Abstract

Key messageTranscriptomic 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.

Highlights

  • Fungal pathogens have developed specific strategies to obtain nutrients from their hosts depending on their lifestyle

  • To characterize the specific infection strategies based on the resulting transcriptomic changes in the early stages of infection with the hemibiotrophic D. rosae and the obligate biotrophic P. pannosa, we used next-generation sequencing based on the massive analysis of cDNA ends (MACE) approach

  • With this first analysis of the rose defense transcriptome, we showed contrasting responses of the host to two fungal pathogens, the hemibiotrophic D. rosae and the biotrophic P. pannosa displaying different lifestyles

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Summary

Introduction

Fungal pathogens have developed specific strategies to obtain nutrients from their hosts depending on their lifestyle. Necrotrophic fungi kill the host cells, often by secreting toxins, to feed on the dead tissue, while hemibiotrophic pathogens often change their lifestyle during development from an early biotrophic to a later necrotrophic stage (Horbach et al 2011). In their natural environment, roses are confronted with many different pathogens. After an additional 3 h, subcuticular hyphae and the first haustoria may be developed (Aronescu 1934) In this biotrophic phase, all the fungal structures in the host cells are surrounded by the plasma membrane of the host. Asexually produced spores are released after 3–5 days, completing the life cycle on the living host tissue (Coyier 1983)

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