Interaction of roses with a biotrophic and a hemibiotrophic leaf pathogen leads to differences in defense transcriptome activation

Plant Mol Biol. 2019 Mar;99(4-5):299-316. doi: 10.1007/s11103-018-00818-2. Epub 2019 Jan 31.

Abstract

Transcriptomic analysis resulted in the upregulation of the genes related to common defense mechanisms for black spot and the downregulation of the genes related to photosynthesis and cell wall modification for powdery mildew. Plant pathogenic fungi successfully colonize their hosts by manipulating the host defense mechanisms, which is accompanied by major transcriptome changes in the host. To characterize compatible plant pathogen interactions at early stages of infection by the obligate biotrophic fungus Podosphaera pannosa, which causes powdery mildew, and the hemibiotrophic fungus Diplocarpon rosae, which causes black spot, we analyzed changes in the leaf transcriptome after the inoculation of detached rose leaves with each pathogen. In addition, we analyzed differences in the transcriptomic changes inflicted by both pathogens as a first step to characterize specific infection strategies. Transcriptomic changes were analyzed using next-generation sequencing based on the massive analysis of cDNA ends approach, which was validated using high-throughput qPCR. We identified a large number of differentially regulated genes. A common set of the differentially regulated genes comprised of pathogenesis-related (PR) genes, such as of PR10 homologs, chitinases and defense-related transcription factors, such as various WRKY genes, indicating a conserved but insufficient PTI [pathogen associated molecular pattern (PAMP) triggered immunity] reaction. Surprisingly, most of the differentially regulated genes were specific to the interactions with either P. pannosa or D. rosae. Specific regulation in response to D. rosae was detected for genes from the phenylpropanoid and flavonoid pathways and for individual PR genes, such as paralogs of PR1 and PR5, and other factors of the salicylic acid signaling pathway. Differently, inoculation with P. pannosa leads in addition to the general pathogen response to a downregulation of genes related to photosynthesis and cell wall modification.

Keywords: Black spot; High-throughput qPCR; MACE analysis; PR genes; Powdery mildew; WRKY genes.

MeSH terms

  • Arabidopsis Proteins
  • Ascomycota / pathogenicity
  • Chitinases / genetics
  • Flavonoids / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / immunology
  • Genes, Plant / genetics
  • Genes, Plant / immunology
  • High-Throughput Nucleotide Sequencing
  • Host-Pathogen Interactions / genetics
  • Host-Pathogen Interactions / immunology
  • Immunity
  • Pathogen-Associated Molecular Pattern Molecules / metabolism
  • Plant Diseases / genetics*
  • Plant Diseases / immunology
  • Plant Diseases / microbiology*
  • Plant Growth Regulators / genetics
  • Plant Growth Regulators / immunology
  • Plant Leaves / genetics*
  • Plant Leaves / immunology*
  • Plant Leaves / metabolism
  • Plant Leaves / microbiology
  • Plant Proteins / genetics
  • Plant Proteins / immunology
  • Rosa / genetics*
  • Rosa / immunology*
  • Rosa / metabolism
  • Salicylic Acid
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • Transcription Factors / genetics
  • Transcription Factors / immunology
  • Transcriptome / genetics*
  • Transcriptome / immunology*

Substances

  • Arabidopsis Proteins
  • Flavonoids
  • Pathogen-Associated Molecular Pattern Molecules
  • Plant Growth Regulators
  • Plant Proteins
  • Transcription Factors
  • WRKY57 protein, Arabidopsis
  • Chitinases
  • Salicylic Acid