invaluable genomic and metagenomic data ... ...

Abstract	Biotechnological advances now permit broad exploration of past microbial communities preserved in diverse substrates. Despite biomolecular degradation, high-throughput sequencing of preserved materials can yield invaluable genomic and metagenomic data from the past. This line of research has expanded from its initial human- and animal-centric foci to include plant-associated microbes (viruses, archaea, bacteria, fungi, and oomycetes), for which historical, archaeological, and paleontological data illuminate past epidemics and evolutionary history. Genetic mechanisms underlying the acquisition of microbial pathogenicity, including hybridization, polyploidization, and horizontal gene transfer, can now be reconstructed, as can gene-for-gene coevolution with plant hosts. Epidemiological parameters, such as geographic origin and range expansion, can also be assessed. Building on published case studies with individual phytomicrobial taxa, the stage is now set for broader, community-wide studies of preserved plant microbiomes to strengthen mechanistic understanding of microbial interactions and plant disease emergence.
MeSH term(s)	Animals ; Archaea ; Bacteria ; Fungi ; Humans ; Microbiota ; Plants
Language	English
Publishing date	2022-04-28
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	207934-3
ISSN	1545-2107 ; 0066-4286
ISSN (online)	1545-2107
ISSN	0066-4286
DOI	10.1146/annurev-phyto-021021-041830
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Article: Epidemiology and Control of Mango Bacterial Black Spot.

Gagnevin, Lionel / Pruvost, Olivier

Plant disease

2019 Volume 85, Issue 9, Page(s) 928–935

Language	English
Publishing date	2019-03-01
Publishing country	United States
Document type	Journal Article
ZDB-ID	754182-x
ISSN	0191-2917
ISSN	0191-2917
DOI	10.1094/PDIS.2001.85.9.928
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Article ; Online: Herbarium specimen sequencing allows precise dating of Xanthomonas citri pv. citri diversification history.

Campos, Paola E / Pruvost, Olivier / Boyer, Karine / Chiroleu, Frederic / Cao, Thuy Trang / Gaudeul, Myriam / Baider, Cláudia / Utteridge, Timothy M A / Becker, Nathalie / Rieux, Adrien / Gagnevin, Lionel

Nature communications

2023 Volume 14, Issue 1, Page(s) 4306

Abstract: Herbarium collections are an important source of dated, identified and preserved DNA, whose use in comparative genomics and phylogeography can shed light on the emergence and evolutionary history of plant pathogens. Here, we reconstruct 13 historical ... ...

Abstract	Herbarium collections are an important source of dated, identified and preserved DNA, whose use in comparative genomics and phylogeography can shed light on the emergence and evolutionary history of plant pathogens. Here, we reconstruct 13 historical genomes of the bacterial crop pathogen Xanthomonas citri pv. citri (Xci) from infected Citrus herbarium specimens. Following authentication based on ancient DNA damage patterns, we compare them with a large set of modern genomes to estimate their phylogenetic relationships, pathogenicity-associated gene content and several evolutionary parameters. Our results indicate that Xci originated in Southern Asia ~11,500 years ago (perhaps in relation to Neolithic climate change and the development of agriculture) and diversified during the beginning of the 13th century, after Citrus diversification and before spreading to the rest of the world (probably via human-driven expansion of citriculture through early East-West trade and colonization).
MeSH term(s)	Humans ; Phylogeny ; Xanthomonas/genetics ; Genomics ; Citrus/microbiology ; Plant Diseases/microbiology
Language	English
Publishing date	2023-07-20
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-39950-z
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Article ; Online: CRISPRi in Xanthomonas demonstrates functional convergence of transcription activator‐like effectors in two divergent pathogens

Zárate‐Chaves, Carlos Andrés / Audran, Corinne / Medina Culma, César Augusto / Escalon, Aline / Javegny, Stéphanie / Gagnevin, Lionel / Thomas, Emilie / Pimparé, Léa‐Lou / López, Camilo E. / Jacobs, Jonathan M. / Noël, Laurent D. / Koebnik, Ralf / Bernal, Adriana Jimena / Szurek, Boris

New Phytologist. 2023 May, v. 238, no. 4 p.1593-1604

2023

Abstract: Functional analysis of large gene families in plant pathogens can be cumbersome using classical insertional mutagenesis. Additionally, Cas9 toxicity has limited the application of CRISPR–Cas9 for directed mutagenesis in bacteria. Here, we successfully ... ...

