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Publications - Stress and Develop Biology

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Guerra, T.; Schilling, S.; Hake, K.; Gorzolka, K.; Sylvester, F.-P.; Conrads, B.; Westermann, B.; Romeis, T. Calcium‐dependent protein kinase 5 links calcium‐signaling with N‐Hydroxy‐L‐pipecolic acid‐ and SARD1‐dependent immune memory in systemic acquired resistance New Phytol 225, 310-325, (2020) DOI: 10.1111/nph.16147

Systemic acquired resistance (SAR) prepares infected plants for faster and stronger defense activation upon subsequent attacks. SAR requires an information relay from primary infection to distal tissue and the initiation and maintenance of a self‐maintaining phytohormone salicylic acid (SA)‐defense loop.In spatial and temporal resolution, we show that calcium‐dependent protein kinase CPK5 contributes to immunity and SAR. In local basal resistance, CPK5 functions upstream of SA synthesis, perception, and signaling. In systemic tissue, CPK5 signaling leads to accumulation of SAR‐inducing metabolite N‐hydroxy‐L‐pipecolic acid (NHP) and SAR marker genes, including Systemic Acquired Resistance Deficient 1 (SARD1)Plants of increased CPK5, but not CPK6, signaling display an ‘enhanced SAR’ phenotype towards a secondary bacterial infection. In the sard1‐1 background, CPK5‐mediated basal resistance is still mounted, but NHP concentration is reduced and enhanced SAR is lost.The biochemical analysis estimated CPK5 half maximal kinase activity for calcium, K50 [Ca2+], to be c. 100 nM, close to the cytoplasmic resting level. This low threshold uniquely qualifies CPK5 to decode subtle changes in calcium, a prerequisite to signal relay and onset and maintenance of priming at later time points in distal tissue. Our data explain why CPK5 functions as a hub in basal and systemic plant immunity.

Wang, W.; Liu, N.; Gao, C.; Cai, H.; Romeis, T.; Tang, D. The Arabidopsis exocyst subunits EXO70B1 and EXO70B2 regulate FLS2 homeostasis at the plasma membrane New Phytol 227, 529-544, (2020) DOI: 10.1111/nph.16515

The plasma membrane (PM)‐localized receptor kinase FLAGELLIN SENSING 2 (FLS2) recognizes bacterial flagellin or its immunogenic epitope flg22, and initiates microbe‐associated molecular pattern‐triggered immunity, which inhibits infection by bacterial pathogens. The localization, abundance and activity of FLS2 are under dynamic control.Here, we demonstrate that Arabidopsis thaliana EXO70B1, a subunit of the exocyst complex, plays a critical role in FLS2 signaling that is independent of the truncated Toll/interleukin‐1 receptor‐nucleotide binding sequence protein TIR‐NBS2 (TN2). In the exo70B1‐3 mutant, the abundance of FLS2 protein at the PM is diminished, consistent with the impaired flg22 response of this mutant. EXO70B1‐GFP plants showed increased FLS2 accumulation at the PM and therefore enhanced FLS2 signaling.The EXO70B1‐mediated trafficking of FLS2 to the PM is partially independent of the PENETRATION 1 (PEN1)‐containing secretory pathway. In addition, EXO70B1 interacts with EXO70B2, a close homolog of EXO70B1, and both proteins associate with FLS2 and contribute to the accumulation of FLS2 at the PM.Taken together, our data suggest that the exocyst complex subunits EXO70B1 and EXO70B2 regulate the trafficking of FLS2 to the PM, which represents a new layer of regulation of FLS2 function in plant immunity.

