Variable Suites of Non-effector Genes Are Co-regulated in the Type III Secretion Virulence Regulon across the Pseudomonas syringae Phylogeny

Tatiana S. Mucyn, Scott Yourstone, Abigail L. Lind, Surojit Biswas, Marc T. Nishimura, David A Baltrus, Jason S. Cumbie, Jeff H. Chang, Corbin D. Jones, Jeffery L. Dangl, Sarah R. Grant

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

Pseudomonas syringae is a phylogenetically diverse species of Gram-negative bacterial plant pathogens responsible for crop diseases around the world. The HrpL sigma factor drives expression of the major P. syringae virulence regulon. HrpL controls expression of the genes encoding the structural and functional components of the type III secretion system (T3SS) and the type three secreted effector proteins (T3E) that are collectively essential for virulence. HrpL also regulates expression of an under-explored suite of non-type III effector genes (non-T3E), including toxin production systems and operons not previously associated with virulence. We implemented and refined genome-wide transcriptional analysis methods using cDNA-derived high-throughput sequencing (RNA-seq) data to characterize the HrpL regulon from six isolates of P. syringae spanning the diversity of the species. Our transcriptomes, mapped onto both complete and draft genomes, significantly extend earlier studies. We confirmed HrpL-regulation for a majority of previously defined T3E genes in these six strains. We identified two new T3E families from P. syringae pv. oryzae 1_6, a strain within the relatively underexplored phylogenetic Multi-Locus Sequence Typing (MLST) group IV. The HrpL regulons varied among strains in gene number and content across both their T3E and non-T3E gene suites. Strains within MLST group II consistently express the lowest number of HrpL-regulated genes. We identified events leading to recruitment into, and loss from, the HrpL regulon. These included gene gain and loss, and loss of HrpL regulation caused by group-specific cis element mutations in otherwise conserved genes. Novel non-T3E HrpL-regulated genes include an operon that we show is required for full virulence of P. syringae pv. phaseolicola 1448A on French bean. We highlight the power of integrating genomic, transcriptomic, and phylogenetic information to drive concise functional experimentation and to derive better insight into the evolution of virulence across an evolutionarily diverse pathogen species.

Original languageEnglish (US)
Article numbere1003807
JournalPLoS Pathogens
Volume10
Issue number1
DOIs
StatePublished - Jan 2014

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Pseudomonas syringae
Regulon
Phylogeny
Virulence
Genes
Operon
Genome
Sigma Factor
High-Throughput Nucleotide Sequencing
Transcriptome
Complementary DNA
Gene Expression
Mutation

ASJC Scopus subject areas

  • Microbiology
  • Parasitology
  • Virology
  • Immunology
  • Genetics
  • Molecular Biology
  • Medicine(all)

Cite this

Variable Suites of Non-effector Genes Are Co-regulated in the Type III Secretion Virulence Regulon across the Pseudomonas syringae Phylogeny. / Mucyn, Tatiana S.; Yourstone, Scott; Lind, Abigail L.; Biswas, Surojit; Nishimura, Marc T.; Baltrus, David A; Cumbie, Jason S.; Chang, Jeff H.; Jones, Corbin D.; Dangl, Jeffery L.; Grant, Sarah R.

In: PLoS Pathogens, Vol. 10, No. 1, e1003807, 01.2014.

Research output: Contribution to journalArticle

Mucyn, TS, Yourstone, S, Lind, AL, Biswas, S, Nishimura, MT, Baltrus, DA, Cumbie, JS, Chang, JH, Jones, CD, Dangl, JL & Grant, SR 2014, 'Variable Suites of Non-effector Genes Are Co-regulated in the Type III Secretion Virulence Regulon across the Pseudomonas syringae Phylogeny', PLoS Pathogens, vol. 10, no. 1, e1003807. https://doi.org/10.1371/journal.ppat.1003807
Mucyn, Tatiana S. ; Yourstone, Scott ; Lind, Abigail L. ; Biswas, Surojit ; Nishimura, Marc T. ; Baltrus, David A ; Cumbie, Jason S. ; Chang, Jeff H. ; Jones, Corbin D. ; Dangl, Jeffery L. ; Grant, Sarah R. / Variable Suites of Non-effector Genes Are Co-regulated in the Type III Secretion Virulence Regulon across the Pseudomonas syringae Phylogeny. In: PLoS Pathogens. 2014 ; Vol. 10, No. 1.
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abstract = "Pseudomonas syringae is a phylogenetically diverse species of Gram-negative bacterial plant pathogens responsible for crop diseases around the world. The HrpL sigma factor drives expression of the major P. syringae virulence regulon. HrpL controls expression of the genes encoding the structural and functional components of the type III secretion system (T3SS) and the type three secreted effector proteins (T3E) that are collectively essential for virulence. HrpL also regulates expression of an under-explored suite of non-type III effector genes (non-T3E), including toxin production systems and operons not previously associated with virulence. We implemented and refined genome-wide transcriptional analysis methods using cDNA-derived high-throughput sequencing (RNA-seq) data to characterize the HrpL regulon from six isolates of P. syringae spanning the diversity of the species. Our transcriptomes, mapped onto both complete and draft genomes, significantly extend earlier studies. We confirmed HrpL-regulation for a majority of previously defined T3E genes in these six strains. We identified two new T3E families from P. syringae pv. oryzae 1_6, a strain within the relatively underexplored phylogenetic Multi-Locus Sequence Typing (MLST) group IV. The HrpL regulons varied among strains in gene number and content across both their T3E and non-T3E gene suites. Strains within MLST group II consistently express the lowest number of HrpL-regulated genes. We identified events leading to recruitment into, and loss from, the HrpL regulon. These included gene gain and loss, and loss of HrpL regulation caused by group-specific cis element mutations in otherwise conserved genes. Novel non-T3E HrpL-regulated genes include an operon that we show is required for full virulence of P. syringae pv. phaseolicola 1448A on French bean. We highlight the power of integrating genomic, transcriptomic, and phylogenetic information to drive concise functional experimentation and to derive better insight into the evolution of virulence across an evolutionarily diverse pathogen species.",
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