Abstract	Functional analysis of large gene families in plant pathogens can be cumbersome using classical insertional mutagenesis. Additionally, Cas9 toxicity has limited the application of CRISPR–Cas9 for directed mutagenesis in bacteria. Here, we successfully applied a CRISPR interference strategy to investigate the cryptic role of the transcription activator‐like effector (tale) multigene family in several plant‐pathogenic Xanthomonas bacterial species, owing to their contribution to pathogen virulence. Single guide RNAs (sgRNAs) designed against Xanthomonas phaseoli pv manihotis tale conserved gene sequences efficiently silenced expression of all tales, with concomitant decrease in virulence and TALE‐induced host gene expression. The system is readily translatable to other Xanthomonas species infecting rice, citrus, Brassica, and cassava, silencing up to 16 tales in a given strain using a single sgRNA. Complementation with plasmid‐borne designer tales lacking the sgRNA‐targeted sequence restored molecular and virulence phenotypes in all pathosystems. Our results evidenced that X. campestris pv campestris CN08 tales are relevant for symptom development in cauliflower. They also show that the MeSWEET10a sugar transporter is surprisingly targeted by the nonvascular cassava pathogen X. cassavae, highlighting a new example of TALE functional convergence between phylogenetically distant Xanthomonas. Overall, this novel technology provides a platform for discovery and rapid functional understanding of highly conserved gene families.
Keywords	Brassica ; CRISPR-Cas systems ; Citrus ; Xanthomonas campestris pv. phaseoli ; cassava ; cauliflower ; gene expression ; insertional mutagenesis ; multigene family ; pathogens ; phylogeny ; rice ; sugars ; technology ; toxicity ; virulence
Language	English
Dates of publication	2023-05
Size	p. 1593-1604.
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18808
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: CRISPRi in Xanthomonas demonstrates functional convergence of transcription activator-like effectors in two divergent pathogens.

Zárate-Chaves, Carlos Andrés / Audran, Corinne / Medina Culma, César Augusto / Escalon, Aline / Javegny, Stéphanie / Gagnevin, Lionel / Thomas, Emilie / Pimparé, Léa-Lou / López, Camilo E / Jacobs, Jonathan M / Noël, Laurent D / Koebnik, Ralf / Bernal, Adriana Jimena / Szurek, Boris

The New phytologist

2023 Volume 238, Issue 4, Page(s) 1593–1604

Abstract: Functional analysis of large gene families in plant pathogens can be cumbersome using classical insertional mutagenesis. Additionally, Cas9 toxicity has limited the application of CRISPR-Cas9 for directed mutagenesis in bacteria. Here, we successfully ... ...

Abstract	Functional analysis of large gene families in plant pathogens can be cumbersome using classical insertional mutagenesis. Additionally, Cas9 toxicity has limited the application of CRISPR-Cas9 for directed mutagenesis in bacteria. Here, we successfully applied a CRISPR interference strategy to investigate the cryptic role of the transcription activator-like effector (tale) multigene family in several plant-pathogenic Xanthomonas bacterial species, owing to their contribution to pathogen virulence. Single guide RNAs (sgRNAs) designed against Xanthomonas phaseoli pv manihotis tale conserved gene sequences efficiently silenced expression of all tales, with concomitant decrease in virulence and TALE-induced host gene expression. The system is readily translatable to other Xanthomonas species infecting rice, citrus, Brassica, and cassava, silencing up to 16 tales in a given strain using a single sgRNA. Complementation with plasmid-borne designer tales lacking the sgRNA-targeted sequence restored molecular and virulence phenotypes in all pathosystems. Our results evidenced that X. campestris pv campestris CN08 tales are relevant for symptom development in cauliflower. They also show that the MeSWEET10a sugar transporter is surprisingly targeted by the nonvascular cassava pathogen X. cassavae, highlighting a new example of TALE functional convergence between phylogenetically distant Xanthomonas. Overall, this novel technology provides a platform for discovery and rapid functional understanding of highly conserved gene families.
MeSH term(s)	Transcription Activator-Like Effectors/genetics ; Xanthomonas/genetics ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Virulence/genetics ; Biological Transport ; Plant Diseases/microbiology ; Oryza/genetics
Chemical Substances	Transcription Activator-Like Effectors ; Bacterial Proteins
Language	English
Publishing date	2023-03-14
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18808
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Article ; Online: First historical genome of a crop bacterial pathogen from herbarium specimen: Insights into citrus canker emergence.