Menzel, W.; Stenzel, I.; Helbig, L.; Krishnamoorthy, P.; Neumann, S.; Eschen‐Lippold, L.; Heilmann, M.; Lee, J.; Heilmann, I. A PAMP‐triggered MAPK cascade inhibits phosphatidylinositol 4,5‐bisphosphate production by PIP5K6 in Arabidopsis thaliana New Phytol 224, 833-847, (2019) DOI: 10.1111/nph.16069

The phosphoinositide kinase PIP5K6 has recently been identified as a target for the mitogen‐activated protein kinase (MAPK) MPK6. Phosphorylation of PIP5K6 inhibited the production of phosphatidylinositol 4,5‐bisphosphate (PtdIns(4,5)P2), impacting membrane trafficking and cell expansion in pollen tubes. Here, we analyzed whether MPK6 regulated PIP5K6 in vegetative Arabidopsis cells in response to the pathogen‐associated molecular pattern (PAMP) flg22.Promoter‐β‐glucuronidase analyses and quantitative real‐time reverse transcription polymerase chain reaction data show PIP5K6 expressed throughout Arabidopsis tissues. Upon flg22 treatment of transgenic protoplasts, the PIP5K6 protein was phosphorylated, and this modification was reduced for a PIP5K6 variant lacking MPK6‐targeted residues, or in protoplasts from mpk6 mutants.Upon flg22 treatment of Arabidopsis plants, phosphoinositide levels mildly decreased and a fluorescent reporter for PtdIns(4,5)P2 displayed reduced plasma membrane association, contrasting with phosphoinositide increases reported for abiotic stress responses. Flg22 treatment and chemical induction of the upstream MAPK kinase, MKK5, decreased phosphatidylinositol 4‐phosphate 5‐kinase activity in mesophyll protoplasts, indicating that the flg22‐activated MAPK cascade limited PtdIns(4,5)P2 production. PIP5K6 expression or PIP5K6 protein abundance changed only marginally upon flg22 treatment, consistent with post‐translational control of PIP5K6 activity. PtdIns(4,5)P2‐dependent endocytosis of FM 4‐64, PIN2 and the NADPH‐oxidase RbohD were reduced upon flg22 treatment or MKK5 induction. Reduced RbohD‐endocytosis was correlated with enhanced ROS production.We conclude that MPK6‐mediated phosphorylation of PIP5K6 limits the production of a functional PtdIns(4,5)P2 pool upon PAMP perception.

Sopeña‐Torres, S.; Jordá, L.; Sánchez‐Rodríguez, C.; Miedes, E.; Escudero, V.; Swami, S.; López, G.; Piślewska‐Bednarek, M.; Lassowskat, I.; Lee, J.; Gu, Y.; Haigis, S.; Alexander, D.; Pattathil, S.; Muñoz‐Barrios, A.; Bednarek, P.; Somerville, S.; Schulze‐Lefert, P.; Hahn, M. G.; Scheel, D.; Molina, A. YODA MAP3K kinase regulates plant immune responses conferring broad‐spectrum disease resistance New Phytol 218, 661-680, (2018) DOI: 10.1111/nph.15007


Wirthmueller, L.; Asai, S.; Rallapalli, G.; Sklenar, J.; Fabro, G.; Kim, D. S.; Lintermann, R.; Jaspers, P.; Wrzaczek, M.; Kangasjärvi, J.; MacLean, D.; Menke, F. L. H.; Banfield, M. J.; Jones, J. D. G. Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to RADICAL-INDUCED CELL DEATH1 New Phytol 220, 232-248, (2018) DOI: 10.1111/nph.15277

