Homologous RXLR effectors from Hyaloperonospora arabidopsidis and Phytophthora sojae suppress immunity in distantly related plants

Department of Plant Pathology, Physiology and Weed Science, Virginia Tech, Blacksburg, VA, 24061-0329, USA Chemistry Research Unit, Center of Medical, Agricultural, and Veterinary Entomology, US Department of Agriculture, Agricultural Research Service, Gainesville, FL 32608, USA Virginia Bioinformatics Institute, Virginia Tech, Blacksburg, VA, 24061-0329, USA.
The Plant Journal (Impact Factor: 5.97). 06/2012; 72(6). DOI: 10.1111/j.1365-313X.2012.05079.x
Source: PubMed


Diverse pathogens secrete effector proteins into plant cells to manipulate host cellular processes. Oomycete pathogens contain large complements of predicted effector genes defined by an RXLR host cell entry motif. The genome of Hyaloperonospora arabidopsidis (Hpa, downy mildew of Arabidopsis) contains at least 134 candidate RXLR effector genes. Only a small subset of these genes is conserved in related oomycetes from the Phytophthora genus. Here, we describe a comparative functional characterization of the Hpa RXLR effector gene HaRxL96 and a homologous gene, PsAvh163, from the soybean pathogen Phytophthora sojae. HaRxL96 and PsAvh163 are induced during early stages of infection and carry a functional RXLR motif that is sufficient for protein uptake into plant cells. Both effectors can suppress immune responses in soybean. HaRxL96 suppresses immunity in Nicotiana benthamiana, while PsAvh163 induces an HR-like cell death response in Nicotiana that is dependent on RAR1 and Hsp90.1. Transgenic Arabidopsis plants expressing HaRxL96 or PsAvh163 exhibit elevated susceptibility to virulent and avirulent Hpa as well as decreased callose deposition in response to non-pathogenic P. syringae. Both effectors interfere with defense marker gene induction, but do not affect salicylic acid biosynthesis. Together, these experiments demonstrate that evolutionarily conserved effectors from different oomycete species can suppress immunity in plant species that are divergent from the source pathogen's host. © 2012 The Authors. The Plant Journal © 2012 Blackwell Publishing Ltd.

Download full-text


Available from: Devdutta Deb, Jul 28, 2015
  • Source
    • "vinifera),wehaveutilizedtransientexpressionofeffectorgenesin thenonhostspeciesN.benthamianatoexaminewhetherthese candidatePvRXLReffectorsareabletosuppressprogrammedcell death(PCD)triggeredbyectopicexpressionofeitherthemouse proapoptoticBAXproteinorthePAMPelicitorInfestans1(INF1) fromP.infestans.Thisapproachhasbeenusedsuccessfullyforthe functionalcharacterizationofanumberofoomyceteeffectorpro- teins[36] [42] [54] [57].ThetenPvRXLReffectorsselectedforfunctional testingincludedrepresentativesfromeachofthedifferentPvRXLR expressionprofilegroups(Fig.1)toinvestigateiftherewasanylink betweenthetimingofexpressionandeffectorfunction. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Plasmopara viticola is an oomycete pathogen that causes downy mildew, one of the most devastating diseases of grapevine. Currently, the molecular basis of the interaction between this pathogen and the grapevine host is not well understood. To explore the genes involved in P. viticola pathogenicity we performed RNA-Seq analysis of cDNAs derived from downy mildew-infected grapevine leaves for three different P. viticola isolates; two from China (JL-7-2, ZJ-1-1) and one from Australia (CSIRO-L-2). Approximately 30,000 unigenes were predicted for each of the three isolates and from these over 500 potential secreted proteins were identified. Using three prediction methods, a total of 51 PvRXLR effectors were identified to be present in the secretome, with at least 26 shared by two or more P. viticola isolates. Expression profiling, based on RNA-Seq data, indicated that PvRXLRs showed three different expression patterns during infection. Transient expression of selected PvRXLRs in Nicotiana benthamiana demonstrated that all were capable of suppressing programmed cell death triggered by the mouse BAX protein or the PAMP INF1. Additionally, BLASTP and Hidden Markov Model (HMM) searches identified 10 predicted proteins belonging to the CRN (Crinkler) group of oomycete effectors. Pfam domain analysis of the secretome also identified a diverse range of putative apoplastic effectors, the major groups being glycosyl hydrolases, peptidases and protease-inhibitors. This study provides the first detailed analysis of the secretome of grapevine downy mildew and its encoded effector arsenal.
    Full-text · Article · Jul 2015 · Physiological and Molecular Plant Pathology
  • Source
    • "In M. oryzae and in C. orbiculare the effector MC69 is conserved and functions in virulence of both pathogens by suppression of PTI (Saitoh et al., 2012). Similarly the H. arabidopsidis effector HaRxL96 and its homologue from Phytophthora sojae, PsAvh163, suppress defence responses in both soybean and Arabidopsis (Anderson et al., 2012). Although the mode of action of these effectors is not fully understood, they are examples of conserved effectors that are essential for microbial virulence. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The secreted fungal effector Pep1 is essential for penetration of the host epidermis and establishment of biotrophy in the Ustilago maydis–maize pathosystem. Previously, Pep1 was found to be an inhibitor of apoplastic plant peroxidases, which suppresses the oxidative burst, a primary immune response of the host plant and enables fungal colonization. To investigate the conservation of Pep1 in other pathogens, genomes of related smut spe-cies were screened for pep1 orthologues. Pep1 proteins were produced in Escherichia coli for functional assays. The biological function of Pep1 was tested by heterologous expression in U. maydis and Hordeum vulgare. Pep1 orthologues revealed a remarkable degree of sequence conservation, indicating that this effector might play a fundamental role in virulence of biotrophic smut fungi. Pep1 func-tion and its role in virulence are conserved in different pathogenic fungi, even across the monocot–dicot border of host plants. The findings described in this study classify Pep1 as a phylogenetically conserved fungal core effector. Furthermore, we documented the influence of Pep1 on the disease caused by Blumeria graminis f. sp. hordei which is a non-smut-related pathosystem.
    Full-text · Article · Jan 2015 · New Phytologist
  • Source
    • "However, the fundamental question, " how do mature plants become competent for ARR?, " remains to be answered. In Arabidopsis, several matureplant developmental processes have been associated with SA accumulation (reviewed in Rivas-San Vicente and Plasencia, 2011). We speculate that these SA-dependent processes may contribute to ARR competence. "
    [Show abstract] [Hide abstract]
    ABSTRACT: In Arabidopsis, much of what we know about the phytohormone salicylic acid (SA) and its role in plant defense comes from experiments using young plants. We are interested in understanding why young plants are susceptible to virulent strains of Pseudomonas syringae, while mature plants exhibit a robust defense response known as age-related resistance (ARR). SA-mediated signaling is important for defense in young plants, however, ARR occurs independently of the defense regulators NPR1 and WHY1. Furthermore, intercellular SA accumulation is an important component of ARR, and intercellular washing fluids from ARR-competent plants exhibit antibacterial activity, suggesting that SA acts as an antimicrobial agent in the intercellular space. Young plants accumulate both intracellular and intercellular SA during PAMP- and effector-triggered immunity, however, virulent P. syringae promotes susceptibility by suppressing SA accumulation using the phytotoxin coronatine. Here we outline the hypothesis that mature, ARR-competent Arabidopsis alleviates coronatine-mediated suppression of SA accumulation. We also explore the role of SA in other mature-plant processes such as flowering and senescence, and discuss their potential impact on ARR.
    Full-text · Article · Jan 2014 · Frontiers in Plant Science
Show more