Campos, Paola E / Groot Crego, Clara / Boyer, Karine / Gaudeul, Myriam / Baider, Claudia / Richard, Damien / Pruvost, Olivier / Roumagnac, Philippe / Szurek, Boris / Becker, Nathalie / Gagnevin, Lionel / Rieux, Adrien

PLoS pathogens

2021 Volume 17, Issue 7, Page(s) e1009714

Abstract: Over the past decade, ancient genomics has been used in the study of various pathogens. In this context, herbarium specimens provide a precious source of dated and preserved DNA material, enabling a better understanding of plant disease emergences and ... ...

Abstract	Over the past decade, ancient genomics has been used in the study of various pathogens. In this context, herbarium specimens provide a precious source of dated and preserved DNA material, enabling a better understanding of plant disease emergences and pathogen evolutionary history. We report here the first historical genome of a crop bacterial pathogen, Xanthomonas citri pv. citri (Xci), obtained from an infected herbarium specimen dating back to 1937. Comparing the 1937 genome within a large set of modern genomes, we reconstructed their phylogenetic relationships and estimated evolutionary parameters using Bayesian tip-calibration inferences. The arrival of Xci in the South West Indian Ocean islands was dated to the 19th century, probably linked to human migrations following slavery abolishment. We also assessed the metagenomic community of the herbarium specimen, showed its authenticity using DNA damage patterns, and investigated its genomic features including functional SNPs and gene content, with a focus on virulence factors.
MeSH term(s)	Citrus/microbiology ; Genome, Bacterial ; History, 20th Century ; Mauritius ; Phylogeny ; Plant Diseases/genetics ; Plant Diseases/history ; Plant Diseases/microbiology ; Xanthomonas/genetics
Language	English
Publishing date	2021-07-29
Publishing country	United States
Document type	Historical Article ; Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1009714
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Article ; Online: Development and comparative validation of genomic-driven PCR-based assays to detect Xanthomonas citri pv. citri in citrus plants.

Robène, Isabelle / Maillot-Lebon, Véronique / Chabirand, Aude / Moreau, Aurélie / Becker, Nathalie / Moumène, Amal / Rieux, Adrien / Campos, Paola / Gagnevin, Lionel / Gaudeul, Myriam / Baider, Claudia / Chiroleu, Fréderic / Pruvost, Olivier

BMC microbiology

2020 Volume 20, Issue 1, Page(s) 296

Abstract: Background: Asiatic Citrus Canker, caused by Xanthomonas citri pv. citri, severely impacts citrus production worldwide and hampers international trade. Considerable regulatory procedures have been implemented to prevent the introduction and ... ...

Abstract	Background: Asiatic Citrus Canker, caused by Xanthomonas citri pv. citri, severely impacts citrus production worldwide and hampers international trade. Considerable regulatory procedures have been implemented to prevent the introduction and establishment of X. citri pv. citri into areas where it is not present. The effectiveness of this surveillance largely relies on the availability of specific and sensitive detection protocols. Although several PCR- or real-time PCR-based methods are available, most of them showed analytical specificity issues. Therefore, we developed new conventional and real-time quantitative PCR assays, which target a region identified by comparative genomic analyses, and compared them to existing protocols. Results: Our assays target the X. citri pv. citri XAC1051 gene that encodes for a putative transmembrane protein. The real-time PCR assay includes an internal plant control (5.8S rDNA) for validating the assay in the absence of target amplification. A receiver-operating characteristic approach was used in order to determine a reliable cycle cut-off for providing accurate qualitative results. Repeatability, reproducibility and transferability between real-time devices were demonstrated for this duplex qPCR assay (XAC1051-2qPCR). When challenged with an extensive collection of target and non-target strains, both assays displayed a high analytical sensitivity and specificity performance: LOD Conclusions: We developed new valuable detection assays useful for routine diagnostics and surveillance of X. citri pv. citri in citrus material. Their reliability was evidenced through numerous trials on a wide range of bacterial strains and plant samples. Successful detection of the pathogen was achieved from both artificially and naturally infected plants, as well as from citrus herbarium samples, suggesting that these assays will have positive impact both for future applied and academic research on this bacterium.
MeSH term(s)	Bacterial Proteins/genetics ; Bacterial Typing Techniques ; Benchmarking ; Citrus/microbiology ; DNA, Bacterial/genetics ; Gene Expression ; Humans ; Membrane Proteins/genetics ; Plant Diseases/microbiology ; ROC Curve ; Real-Time Polymerase Chain Reaction/methods ; Real-Time Polymerase Chain Reaction/standards ; Reproducibility of Results ; Xanthomonas/genetics ; Xanthomonas/isolation & purification
Chemical Substances	Bacterial Proteins ; DNA, Bacterial ; Membrane Proteins
Language	English
Publishing date	2020-10-01
Publishing country	England
Document type	Comparative Study ; Journal Article ; Research Support, Non-U.S. Gov't ; Validation Study
ISSN	1471-2180
ISSN (online)	1471-2180
DOI	10.1186/s12866-020-01972-8
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Article ; Online: CRISPR elements provide a new framework for the genealogy of the citrus canker pathogen Xanthomonas citri pv. citri.