The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. To colonize its host, Hpa translocates effector proteins that suppress plant immunity into infected host cells. Here, we investigate the relevance of the interaction between one of these effectors, HaRxL106, and Arabidopsis RADICAL‐INDUCED CELL DEATH1 (RCD1).We use pathogen infection assays as well as molecular and biochemical analyses to test the hypothesis that HaRxL106 manipulates RCD1 to attenuate transcriptional activation of defense genes.We report that HaRxL106 suppresses transcriptional activation of salicylic acid (SA)‐induced defense genes and alters plant growth responses to light. HaRxL106‐mediated suppression of immunity is abolished in RCD1 loss‐of‐function mutants. We report that RCD1‐type proteins are phosphorylated, and we identified Mut9‐like kinases (MLKs), which function as phosphoregulatory nodes at the level of photoreceptors, as RCD1‐interacting proteins. An mlk1,3,4 triple mutant exhibits stronger SA‐induced defense marker gene expression compared with wild‐type plants, suggesting that MLKs also affect transcriptional regulation of SA signaling.Based on the combined evidence, we hypothesize that nuclear RCD1/MLK complexes act as signaling nodes that integrate information from environmental cues and pathogen sensors, and that the Arabidopsis downy mildew pathogen targets RCD1 to prevent activation of plant immunity.

Mönchgesang, S.; Strehmel, N.; Trutschel, D.; Westphal, L.; Neumann, S.; Scheel, D. Plant-to-plant variability in root metabolite profiles of 19 <i>Arabidopsis thaliana</i> accessions is substance-class-dependent Inter J Mol Sci 17, (2016) DOI: 10.3390/ijms17091565

Natural variation of secondary metabolism between different accessions of Arabidopsis thaliana (A. thaliana) has been studied extensively. In this study, we extended the natural variation approach by including biological variability (plant-to-plant variability) and analysed root metabolic patterns as well as their variability between plants and naturally occurring accessions. To screen 19 accessions of A. thaliana, comprehensive non-targeted metabolite profiling of single plant root extracts was performed using ultra performance liquid chromatography/electrospray ionization quadrupole time-of-flight mass spectrometry (UPLC/ESI-QTOF-MS) and gas chromatography/electron ionization quadrupole mass spectrometry (GC/EI-QMS). Linear mixed models were applied to dissect the total observed variance. All metabolic profiles pointed towards a larger plant-to-plant variability than natural variation between accessions and variance of experimental batches. Ratios of plant-to-plant to total variability were high and distinct for certain secondary metabolites. None of the investigated accessions displayed a specifically high or low biological variability for these substance classes. This study provides recommendations for future natural variation analyses of glucosinolates, flavonoids, and phenylpropanoids and also reference data for additional substance classes.

Seybold, H.; Trempel, F.; Ranf, S.; Scheel, D.; Romeis, T.; Lee, J. Ca2+ signalling in plant immune response: from pattern recognition receptors to Ca2+ decoding mechanisms. New Phytol 204, 782–790, (2014) DOI: 10.1111/nph.13031

Ca2+ is a ubiquitous second messenger for cellular signalling in various stresses and developmental processes. Here, we summarize current developments in the roles of Ca2+ during plant immunity responses. We discuss the early perception events preceding and necessary for triggering cellular Ca2+ fluxes, the potential Ca2+-permeable channels, the decoding of Ca2+ signals predominantly via Ca2+-dependent phosphorylation events and transcriptional reprogramming. To highlight the complexity of the cellular signal network, we briefly touch on the interplay between Ca2+-dependent signalling and selected major signalling mechanisms – with special emphasis on reactive oxygen species at local and systemic levels.

Eschen-Lippold, L.; Landgraf, R.; Smolka, U.; Schulze, S.; Heilmann, M.; Heilmann, I.; Hause, G.; Rosahl, S. Activation of defense against Phytophthora infestans in potato by down-regulation of syntaxin gene expression New Phytol 193, 985-996, (2012) DOI: 10.1111/j.1469-8137.2011.04024.x

