Plants use autophagy to safeguard against infectious diseases. However, how plant pathogens interfere with autophagy-related processes is unknown. Here, we show that PexRD54, an effector from the Irish potato famine pathogen Phytophthora infestans, binds host autophagy protein ATG8CL to stimulate autophagosome formation. PexRD54 depletes the autophagy cargo receptor Joka2 out of ATG8CL complexes and interferes with Joka2's positive effect on pathogen defense. Thus, a plant pathogen effector has evolved to antagonize a host autophagy cargo receptor to counteract host defenses.DOI: http://dx.doi.org/10.7554/eLife.10856.001

No abstract

The rice blast fungus Magnaporthe oryzae causes a devastating disease that threatens global rice (Oryza sativa) production. Despite intense study, the biology of plant tissue invasion during blast disease remains poorly understood. Here we report a high resolution, transcriptional profiling study of the entire plant-associated development of the blast fungus. Our analysis revealed major temporal changes in fungal gene expression during plant infection. Pathogen gene expression could be classified into 10 modules of temporally co-expressed genes, providing evidence for the induction of pronounced shifts in primary and secondary metabolism, cell signalling and transcriptional regulation. A set of 863 genes encoding secreted proteins are differentially expressed at specific stages of infection, and 546 genes named MEP (Magnaporthe  effector protein) genes were predicted to encode effectors. Computational prediction of structurally-related MEPs, including the MAX effector family, revealed their temporal co-regulation in the same co-expression modules. We characterised 32 MEP genes and demonstrate that Mep effectors are predominantly targeted to the cytoplasm of rice cells via the biotrophic interfacial complex (BIC) and use a common unconventional secretory pathway. Taken together, our study reveals major changes in gene expression associated with blast disease and identifies a diverse repertoire of effectors critical for successful infection.

Elicitins are structurally conserved extracellular proteins in Phytophthora and Pythium oomycete pathogen species. They were first described in the late 1980s as abundant proteins in Phytophthora culture filtrates that have the capacity to elicit hypersensitive (HR) cell death and disease resistance in tobacco. Later, they became well-established as having features of microbe-associated molecular patterns (MAMPs) and to elicit defences in a variety of plant species. Research on elicitins culminated in the recent cloning of the elicitin response (ELR) cell surface receptor-like protein, from the wild potato Solanum microdontum, which mediates response to a broad range of elicitins. In this review, we provide an overview on elicitins and the plant responses they elicit. We summarize the state of the art by describing what we consider to be the nine most important features of elicitin biology

ice blast disease is an important threat to global food security 1 . The disease starts when asexual spores of Magnaporthe oryzae, called conidia, land on the hydrophobic surface of a rice leaf inducing differentiation of an infection cell called an appressorium 1-3 . The appressorium develops turgor of up to 8.0 MPa due to glycerol accumulation, which generates osmotic pressure 4 . Glycerol is maintained in the appressorium by melanin in the cell wall, which reduces its porosity 4,5 . Development of the appressorium is tightly linked to the cell cycle, autophagy [6][7][8] and metabolic checkpoint control mediated by TOR kinase and the cAMP-dependent protein kinase A (PKA) pathway [9][10][11] . Appressorium turgor is monitored by a sensor kinase, Sln1, and once a threshold is reached 12 , septin GTPases in the appressorium pore form a hetero-oligomeric complex that scaffolds cortical F-actin at the base of the appressorium 13,14 . This leads to force generation to pierce the cuticle with a rigid penetration hypha. Once inside the leaf, invasive hyphae colonize the first epidermal cell before seeking out plasmodesmata-rich pit fields through which the fungus invades neighbouring cells 15 . M. oryzae actively suppresses plant immunity using fungal effector proteins delivered into plant cells 16 . After five days, disease lesions appear from which the fungus sporulates to colonize neighbouring plants.Formation of an appressorium by M. oryzae requires a conserved pathogenicity mitogen-activated protein kinase (MAPK), called Pmk1 (ref. 17 ). Pmk1 mutants cannot form appressoria or cause plant infection, even when plants are wounded 17 . Instead, Δpmk1 mutants produce undifferentiated germlings that undergo several rounds of mitosis and septation 17,18 . Pmk1 is also responsible for lipid and glycogen mobilization to the appressorium, autophagy in the conidium 4,8,19,20 and invasive cell-to-cell movement 15 . A set of pl surface sensors 21 that trigger cAMP-PKA signalling are required for Pmk1 activation 17 , and a TOR-dependent nutrient sensing pathway is necessary for appressorium formation, acting upstream, or perhaps independently, of Pmk1 (refs. [9][10][11] ). The mechanism by which Pmk1 exerts such an important role in plant infection has remained largely unknown and only one transcriptional regulator, Mst12, which may act downstream of Pmk1, has been characterized in detail. Mst12 mutants form appressoria normally but are non-functional and cannot cause disease 22 .In this study we set out to identify the mechanism by which major transcriptional changes are regulated during appressorium development by M. oryzae. We identified major temporal changes in gene expression in response to an appressorium-inductive hydrophobic

Autophagy-related protein 8 (ATG8) is a highly conserved ubiquitin-like protein that modulates autophagy pathways by binding autophagic membranes and a number of proteins, including cargo receptors and core autophagy components. Throughout plant evolution, ATG8 has expanded from a single protein in algae to multiple isoforms in higher plants. However, the degree to which ATG8 isoforms have functionally specialized to bind distinct proteins remains unclear. Here, we describe a comprehensive protein–protein interaction resource, obtained using in planta immunoprecipitation (IP) followed by mass spectrometry (MS), to define the potato ATG8 interactome. We discovered that ATG8 isoforms bind distinct sets of plant proteins with varying degrees of overlap. This prompted us to define the biochemical basis of ATG8 specialization by comparing two potato ATG8 isoforms using both in vivo protein interaction assays and in vitro quantitative binding affinity analyses. These experiments revealed that the N-terminal β-strand—and, in particular, a single amino acid polymorphism—underpins binding specificity to the substrate PexRD54 by shaping the hydrophobic pocket that accommodates this protein’s ATG8-interacting motif (AIM). Additional proteomics experiments indicated that the N-terminal β-strand shapes the broader ATG8 interactor profiles, defining interaction specificity with about 80 plant proteins. Our findings are consistent with the view that ATG8 isoforms comprise a layer of specificity in the regulation of selective autophagy pathways in plants.

No abstract

Eukaryotes contain three types of lipid kinases that belong to the phosphatidylinositol 3-kinase (PI3K) family. In plants and Saccharomyces cerevisiae, only PI3K class III family members have been identified. These enzymes regulate the innate immune response, intracellular trafficking, autophagy, and senescence. Here, we report that RNAi-mediated downregulation of common bean (Phaseolus vulgaris) PI3K severely impaired symbiosis in composite P. vulgaris plants with endosymbionts such as Rhizobium tropici and Rhizophagus irregularis. Downregulation of Pv-PI3K was associated with a marked decrease in root hair growth and curling. Additionally, infection thread growth, root-nodule number, and symbiosome formation in root nodule cells were severely affected. Interestingly, root colonization by AM fungi and the formation of arbuscules were also abolished in PI3K loss-of-function plants. Furthermore, the transcript accumulation of genes encoding proteins known to interact with PI3K to form protein complexes involved in autophagy was drastically reduced in these transgenic roots. RNAimediated downregulation of one of these genes, Beclin1/Atg6, resulted in a similar phenotype as observed for transgenic roots in which Pv-PI3K had been downregulated. Our findings show that an autophagy-related process is crucial for the mutualistic interactions of P. vulgaris with beneficial microorganisms.