Jeong, Kwanho / Muñoz-Bodnar, Alejandra / Arias Rojas, Nathalia / Poulin, Lucie / Rodriguez-R, Luis Miguel / Gagnevin, Lionel / Vernière, Christian / Pruvost, Olivier / Koebnik, Ralf

BMC genomics

2019 Volume 20, Issue 1, Page(s) 917

Abstract: Background: Xanthomonads are an important clade of Gram-negative bacteria infecting a plethora of economically important host plants, including citrus. Knowledge about the pathogen's diversity and population structure are prerequisite for ... ...

Abstract	Background: Xanthomonads are an important clade of Gram-negative bacteria infecting a plethora of economically important host plants, including citrus. Knowledge about the pathogen's diversity and population structure are prerequisite for epidemiological surveillance and efficient disease management. Rapidly evolving genetic loci, such as Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR), are of special interest to develop new molecular typing tools. Results: We analyzed CRISPR loci of 56 Xanthomonas citri pv. citri strains of world-wide origin, a regulated pathogen causing Asiatic citrus canker in several regions of the world. With one exception, 23 unique sequences built up the repertoire of spacers, suggesting that this set of strains originated from a common ancestor that already harbored these 23 spacers. One isolate originating from Pakistan contained a string of 14 additional, probably more recently acquired spacers indicating that this genetic lineage has or had until recently the capacity to acquire new spacers. Comparison of CRISPR arrays with previously obtained molecular typing data, such as amplified fragment length polymorphisms (AFLP), variable-number of tandem-repeats (VNTR) and genome-wide single-nucleotide polymorphisms (SNP), demonstrated that these methods reveal similar evolutionary trajectories. Notably, genome analyses allowed to generate a model for CRISPR array evolution in X. citri pv. citri, which provides a new framework for the genealogy of the citrus canker pathogen. Conclusions: CRISPR-based typing will further improve the accuracy of the genetic identification of X. citri pv. citri outbreak strains in molecular epidemiology analyses, especially when used concomitantly with another genotyping method.
MeSH term(s)	CRISPR-Associated Proteins/genetics ; Clustered Regularly Interspaced Short Palindromic Repeats ; Genotyping Techniques ; Molecular Typing/methods ; Phylogeny ; Polymerase Chain Reaction ; Xanthomonas/classification ; Xanthomonas/genetics
Chemical Substances	CRISPR-Associated Proteins
Language	English
Publishing date	2019-12-02
Publishing country	England
Document type	Journal Article
ISSN	1471-2164
ISSN (online)	1471-2164
DOI	10.1186/s12864-019-6267-z
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Article ; Online: The new IS1595 family, its relation to IS1 and the frontier between insertion sequences and transposons.

Siguier, Patricia / Gagnevin, Lionel / Chandler, Michael

Research in microbiology

2009 Volume 160, Issue 3, Page(s) 232–241

Abstract: A picture of insertion sequence (IS) diversity is emerging in which previously well-defined groups or families, while remaining tightly clustered, no longer have defined borders but tend to be joined by ISs with partially shared characteristics. This is ... ...

