Barley MLO Modulates Actin-Dependent and Actin-Independent Antifungal Defense Pathways at the Cell Periphery

Miklis, Marco; Consonni, Chiara; Bhat, Riyaz Ahmad; Lipka, Volker; Schulze‐Lefert, Paul; Panstruga, Ralph

doi:10.1104/pp.107.098897

Cited by 182 publications

(168 citation statements)

References 90 publications

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“…Cyan fluorescent protein or yellow fluorescent protein was inserted at the C terminus of ADF in this study. As overexpression of ADF could interfere with plant development (Dong et al, 2001) and response to the powdery mildew fungus (Miklis et al, 2007), we cloned the ADF4 genomic region containing the 1.5-kb ADF4 promoter, introns, and 39 UTR for examination of the subcellular localization and function of ADF in the Arabidopsis-G. orontii interaction. The ADF4 genomic construct fused with GFP inserted upstream of the first exon (GFP-ADF4) was transformed into adf4, and T2 plants were examined.…”

Section: Nuclear Localization and Phosphorylation Of Adf4 Are Both Immentioning

confidence: 99%

“…Transient overexpression of HvADF3, AtADF1, AtADF5, AtADF6, AtADF7, and AtADF11 (called AtADF12 in this article), but not the overexpression of AtADF2, AtADF3, AtADF4, and AtADF9, partially breaks down the resistance of barley (Hordeum vulgare) mlo against the barley-adapted powdery mildew fungus Blumeria graminis f. sp. hordei (Bgh; Miklis et al, 2007). The localization of RPW8.2 to the membrane surrounding the powdery mildew fungal haustorium is inhibited by the overexpression of Arabidopsis ADF6 but not by the overexpression of ADF5 (Wang et al, 2009).…”

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confidence: 99%

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Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

2016

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Actin-depolymerizing factors (ADFs) are conserved proteins that function in regulating the structure and dynamics of actin microfilaments in eukaryotes. In this study, we present evidence that Arabidopsis (Arabidopsis thaliana) subclass I ADFs, particularly ADF4, functions as a susceptibility factor for an adapted powdery mildew fungus. The null mutant of ADF4 significantly increased resistance against the adapted powdery mildew fungus Golovinomyces orontii. The degree of resistance was further enhanced in transgenic plants in which the expression of all subclass I ADFs (i.e. ADF1-ADF4) was suppressed. Microscopic observations revealed that the enhanced resistance of adf4 and ADF1-4 knockdown plants (ADF1-4Ri) was associated with the accumulation of hydrogen peroxide and cell death specific to G. orontii-infected cells. The increased resistance and accumulation of hydrogen peroxide in ADF1-4Ri were suppressed by the introduction of mutations in the salicylic acid-and jasmonic acid-signaling pathways but not by a mutation in the ethylene-signaling pathway. Quantification by microscopic images detected an increase in the level of actin microfilament bundling in ADF1-4Ri but not in adf4 at early G. orontii infection time points. Interestingly, complementation analysis revealed that nuclear localization of ADF4 was crucial for susceptibility to G. orontii. Based on its G. orontii-infected-cell-specific phenotype, we suggest that subclass I ADFs are susceptibility factors that function in a direct interaction between the host plant and the powdery mildew fungus.Powdery mildew is an obligate biotrophic fungal pathogen that infects approximately 10,000 plant species, including crops, vegetables, and ornamental plants, thus causing extensive economic losses worldwide (Takamatsu, 2004). In an effort to understand the plant response to powdery mildew fungal infection and the mechanism of plant-powdery mildew fungus interactions, many mutants of host plants, particularly the model plant Arabidopsis (Arabidopsis thaliana), have been identified and analyzed.Genes for which loss causes increased resistance to a pathogen could encode factors involved in the suppression of plant immunity or susceptibility factors that function in support of the pathogenic infection. Previously identified Arabidopsis genes, the loss of whose expression causes enhanced resistance against adapted powdery mildew fungi, include POWDERY MILDEW RESISTANT1 (PMR1)

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Section: Nuclear Localization and Phosphorylation Of Adf4 Are Both Immentioning

confidence: 99%

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confidence: 99%

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

2016

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“…34 Direct evidence for a role for F-actin in HR-PCD is limited. Several studies have shown that cytochalasins affect resistance to pathogens, 48 suggesting a role for actin polymerisation, but as resistance is not always accompanied by HR-PCD, we do not consider these studies here. More direct evidence for a role for the actin cytoskeleton in HR-PCD is provided by data showing that cytochalasins can suppress cell death triggered by Phytophthora infestans in potato; cytochalasin D treatment also delayed induction of key defence markers and decreased the accumulation of PR proteins, with concomitant alleviation of cell death in potato tubers treated with P. infestans cell wall extracts (Figure 2b).…”

