Article

Stage-specific suppression of basal defense discriminates barley plants containing fast- and delayed-acting Mla powdery mildew resistance alleles

Department of Plant Pathology, Center for Plant Responses to Environmental Stresses, USDA-ARS, Iowa State University, Ames, IA 50011, USA.
Molecular Plant-Microbe Interactions (Impact Factor: 4.46). 10/2006; 19(9):939-47. DOI: 10.1094/MPMI-19-0939
Source: PubMed

ABSTRACT Nonspecific recognition of pathogen-derived general elicitors triggers the first line of plant basal defense, which in turn, preconditions the host towards resistance or susceptibility. To elucidate how basal defense responses influence the onset of Mla (mildew resistance locus a)-specified resistance, we performed a meta-analysis of GeneChip mRNA expression for 155 basal defense-related genes of barley (Hordeum vulgare) challenged with Blumeria graminis f. sp. hordei, the causal agent of powdery mildew disease. In plants containing the fast-acting Mla1, Mla6, or Mla13 alleles, transcripts hyper-accumulated from 0 to 16 h after inoculation (hai) in both compatible and incompatible interactions. Suppression of basal defense-related transcripts was observed after 16 hai only in compatible interactions, whereas these transcripts were sustained or increased in incompatible interactions. By contrast, in plants containing wild-type and mutants of the delayed-acting Mla12 allele, an early hyper-induction of transcripts from 0 to 8 hai was observed, but the expression of many of these genes is markedly suppressed from 8 to 16 hai. These results suggest that the inhibition of basal defense facilitates the development of haustoria by the pathogen, consequently delaying the onset of host resistance responses. Thus, we hypothesize that the regulation of basal defense influences host-cell accessibility to the fungal pathogen and drives allelic diversification of gene-specific resistance phenotypes.