Abstract	A picture of insertion sequence (IS) diversity is emerging in which previously well-defined groups or families, while remaining tightly clustered, no longer have defined borders but tend to be joined by ISs with partially shared characteristics. This is to some extent due to the presence or absence of different structurally defined transposase domains (and their spacing) and sequence similarities between IS ends. A surprising result arising from the detailed analysis of ISs in various bacterial genomes is the presence of close relatives carrying passenger genes (e.g. antibiotic resistances, methyltransferases, or transcriptional regulators as well as unknown functions). This is beginning to obscure the previously defined line between ISs (no additional orfs) and transposons. We include the lowercase prefix "t" to distinguish them from classical ISs. This is illustrated here by the IS1595 family, distantly related to IS1, which can be subdivided into several groups based on BLAST analysis of transposases, the genetic organization (number and position of the orfs) and the inverted repeats at their ends. The classification was subsequently confirmed using MCL (Markov cluster algorithm) software with parameters derived from the well-defined IS3 family. Many new ISs were identified from the public databases using a reiterative BLAST approach.
MeSH term(s)	DNA Transposable Elements ; DNA, Bacterial/genetics ; Genetic Variation ; Genome, Bacterial ; Sequence Homology
Chemical Substances	DNA Transposable Elements ; DNA, Bacterial
Language	English
Publishing date	2009-04
Publishing country	France
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1004220-9
ISSN	1769-7123 ; 0923-2508
ISSN (online)	1769-7123
ISSN	0923-2508
DOI	10.1016/j.resmic.2009.02.003
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Article ; Online: Horizontal gene transfer plays a major role in the pathological convergence of Xanthomonas lineages on common bean.

Chen, Nicolas W G / Serres-Giardi, Laurana / Ruh, Mylène / Briand, Martial / Bonneau, Sophie / Darrasse, Armelle / Barbe, Valérie / Gagnevin, Lionel / Koebnik, Ralf / Jacques, Marie-Agnès

BMC genomics

2018 Volume 19, Issue 1, Page(s) 606

Abstract: Background: Host specialization is a hallmark of numerous plant pathogens including bacteria, fungi, oomycetes and viruses. Yet, the molecular and evolutionary bases of host specificity are poorly understood. In some cases, pathological convergence is ... ...

Abstract	Background: Host specialization is a hallmark of numerous plant pathogens including bacteria, fungi, oomycetes and viruses. Yet, the molecular and evolutionary bases of host specificity are poorly understood. In some cases, pathological convergence is observed for individuals belonging to distant phylogenetic clades. This is the case for Xanthomonas strains responsible for common bacterial blight of bean, spread across four genetic lineages. All the strains from these four lineages converged for pathogenicity on common bean, implying possible gene convergences and/or sharing of a common arsenal of genes conferring the ability to infect common bean. Results: To search for genes involved in common bean specificity, we used a combination of whole-genome analyses without a priori, including a genome scan based on k-mer search. Analysis of 72 genomes from a collection of Xanthomonas pathovars unveiled 115 genes bearing DNA sequences specific to strains responsible for common bacterial blight, including 20 genes located on a plasmid. Of these 115 genes, 88 were involved in successive events of horizontal gene transfers among the four genetic lineages, and 44 contained nonsynonymous polymorphisms unique to the causal agents of common bacterial blight. Conclusions: Our study revealed that host specificity of common bacterial blight agents is associated with a combination of horizontal transfers of genes, and highlights the role of plasmids in these horizontal transfers.
MeSH term(s)	Bacterial Proteins/genetics ; Gene Transfer, Horizontal ; Genome, Bacterial ; Host-Pathogen Interactions ; Phaseolus/genetics ; Phaseolus/growth & development ; Phaseolus/microbiology ; Phylogeny ; Plant Diseases/genetics ; Plant Diseases/microbiology ; Polymorphism, Single Nucleotide ; Sequence Analysis, DNA ; Virulence ; Whole Genome Sequencing ; Xanthomonas/classification ; Xanthomonas/pathogenicity
Chemical Substances	Bacterial Proteins
Language	English
Publishing date	2018-08-13
Publishing country	England
Document type	Journal Article
ZDB-ID	2041499-7
ISSN	1471-2164 ; 1471-2164
ISSN (online)	1471-2164
ISSN	1471-2164
DOI	10.1186/s12864-018-4975-4
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