Abstract
Summary The potato blight pathogen Phytophthora infestans secretes effector proteins that are delivered inside (cytoplasmic) or can act outside (apoplastic) plant cells to neutralize host immunity. Little is known about how and where effectors are secreted during infection, yet such knowledge is essential to understand and combat crop disease.We used transient Agrobacterium tumefaciens‐mediated in planta expression, transformation of P. infestans with fluorescent protein fusions and confocal microscopy to investigate delivery of effectors to plant cells during infection.The cytoplasmic effector Pi04314, expressed as a monomeric red fluorescent protein (mRFP) fusion protein with a signal peptide to secrete it from plant cells, did not passively re‐enter the cells upon secretion. However, Pi04314‐mRFP expressed in P. infestans was translocated from haustoria, which form intimate interactions with plant cells, to accumulate at its sites of action in the host nucleus. The well‐characterized apoplastic effector EPIC1, a cysteine protease inhibitor, was also secreted from haustoria. EPIC1 secretion was inhibited by brefeldin A (BFA), demonstrating that it is delivered by conventional Golgi‐mediated secretion. By contrast, Pi04314 secretion was insensitive to BFA treatment, indicating that the cytoplasmic effector follows an alternative route for delivery into plant cells. Phytophthora infestans haustoria are thus sites for delivery of both apoplastic and cytoplasmic effectors during infection, following distinct secretion pathways.
Highlights
IntroductionSuccessful plant pathogens secrete effector proteins that act outside (termed apoplastic effectors) or inside (cytoplasmic effectors) plant cells to suppress or otherwise manipulate host processes (Asai & Shirasu, 2015)
Successful plant pathogens secrete effector proteins that act outside or inside plant cells to suppress or otherwise manipulate host processes (Asai & Shirasu, 2015)
We used transient Agrobacterium tumefaciens-mediated in planta expression, transformation of P. infestans with fluorescent protein fusions and confocal microscopy to investigate delivery of effectors to plant cells during infection
Summary
Successful plant pathogens secrete effector proteins that act outside (termed apoplastic effectors) or inside (cytoplasmic effectors) plant cells to suppress or otherwise manipulate host processes (Asai & Shirasu, 2015). Bacterial plant pathogens use a variety of secretion systems to deliver effectors. Filamentous (fungal and oomycete) plant pathogens secrete effectors that act inside or outside of host cells. Fungal effector research has historically been driven by the search for avirulence proteins, which are detected by matching plant resistance proteins. Such effectors include the Cladosporium fulvum Avirulence 2 (Avr2), Avr and Avr proteins, which are predicted apoplastic effectors that are detected by cell surface C. fulvum (Cf) resistance proteins (de Wit, 2016). Avirulences characterized in the rice blast pathogen Magnaporthe oryzae (Jia et al, 2000) and the flax rust pathogen Melampsora lini (Dodds et al, 2004) are generally cytoplasmic effectors detected by plant nucleotide-binding leucine-rich repeat (NB-LRR) resistance proteins. Avirulence proteins have yet to be characterized in the maize (Zea mays) pathogen Ustilago maydis, this fungus secretes both apoplastic (e.g. Mueller et al, 2013) and cytoplasmic (e.g. Tanaka et al, 2014) effectors to suppress plant defences
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