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Review
. 2016 Aug 4:54:419-41.
doi: 10.1146/annurev-phyto-080615-100204. Epub 2016 Jan 17.

Plant-Pathogen Effectors: Cellular Probes Interfering with Plant Defenses in Spatial and Temporal Manners

Affiliations
Review

Plant-Pathogen Effectors: Cellular Probes Interfering with Plant Defenses in Spatial and Temporal Manners

Tania Y Toruño et al. Annu Rev Phytopathol. .

Abstract

Plants possess large arsenals of immune receptors capable of recognizing all pathogen classes. To cause disease, pathogenic organisms must be able to overcome physical barriers, suppress or evade immune perception, and derive nutrients from host tissues. Consequently, to facilitate some of these processes, pathogens secrete effector proteins that promote colonization. This review covers recent advances in the field of effector biology, focusing on conserved cellular processes targeted by effectors from diverse pathogens. The ability of effectors to facilitate pathogen entry into the host interior, suppress plant immune perception, and alter host physiology for pathogen benefit is discussed. Pathogens also deploy effectors in a spatial and temporal manner, depending on infection stage. Recent advances have also enhanced our understanding of effectors acting in specific plant organs and tissues. Effectors are excellent cellular probes that facilitate insight into biological processes as well as key points of vulnerability in plant immune signaling networks.

Keywords: apoplastic effectors; effector timing; immunity; intracellular effectors; pathogen.

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Figures

Figure 1
Figure 1
The battle in the apoplast between plants and pathogens. Filamentous pathogens secrete multiple effectors to interfere with host immunity. The Cladosporium fulvum Avr4 effector shields and masks chitin present in the fungal cell walls from tomato chitinases during infection. The Avr2 effector binds to and inhibits tomato apoplastic proteases such as Rcr3 and PiP1. The plant-parasitic nematode Globodera rostochiensis secretes the VAP1 effector that blocks Rcr3’s active site. The Phytophthora infestans EPIC1 and EPIC2B effectors also inhibit apoplastic proteases. Perception of apoplastic effectors can be mediated by receptor-like proteins (RLPs). Avr2 results in a conformational change in Rcr3, which is perceived by the cognate tomato Cf-2 RLP. Perception of Avr4 by the tomato RLP Cf-4 is hypothesized to occur through direct effector binding. The LysM-domain containing effector Ecp6 interferes with host immunity by sequestering short chito-oligosaccharides that could be released by the fungus. Such short chito-oligosaccharides, usually six to eight oligomers in length [(GlcNAc)6–8], act as PAMPs (pathogen-associated molecular patterns) and are perceived by plant LsyM domain–containing immune receptors, including Arabidopsis thaliana CERK1 and LYK5, a receptor-like kinases (RLKs), and the Oryza sativa CEBiP. Cyst nematodes secrete effectors mimicking plant CLE (CLAVATA3/endosperm surrounding region-related) peptide hormones, which are perceived by CLAVATA RLKs. CLAVATA RLKs regulate stem cell maintenance, and it is hypothesized that nematode CLE effectors act to inhibit cell division to promote syncytium development. Not to scale.
Figure 2
Figure 2
Waves of effector expression over time and pathogen type. Plant pathogens range from obligate biotrophs with narrow host ranges to hemibiotrophs and necrotrophs with broad host ranges. Effector expression patterns change over the course of infection and type of tissue infected. Obligate biotrophs secrete effectors that act to suppress immune recognition and promote cell survival. Hemibiotrophs initially secrete effectors promoting cell survival, but during later stages of infection secrete cell death–promoting effectors. Necrotrophic pathogens can also secrete effectors promoting cell survival during very early infection stages but predominantly secrete cell death–promoting effectors to facilitate colonization.
Figure 3
Figure 3
Pathogen effectors manipulate host gene transcription. Bacterial effectors are depicted in blue, effectors from filamentous pathogens are depicted in red, and viral effectors are depicted in purple. Transcriptional activator-like effectors (TALEs) from Xanthomonas and Ralstonia bacterial pathogens are secreted through the type III secretion system (T3SS) into host cells. TALEs bind to promoter regions of target genes to activate transcription of susceptibility (S) genes and promote virulence. However, some plant genotypes possess resistance (R) genes with TALE-binding promoter regions and act as decoys to activate immune responses. The bacterial pathogen Pseudomonas syringae delivers the T3SS effector HopU1 (blue circle) that targets the RNA-binding protein GRP7. HopU1 interferes with GRP7’s ability to bind messenger RNAs, including immunity-related RNAs. Phytoplasmas are insect-transmitted, phloem-limited bacterial pathogens that secrete SAP effectors (blue star). SAP effectors are able to move throughout the plant via plasmodesmata, and some, such as SAP11 and SAP54, manipulate host transcription factors to induce plant developmental changes favoring insect colonization. Filamentous pathogens (oomycetes and fungi) as well as viruses deliver effectors to suppress plant RNA silencing and thus interfere with plant transcription factors and promote virulence. Botrytis cinerea is able to deliver fungal small RNAs into the host cells that suppress gene expression (red line).

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