Section: Evidence That Actin Dynamics Are Involved In Mediating Pcdmentioning

confidence: 99%

“…Only actin-depolymerising factor (ADF) has been shown to have a role in the regulation of HR-PCD. 48,52 ADF severs F-actin, promotes dissociation of monomeric actin from the pointed end and increases F-actin turnover, 54 so is important for the reorganisation of actin filaments. Proteomic analysis of Petunia flowers reveals downregulation of a basic isoform and upregulation of an acidic isoform of ADF, 15 suggesting ADF may be phosphorylated during senescence.…”

Section: How Is Regulation Of the Cytoskeleton To Mediate Pcd Achieved?mentioning

confidence: 99%

Organisation and regulation of the cytoskeleton in plant programmed cell death

2011

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Programmed cell death (PCD) involves precise integration of cellular responses to extracellular and intracellular signals during both stress and development. In recent years much progress in our understanding of the components involved in PCD in plants has been made. Signalling to PCD results in major reorganisation of cellular components. The plant cytoskeleton is known to play a major role in cellular organisation, and reorganization and alterations in its dynamics is a well known consequence of signalling. There are considerable data that the plant cytoskeleton is reorganised in response to PCD, with remodelling of both microtubules and microfilaments taking place. In the majority of cases, the microtubule network depolymerises, whereas remodelling of microfilaments can follow two scenarios, either being depolymerised and then forming stable foci, or forming distinct bundles and then depolymerising. Evidence is accumulating that demonstrate that these cytoskeletal alterations are not just a consequence of signals mediating PCD, but that they also may have an active role in the initiation and regulation of PCD. Here we review key data from higher plant model systems on the roles of the actin filaments and microtubules during PCD and discuss proteins potentially implicated in regulating these alterations.

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“…Evidence largely comes from studies using actin cytoskeleton-disrupting agents, such as cytochalasins. Treatments with a variety of cytochalasins were shown to increase the penetration rate of both adapted and nonadapted pathogens in multiple plant-pathogen systems, thereby implicating the actin cytoskeleton as having a role in basal defenses and nonhost resistance (Kobayashi et al, 1997;Yun et al, 2003;Shimada et al, 2006;Miklis et al, 2007). The actin cytoskeleton may also play a role in race-specific resistance (Skalamera and Heath, 1998).…”

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confidence: 99%

Arabidopsis Actin-Depolymerizing Factor AtADF4 Mediates Defense Signal Transduction Triggered by thePseudomonas syringaeEffector AvrPphB

et al. 2009

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The actin cytoskeleton has been implicated in plant defenses against pathogenic fungi and oomycetes with limited, indirect evidence. To date, there are no reports linking actin with resistance against phytopathogenic bacteria. The dynamic behavior of actin filaments is regulated by a diverse array of actin-binding proteins, among which is the Actin-Depolymerizing Factor (ADF) family of proteins. Here, we demonstrate that actin dynamics play a role in the activation of gene-for-gene resistance in Arabidopsis (Arabidopsis thaliana) following inoculation with the phytopathogenic bacterium Pseudomonas syringae pv tomato. Using a reverse genetics approach, we explored the roles of Arabidopsis ADFs in plant defenses. AtADF4 was identified as being specifically required for resistance triggered by the effector AvrPphB but not AvrRpt2 or AvrB. Recombinant AtADF4 bound to monomeric actin (G-actin) with a marked preference for the ADP-loaded form and inhibited the rate of nucleotide exchange on G-actin, indicating that AtADF4 is a bona fide actin-depolymerizing factor. Exogenous application of the actindisrupting agent cytochalasin D partially rescued the Atadf4 mutant in the AvrPphB-mediated hypersensitive response, demonstrating that AtADF4 mediates defense signaling through modification of the actin cytoskeleton. Unlike the mechanism by which the actin cytoskeleton confers resistance against fungi and oomycetes, AtADF4 is not involved in resistance against pathogen entry. Collectively, this study identifies AtADF4 as a novel component of the plant defense signaling pathway and provides strong evidence for actin dynamics as a primary component that orchestrates plant defenses against P. syringae.

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Barley MLO Modulates Actin-Dependent and Actin-Independent Antifungal Defense Pathways at the Cell Periphery

Cited by 182 publications

References 90 publications

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

Organisation and regulation of the cytoskeleton in plant programmed cell death

Arabidopsis Actin-Depolymerizing Factor AtADF4 Mediates Defense Signal Transduction Triggered by thePseudomonas syringaeEffector AvrPphB

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