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Two for all: receptor-associated kinases SOBIR1 and BAK1
Liebrand, T.W.H. ; Burg, H.A. van den; Joosten, M.H.A.J. - \ 2014
Trends in Plant Science 19 (2014)2. - ISSN 1360-1385 - p. 123 - 132.
plant innate immunity - pattern-recognition receptors - ethylene-inducing xylanase - arabidopsis-thaliana - cladosporium-fulvum - defense responses - cell-death - signaling pathways - plasma-membrane - protein-kinase
Leucine-rich repeat-receptor-like proteins (LRR-RLPs) are ubiquitous cell surface receptors lacking a cytoplasmic signalling domain. For most of these LRR-RLPs, it remained enigmatic how they activate cellular responses upon ligand perception. Recently, the LRR-receptor-like kinase (LRR-RLK) SUPPRESSOR OF BIR1-1 (SOBIR1) was shown to be essential for triggering defence responses by certain LRR-RLPs that act as immune receptors. In addition to SOBIR1, the regulatory LRR-RLK BRI1-ASSOCIATED KINASE-1 (BAK1) is also required for LRR-RLP function. Here, we compare the roles of SOBIR1 and BAK1 as regulatory LRR-RLKs in immunity and development. BAK1 has a general regulatory role in plasma membrane-associated receptor complexes comprising LRR-RLPs and/or LRR-RLKs. By contrast, SOBIR1 appears to be specifically required for the function of receptor complexes containing LRR-RLPs.
Chaperones of the endoplasmic reticulum are required for Ve1-mediated resistance to Verticillium
Liebrand, T.W.H. ; Kombrink, A. ; Zhang, Z. ; Sklenar, J. ; Jones, A.M.E. ; Robatzek, S. ; Thomma, B.P.H.J. ; Joosten, M.H.A.J. - \ 2014
Molecular Plant Pathology 15 (2014)1. - ISSN 1464-6722 - p. 109 - 117.
receptor-like proteins - defective brassinosteroid receptor - pattern-recognition receptors - er quality-control - plant innate immunity - cell-surface - tomato ve1 - arabidopsis - gene - perception
The tomato receptor-like protein (RLP) Ve1 mediates resistance to the vascular fungal pathogen Verticillium dahliae. To identify the proteins required for Ve1 function, we transiently expressed and immunopurified functional Ve1-enhanced green fluorescent protein (eGFP) from Nicotiana benthamiana leaves, followed by mass spectrometry. This resulted in the identification of peptides originating from the endoplasmic reticulum (ER)-resident chaperones HSP70 binding proteins (BiPs) and a lectin-type calreticulin (CRT). Knock-down of the different BiPs and CRTs in tomato resulted in compromised Ve1-mediated resistance to V.dahliae in most cases, showing that these chaperones play an important role in Ve1 functionality. Recently, it has been shown that one particular CRT is required for the biogenesis of the RLP-type Cladosporium fulvum resistance protein Cf-4 of tomato, as silencing of CRT3a resulted in a reduced pool of complex glycosylated Cf-4 protein. In contrast, knock-down of the various CRTs in N.benthamiana or N.tabacum did not result in reduced accumulation of mature complex glycosylated Ve1 protein. Together, this study shows that the BiP and CRT ER chaperones differentially contribute to Cf-4- and Ve1-mediated immunity.
