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.
Highlights
To penetrate the cuticle and cell wall of their hosts, most plant pathogenic fungi differentiate specialized infection structures called appressoria
Consecutive waves of effector gene expression were associated with key developmental transitions, indicating that distinct suites of effectors are deployed at each infection stage
We add another level of functional complexity to this highly elaborated infection structure that has not been reported previously, namely the local release of effector proteins at a nanoscale interface formed between host and pathogen, defined by the basal penetration pore
Summary
To penetrate the cuticle and cell wall of their hosts, most plant pathogenic fungi differentiate specialized infection structures called appressoria. The appressoria of Colletotrichum and Magnaporthe species display a complex physiology and morphology, adapted for efficient host cell entry. Key features are (a) a melanized cell wall acting as a semipermeable barrier to osmolytes, (b) glycerol accumulation for generating turgor and (c) an extracellular matrix to anchor the cell and counter-balance downward mechanical forces applied during penetration [2]. The appressoria of Colletotrichum and Magnaporthe are highly polarized cells with an upper domed region and a basal region containing the penetration pore, from which a needle-like penetration hypha emerges to puncture the epidermal cell wall [3,4]. Whether appressoria actively manipulate the attacked cell in preparation for invasion is currently unknown
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