TY - JOUR

T1 - Interaction of roses with a biotrophic and a hemibiotrophic leaf pathogen leads to differences in defense transcriptome activation

AU - Neu, Enzo

AU - Domes, Helena Sophia

AU - Menz, Ina

AU - Kaufmann, Helgard

AU - Linde, Marcus

AU - Debener, Thomas

N1 - Funding Information: Funding This work was funded by the DFG GRK 1798 “Signaling at the Plant-Soil Interface” (GRK1798/1).

PY - 2019/3/1

Y1 - 2019/3/1

N2 - KEY MESSAGE: 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.

AB - KEY MESSAGE: 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.

KW - Black spot

KW - High-throughput qPCR

KW - MACE analysis

KW - Powdery mildew

KW - PR genes

KW - WRKY genes

KW - Pathogen-Associated Molecular Pattern Molecules/metabolism

KW - Gene Expression Profiling

KW - Immunity

KW - Gene Expression Regulation, Plant/genetics

KW - Genes, Plant/genetics

KW - Arabidopsis Proteins

KW - Salicylic Acid

KW - Rosa/genetics

KW - Host-Pathogen Interactions/genetics

KW - Chitinases/genetics

KW - Plant Diseases/genetics

KW - Plant Growth Regulators/genetics

KW - Signal Transduction/genetics

KW - Transcription Factors/genetics

KW - Transcriptome/genetics

KW - Ascomycota/pathogenicity

KW - Plant Proteins/genetics

KW - Flavonoids/metabolism

KW - High-Throughput Nucleotide Sequencing

KW - Plant Leaves/genetics

UR - http://www.scopus.com/inward/record.url?scp=85061005574&partnerID=8YFLogxK

U2 - 10.1007/s11103-018-00818-2

DO - 10.1007/s11103-018-00818-2

M3 - Article

C2 - 30706286

AN - SCOPUS:85061005574

VL - 99

SP - 299

EP - 316

JO - Plant molecular biology

JF - Plant molecular biology

SN - 0167-4412

IS - 4-5

ER -