Interaction of Medicago truncatula Lysin Motif Receptor-Like Kinases, NFP and LYK3, Produced in Nicotiana benthamiana Induces Defence-Like Responses
Pietraszewska-Bogiel, A. ; Lefebvre, B. ; Koini, M.A. ; Klaus-Heisen, D. ; Takken, F.L.W. ; Geurts, R. ; Cullimore, J.V. ; Gadella, T.W.J. - \ 2013
PLoS One 8 (2013)6. - ISSN 1932-6203
phospholipid signaling pathways - plant innate immunity - nod factor perception - root hair-cells - lotus-japonicus - arabidopsis-thaliana - molecular-patterns - fluorescent proteins - bacterial-infection - plasma-membrane
Receptor(-like) kinases with Lysin Motif (LysM) domains in their extracellular region play crucial roles during plant interactions with microorganisms; e.g. Arabidopsis thaliana CERK1 activates innate immunity upon perception of fungal chitin/chitooligosaccharides, whereas Medicago truncatula NFP and LYK3 mediate signalling upon perception of bacterial lipo-chitooligosaccharides, termed Nod factors, during the establishment of mutualism with nitrogen-fixing rhizobia. However, little is still known about the exact activation and signalling mechanisms of MtNFP and MtLYK3. We aimed at investigating putative molecular interactions of MtNFP and MtLYK3 produced in Nicotiana benthamiana. Surprisingly, heterologous co-production of these proteins resulted in an induction of defence-like responses, which included defence-related gene expression, accumulation of phenolic compounds, and cell death. Similar defence-like responses were observed upon production of AtCERK1 in N. benthamiana leaves. Production of either MtNFP or MtLYK3 alone or their co-production with other unrelated receptor(-like) kinases did not induce cell death in N. benthamiana, indicating that a functional interaction between these LysM receptor-like kinases is required for triggering this response. Importantly, structure-function studies revealed that the MtNFP intracellular region, specific features of the MtLYK3 intracellular region (including several putative phosphorylation sites), and MtLYK3 and AtCERK1 kinase activity were indispensable for cell death induction, thereby mimicking the structural requirements of nodulation or chitin-induced signalling. The observed similarity of N. benthamiana response to MtNFP and MtLYK3 co-production and AtCERK1 production suggests the existence of parallels between Nod factor-induced and chitin-induced signalling mediated by the respective LysM receptor(-like) kinases. Notably, the conserved structural requirements for MtNFP and MtLYK3 biological activity in M. truncatula (nodulation) and in N. benthamiana (cell death induction) indicates the relevance of the latter system for studies on these, and potentially other symbiotic LysM receptor-like kinases
Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of cf receptor-like proteins involved in pathogen resistance of tomato
Liebrand, T.W.H. ; Smit, P. ; Abd-El-Haliem, A. ; Jonge, R. de; Cordewener, J.H.G. ; America, A.H.P. ; Sklenar, J. ; Jones, A.M. ; Robatzek, S. ; Thomma, B.P.H.J. ; Tameling, W.I. ; Joosten, M.H.A.J. - \ 2012
Plant Physiology 159 (2012)4. - ISSN 0032-0889 - p. 1819 - 1833.
defective brassinosteroid receptor - pattern-recognition receptors - plant innate immunity - cladosporium-fulvum - disease resistance - hypersensitive response - virulence factor - effector ecp6 - cell-death - gene
Cf proteins are receptor-like proteins (RLPs) that mediate resistance of tomato (Solanum lycopersicum) to the foliar pathogen Cladosporium fulvum. These transmembrane immune receptors, which carry extracellular leucine-rich repeats that are subjected to posttranslational glycosylation, perceive effectors of the pathogen and trigger a defense response that results in plant resistance. To identify proteins required for the functionality of these RLPs, we performed immunopurification of a functional Cf-4-enhanced green fluorescent protein fusion protein transiently expressed in Nicotiana benthamiana, followed by mass spectrometry. The endoplasmic reticulum (ER) heat shock protein70 binding proteins (BiPs) and lectin-type calreticulins (CRTs), which are chaperones involved in ER-quality control, were copurifying with Cf-4-enhanced green fluorescent protein. The tomato and N. benthamiana genomes encode four BiP homologs and silencing experiments revealed that these BiPs are important for overall plant viability. For the three tomato CRTs, virus-induced gene silencing targeting the plant-specific CRT3a gene resulted in a significantly compromised Cf-4-mediated defense response and loss of full resistance to C. fulvum. We show that upon knockdown of CRT3a the Cf-4 protein accumulated, but the pool of Cf-4 protein carrying complex-type N-linked glycans was largely reduced. Together, our study on proteins required for Cf function reveals an important role for the CRT ER chaperone CRT3a in the biogenesis and functionality of this type of RLP involved in plant defense
Brassinosteroids inhibit pathogen-associated molecular pattern–triggered immune signaling independent of the receptor kinase BAK1.
Albrecht, C. ; Boutrot, F. ; Segonzac, C. ; Schwessinger, B. ; Gimenez-Ibanez, S. ; Rathjen, J.P. ; Chinchilla, D. ; Vries, S.C. de; Zipfel, C. - \ 2012
Proceedings of the National Academy of Sciences of the United States of America 109 (2012)1. - ISSN 0027-8424 - p. 303 - 308.
plant innate immunity - disease resistance - gene-expression - protein complex - arabidopsis - growth - pathways - fls2 - responses - acid
Plants and animals use innate immunity as a first defense against pathogens, a costly yet necessary tradeoff between growth and immunity. In Arabidopsis, the regulatory leucine-rich repeat receptor-like kinase (LRR-RLK) BAK1 combines with the LRR-RLKs FLS2 and EFR in pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and the LRR-RLK BRI1 in brassinosteroid (BR)-mediated growth. Therefore, a potential tradeoff between these pathways mediated by BAK1 is often postulated. Here, we show a unidirectional inhibition of FLS2-mediated immune signaling by BR perception. Unexpectedly, this effect occurred downstream or independently of complex formation with BAK1 and associated downstream phosphorylation. Thus, BAK1 is not rate-limiting in these pathways. BRs also inhibited signaling triggered by the BAK1-independent recognition of the fungal PAMP chitin. Our results suggest a general mechanism operative in plants in which BR-mediated growth directly antagonizes innate immune signaling.
RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function
Tameling, W.I.L. ; Nooijen, C. ; Ludwig, N. ; Boter, M. ; Slootweg, E.J. ; Goverse, A. ; Shirasu, K. ; Joosten, M.H.A.J. - \ 2010
The Plant Cell 22 (2010). - ISSN 1040-4651 - p. 4176 - 4194.
disease resistance protein - potato-virus-x - gtpase-activating protein - leucine-rich repeat - nuclear transport factor-2 - gene confers resistance - plant innate immunity - tobacco-mosaic-virus - cell-death - ran-gtpase
The potato (Solanum tuberosum) nucleotide binding–leucine-rich repeat immune receptor Rx confers resistance to Potato virus X (PVX) and requires Ran GTPase-activating protein 2 (RanGAP2) for effective immune signaling. Although Rx does not contain a discernible nuclear localization signal, the protein localizes to both the cytoplasm and nucleus in Nicotiana benthamiana. Transient coexpression of Rx and cytoplasmically localized RanGAP2 sequesters Rx in the cytoplasm. This relocation of the immune receptor appeared to be mediated by the physical interaction between Rx and RanGAP2 and was independent of the concomitant increased GAP activity. Coexpression with RanGAP2 also potentiates Rx-mediated immune signaling, leading to a hypersensitive response (HR) and enhanced resistance to PVX. Besides sequestration, RanGAP2 also stabilizes Rx, a process that likely contributes to enhanced defense signaling. Strikingly, coexpression of Rx with the Rx-interacting WPP domain of RanGAP2 fused to a nuclear localization signal leads to hyperaccumulation of both the WPP domain and Rx in the nucleus. As a consequence, both Rx-mediated resistance to PVX and the HR induced by auto-active Rx mutants are significantly suppressed. These data show that a balanced nucleocytoplasmic partitioning of Rx is required for proper regulation of defense signaling. Furthermore, our data indicate that RanGAP2 regulates this partitioning by serving as a cytoplasmic retention factor for Rx
RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector
Bernoux, M. ; Timmers, T. ; Jauneau, A. ; Brière, C. ; Wit, P.J.G.M. de; Marco, Y. ; Deslandes, L. - \ 2008
The Plant Cell 20 (2008)8. - ISSN 1040-4651 - p. 2252 - 2264.
agrobacterium-mediated transformation - cf-2-dependent disease resistance - tomato lycopersicon-esculentum - lifetime imaging microscopy - programmed cell-death - plant innate immunity - for-gene concept - iii effector - cladosporium-fulvum - hypersensitive respon
Bacterial wilt, a disease impacting cultivated crops worldwide, is caused by the pathogenic bacterium Ralstonia solanacearum. PopP2 (for Pseudomonas outer protein P2) is an R. solanacearum type III effector that belongs to the YopJ/AvrRxv protein family and interacts with the Arabidopsis thaliana RESISTANT TO RALSTONIA SOLANACEARUM 1-R (RRS1-R) resistance protein. RRS1-R contains the Toll/Interleukin1 receptor¿nucleotide binding site¿Leu-rich repeat domains found in several cytoplasmic R proteins and a C-terminal WRKY DNA binding domain. In this study, we identified the Arabidopsis Cys protease RESPONSIVE TO DEHYDRATION19 (RD19) as being a PopP2-interacting protein whose expression is induced during infection by R. solanacearum. An Arabidopsis rd19 mutant in an RRS1-R genetic background is compromised in resistance to the bacterium, indicating that RD19 is required for RRS1-R¿mediated resistance. RD19 normally localizes in mobile vacuole-associated compartments and, upon coexpression with PopP2, is specifically relocalized to the plant nucleus, where the two proteins physically interact. No direct physical interaction between RRS1-R and RD19 in the presence of PopP2 was detected in the nucleus as determined by Förster resonance energy transfer. We propose that RD19 associates with PopP2 to form a nuclear complex that is required for activation of the RRS1-R¿mediated resistance response.