Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum

Abstract

Phytopathogens secrete effector proteins to manipulate their hosts for effective colonization. Hemibiotrophic fungi must maintain host viability during initial biotrophic growth and elicit host death for subsequent necrotrophic growth. To identify effectors mediating these opposing processes, we deeply sequenced the transcriptome of Colletotrichum higginsianum infecting Arabidopsis. Most effector genes are host-induced and expressed in consecutive waves associated with pathogenic transitions, indicating distinct effector suites are deployed at each stage. Using fluorescent protein tagging and transmission electron microscopy-immunogold labelling, we found effectors localised to stage-specific compartments at the host-pathogen interface. In particular, we show effectors are focally secreted from appressorial penetration pores before host invasion, revealing new levels of functional complexity for this fungal organ. Furthermore, we demonstrate that antagonistic effectors either induce or suppress plant cell death. Based on these results we conclude that hemibiotrophy in Colletotrichum is orchestrated through the coordinated expression of antagonistic effectors supporting either cell viability or cell death.

Septin-Dependent Assembly of the Exocyst Is Essential for Plant Infection by Magnaporthe oryzae

“…Repolarization of the appressorium is therefore likely to involve remodeling of the secretory apparatus to facilitate the morphogenetic changes required for plant infection. Furthermore, fungal pathogens deliver a large repertoire of effector proteins into host plant cells, requiring rapid and focused secretion, and little is currently understood about this process (Kleemann et al, 2012;Irieda et al, 2014). We therefore characterized the exocyst complex of M. oryzae, and based on the analysis reported here, we can make three major conclusions.…”

Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses

“…One of these, the CSEP-encoding gene called ChEC6 (CH063_01084) 32 , is the most highly and significantly induced of all C. higginsianum genes (>50,000-fold) compared to appressoria in vitro. To experimentally verify this expression pattern at the cellular level, we generated transgenic C. higginsianum strains expressing a reporter gene under the control of the ChEC6 promoter (Fig.…”

Transcriptome and Metabolite Profiling of the Infection Cycle ofZymoseptoria triticion Wheat Reveals a Biphasic Interaction with Plant Immunity Involving Differential Pathogen Chromosomal Contributions and a Variation on the Hemibiotrophic Lifestyle Definition

“…RNA sequencing (RNAseq) technology has become more frequently used to profile fungal pathogen gene expression at particular phases of plant infection (de Jonge et al, 2012;Kleemann et al, 2012;O'Connell et al, 2012;Soanes et al, 2012;Cantu et al, 2013;Garnica et al, 2013;Hacquard et al, 2013;Meinhardt et al, 2014;Zhang et al, 2014). However, comparatively few studies (Kawahara et al, 2012;Yang et al, 2013;Yazawa et al, 2013) have simultaneously analyzed the responses of both pathogen and host, and very few have undertaken such an analysis throughout a complete pathogen reproductive cycle.…”