Download full-text

Full-text

Available from: Roger P Wise, Jun 25, 2014
1 Follower
 · 
74 Views
 · 
22 Downloads
  • Source
    • "Uniform loading was verified by probing with HvACTIN for western blot analysis and hvu- miR167 was used for microRNA. Barley1 GeneChip transcript profile data are from PLEXdb accession BB2 (Caldo et al., 2006; Meng et al., 2009; Moscou et al., 2011). (a) Western blot analysis for HvSOD1 (top panel), RNA gel blot analysis for hvu-miR398 (middle panel), and RNA loading control hvu-miR167 (bottom panel) for Sultan 5 and rar1-rom100. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Barley (Hordeum vulgare L.) Mildew resistance locus a (Mla) confers allele-specific interactions with natural variants of the ascomycete fungus Blumeria graminis f. sp. hordei (Bgh), the causal agent of powdery mildew disease. Significant reprogramming of Mla-mediated gene expression occurs upon infection by this obligate biotrophic pathogen. We utilized a proteomics-based approach, combined with barley mla, required for Mla12 resistance1 (rar1), and restoration of Mla resistance1 (rom1) mutants, to identify components of Mla-directed signaling. Loss-of-function mutations in Mla and Rar1 both resulted in the reduced accumulation of chloroplast copper/zinc superoxide dismutase 1 (HvSOD1), whereas loss of function in Rom1 re-established HvSOD1 levels. In addition, both Mla and Rom1 negatively regulated hvu-microRNA398 (hvu-miR398), and up-regulation of miR398 was coupled to reduced HvSOD1 expression. Barley stripe mosaic virus (BSMV)-mediated over-expression of both barley and Arabidopsis miR398 repressed accumulation of HvSOD1, and BSMV-induced gene silencing of HvSod1 impeded Mla-triggered H2 O2 and hypersensitive reaction (HR) at barley-Bgh interaction sites. These data indicate that Mla- and Rom1-regulated hvu-miR398 represses HvSOD1 accumulation, influencing effector-induced HR in response to the powdery mildew fungus.
    New Phytologist 11/2013; 201(4). DOI:10.1111/nph.12598 · 7.67 Impact Factor
  • Source
    • "). RKN are biotrophic pathogens and the success of infection depends on the ability of the pathogen to overcome PTI, as reported for other pathogens . Several type III secreted protein effectors and fungal effectors have been shown to contribute to pathogen virulence by suppressing PTI (Caldo et al. 2006; Göhre and Robatzek 2008; Kim et al. 2009 "
    [Show abstract] [Hide abstract]
    ABSTRACT: Root-knot nematodes are obligate biotrophic parasites that settle close to the vascular tissues in roots, where they induce the differentiation of specialized feeding cells and maintain a compatible interaction for three to eight weeks. Transcriptome analyses of the plant response to parasitic infection have shown that plant defenses are strictly controlled during the interaction. This suggests that, similar to other pathogens, RKN secrete effectors that suppress host defenses. We show here that Mi-CRT, a calreticulin secreted by the nematode into the apoplasm of infected tissues, plays an important role in infection success, as Mi-CRT knockdown by RNA interference affected the ability of the nematodes to infect plants. Stably transformed Arabidopsis thaliana plants producing the secreted form of Mi-CRT were more susceptible to nematode infection than wild-type plants. They were also more susceptible to infection with another root pathogen, the oomycete Phytophthora parasitica. Mi-CRT overexpression in A. thaliana suppressed the induction of defense marker genes and callose deposition after treatment with the PAMP elf18. Our results show that Mi-CRT secreted in the apoplasm by the nematode has a role in the suppression of plant basal defenses during the interaction.
    Molecular Plant-Microbe Interactions 08/2012; 26(1). DOI:10.1094/MPMI-05-12-0130-R · 4.46 Impact Factor
  • Source
    • "C. graminicola initially colonizes the plant leaf biotrophically and later switches to a necrotrophic lifestyle. It has been well established that biotrophic pathogens such as Uromyces vignae and U. maydis as well as hemibiotrophs such as M. graminicola, during the biotrophic phase, must suppress or attenuate host defenses to be able to parasitize the invaded host cells (Panstruga, 2003; Caldo et al., 2006; Jones and Dangl, 2006; Adhikari et al., 2007; Doehlemann et al., 2008; Eich- Table II "
    [Show abstract] [Hide abstract]
    ABSTRACT: Hemibiotrophic plant pathogens first establish a biotrophic interaction with the host plant and later switch to a destructive necrotrophic lifestyle. Studies of biotrophic pathogens have shown that they actively suppress plant defenses after an initial microbe-associated molecular pattern-triggered activation. In contrast, studies of the hemibiotrophs suggest that they do not suppress plant defenses during the biotrophic phase, indicating that while there are similarities between the biotrophic phase of hemibiotrophs and biotrophic pathogens, the two lifestyles are not analogous. We performed transcriptomic, histological, and biochemical studies of the early events during the infection of maize (Zea mays) with Colletotrichum graminicola, a model pathosystem for the study of hemibiotrophy. Time-course experiments revealed that mRNAs of several defense-related genes, reactive oxygen species, and antimicrobial compounds all begin to accumulate early in the infection process and continue to accumulate during the biotrophic stage. We also discovered the production of maize-derived vesicular bodies containing hydrogen peroxide targeting the fungal hyphae. We describe the fungal respiratory burst during host infection, paralleled by superoxide ion production in specific fungal cells during the transition from biotrophy to a necrotrophic lifestyle. We also identified several novel putative fungal effectors and studied their expression during anthracnose development in maize. Our results demonstrate a strong induction of defense mechanisms occurring in maize cells during C. graminicola infection, even during the biotrophic development of the pathogen. We hypothesize that the switch to necrotrophic growth enables the fungus to evade the effects of the plant immune system and allows for full fungal pathogenicity.
    Plant physiology 03/2012; 158(3):1342-58. DOI:10.1104/pp.111.190397 · 7.39 Impact Factor
Show more