The cytoskeleton is disrupted by the bacterial effector HrpZ, but not by the bacterial PAMP flg22, in tobacco BY-2 cells

Journal of Experimental Botany, Apr 2013

Plant innate immunity is composed of two layers. Basal immunity is triggered by pathogen-associated molecular patterns (PAMPs) such as the flagellin-peptide flg22 and is termed PAMP-triggered immunity (PTI). In addition, effector-triggered immunity (ETI) linked with programmed cell death and cytoskeletal reorganization can be induced by pathogen-derived factors, such as the Harpin proteins originating from phytopathogenic bacteria. To get insight into the link between cytoskeleton and PTI or ETI, this study followed the responses of actin filaments and microtubules to flg22 and HrpZ in vivo by spinning-disc confocal microscopy in GFP-tagged marker lines of tobacco BY-2. At a concentration that clearly impairs mitosis, flg22 can induce only subtle cytoskeletal responses. In contrast, HrpZ causes a rapid and massive bundling of actin microfilaments (completed in ~20min, i.e. almost simultaneously with extracellular alkalinization), which is followed by progressive disintegration of actin cables and cytoplasmic microtubules, a loss of cytoplasmic structure, and vacuolar disintegration. Cytoskeletal disruption is proposed as an early event that discriminates HrpZ-triggered ETI-like defence from flg22-triggered PTI.

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The cytoskeleton is disrupted by the bacterial effector HrpZ, but not by the bacterial PAMP flg22, in tobacco BY-2 cells

XinGuan 1 GntherBuchholz 0 PeterNick 1 0 RLP AgroScience/AlPlanta - Institute for Plant Research , Breitenweg 71, D-67435, Neustadt an der Weinstrae, Germany 1 Molecular Cell Biology, Botanical Institute, Karlsruhe Institute of Technology , Kaiserstr. 2, D-76128 Karlsruhe, Germany Plant innate immunity is composed of two layers. Basal immunity is triggered by pathogen-associated molecular patterns (PAMPs) such as the flagellin-peptide flg22 and is termed PAMP-triggered immunity (PTI). In addition, effector-triggered immunity (ETI) linked with programmed cell death and cytoskeletal reorganization can be induced by pathogen-derived factors, such as the Harpin proteins originating from phytopathogenic bacteria. To get insight into the link between cytoskeleton and PTI or ETI, this study followed the responses of actin filaments and microtubules to flg22 and HrpZ in vivo by spinning-disc confocal microscopy in GFP-tagged marker lines of tobacco BY-2. At a concentration that clearly impairs mitosis, flg22 can induce only subtle cytoskeletal responses. In contrast, HrpZ causes a rapid and massive bundling of actin microfilaments (completed in ~20 min, i.e. almost simultaneously with extracellular alkalinization), which is followed by progressive disintegration of actin cables and cytoplasmic microtubules, a loss of cytoplasmic structure, and vacuolar disintegration. Cytoskeletal disruption is proposed as an early event that discriminates HrpZ-triggered ETI-like defence from flg22-triggered PTI. - Plants lack the somatic adaptive immune system based on mobile defence cells characteristic for animal immunity. Plant defence, in contrast, is based upon an innate immunity of each individual cell (Jones and Dangl, 2006). This innate immunity comprises two distinct layers. The basal layer is evolutionarily ancient and triggered by conserved pathogen structures termed pathogen-associated molecular patterns (PAMPs). These PAMPs, such as flagellin, the subunit building the filament of bacterial flagellum, bind to specific receptors in the plasma membrane triggering so-called PAMP-triggered immunity (PTI). This basal layer of broad immunity is often accompanied by a more advanced and strain-specific immunity termed effector-triggered immunity (ETI), which is triggered by pathogen effectors that have to enter the cytoplasm of the host cell. The reason for this complexity is linked to coevolution between host and pathogen: PTI would be expected to select for pathogens, where the eliciting PAMPs are lost. However, since PAMPs are essential for the lifecycle of the pathogen, this evolutionary strategy does not work a bacterial intruder lacking the PAMP flagellin would not elicit a PTI response, but it would also not be able to move. This dilemma stimulated, during a second round of hostpathogen warfare, the development of microbial effector proteins. These effectors are secreted into the cytoplasm of the host and suppress PTI (for review, see Tsuda and Katagiri, 2010). In response to these pathogen effectors, the host plant has evolved additional pathogen-specific receptors (encoded by so-called R genes) that specifically recognize the effectors in the cytoplasm and trigger the second layer of immunity, ETI (Boller and He, 2009). In many cases, ETI culminates in a plant-specific version of programmed cell death, the hypersensitive response, often followed by systemic acquired resistance of the host. The conceptual dichotomy between PTI and ETI has been very valuable to interpret and classify the huge variety of plant defence responses, but this concept is presently on the move again. Recent studies show that the difference between PAMPs and effectors is more gradual than previously conceived (Thomma etal., 2011). Moreover, PTI and ETI share numerous common events (Tsuda and Katagiri, 2010). Thus, the apparent dichotomy might be a question of signal quantity rather than quality. In addition, plants can discriminate different pathogens and activate different responses that are appropriate for the respective pathogen. Therefore, at present, the PTI-ETI concept is extended towards a signaturebased model (for review, see Aslam etal., 2009). The archetypal elicitor of PTI is bacterial flagellin, which triggers defence responses in various plants (Gmez-Gmez and Boller, 2002). Asynthetic 22-amino-acid peptide (flg22) from a conserved flagellin domain is sufficient to induce most of the cellular responses (Felix etal., 1999). Agenetic screen in Arabidopsis thaliana using flg22 identified the Arabidopsis leucine-rich repeat receptor kinase FLS2, which binds flg22 (for review, see Chinchilla etal., 2006). Upon binding of the ligand, FLS2 is internalized by a receptor-mediated endocytic process that presumably has regulatory functions (Jones and Dangl, 2006). To trigger ETI-like programmed cell death, Harpin proteins have been used. These bacterial proteins, first discovered in Erwinia amylovora, a phytopathogenic bacterium causing t (...truncated)


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Xin Guan, Günther Buchholz, Peter Nick. The cytoskeleton is disrupted by the bacterial effector HrpZ, but not by the bacterial PAMP flg22, in tobacco BY-2 cells, Journal of Experimental Botany, 2013, pp. 1805-1816, 64/7, DOI: 10.1093/jxb/ert042