The oomycete Phytophthora infestans is the causal agent of late blight, the most devastating disease of potato. The importance of vesicle fusion processes and callose deposition for defense of potato against Phytophthora infestans was analyzed.Transgenic plants were generated, which express RNA interference constructs targeted against plasma membrane‐localized SYNTAXIN‐RELATED 1 (StSYR1) and SOLUBLE N‐ETHYLMALEIMIDE‐SENSITIVE FACTOR ADAPTOR PROTEIN 33 (StSNAP33), the potato homologs of Arabidopsis AtSYP121 and AtSNAP33, respectively.Phenotypically, transgenic plants grew normally, but showed spontaneous necrosis and chlorosis formation at later stages. In response to infection with Phytophthora infestans, increased resistance of StSYR1‐RNAi plants, but not StSNAP33‐RNAi plants, was observed. This increased resistance correlated with the constitutive accumulation of salicylic acid and PR1 transcripts. Aberrant callose deposition in Phytophthora infestans‐infected StSYR1‐RNAi plants coincided with decreased papilla formation at penetration sites. Resistance against the necrotrophic fungus Botrytis cinerea was not significantly altered. Infiltration experiments with bacterial solutions of Agrobacterium tumefaciens and Escherichia coli revealed a hypersensitive phenotype of both types of RNAi lines.The enhanced defense status and the reduced growth of Phytophthora infestans on StSYR1‐RNAi plants suggest an involvement of syntaxins in secretory defense responses of potato and, in particular, in the formation of callose‐containing papillae.

Schulze, S.; Kay, S.; Büttner, D.; Egler, M.; Eschen-Lippold, L.; Hause, G.; Krüger, A.; Lee, J.; Müller, O.; Scheel, D.; Szczesny, R.; Thieme, F.; Bonas, U. Analysis of new type III effectors from Xanthomonas uncovers XopB and XopS as suppressors of plant immunity New Phytol 195, 894-911, (2012) DOI: 10.1111/j.1469-8137.2012.04210.x

The pathogenicity of the Gram-negative plant-pathogenic bacterium Xanthomonas campestris pv. vesicatoria (Xcv) is dependent on type III effectors (T3Es) that are injected into plant cells by a type III secretion system and interfere with cellular processes to the benefit of the pathogen. In this study, we analyzed eight T3Es from Xcv strain 85-10, six of which were newly identified effectors. Genetic studies and protoplast expression assays revealed that XopB and XopS contribute to disease symptoms and bacterial growth, and suppress pathogen-associated molecular pattern (PAMP)-triggered plant defense gene expression. In addition, XopB inhibits cell death reactions induced by different T3Es, thus suppressing defense responses related to both PAMP-triggered immunity (PTI) and effector-triggered immunity (ETI). XopB localizes to the Golgi apparatus and cytoplasm of the plant cell and interferes with eukaryotic vesicle trafficking. Interestingly, a XopB point mutant derivative was defective in the suppression of ETI-related responses, but still interfered with vesicle trafficking and was only slightly affected with regard to the suppression of defense gene induction. This suggests that XopB-mediated suppression of PTI and ETI is dependent on different mechanisms that can be functionally separated.

Camehl, I.; Sherameti, I.; Venus, Y.; Bethke, G.; Varma, A.; Lee, J.; Oelmüller, R. Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana New Phytol 185, 1062-73, (2010) DOI: 10.1111/j.1469-8137.2009.03149.x

The endophytic fungus Piriformospora indica colonizes the roots of the model plant Arabidopsis thaliana and promotes its growth and seed production. The fungus can be cultivated in axenic culture without a host, and therefore this is an excellent system to investigate plant-fungus symbiosis. *The growth of etr1, ein2 and ein3/eil1 mutant plants was not promoted or even inhibited by the fungus; the plants produced less seeds and the roots were more colonized compared with the wild-type. This correlates with a mild activation of defence responses. The overexpression of ETHYLENE RESPONSE FACTOR1 constitutively activated defence responses, strongly reduced root colonization and abolished the benefits for the plants. *Piriformospora indica-mediated stimulation of growth and seed yield was not affected by jasmonic acid, and jasmonic acid-responsive promoter beta-glucuronidase gene constructs did not respond to the fungus in Arabidopsis roots. *We propose that ethylene signalling components and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis. The results show that the restriction of fungal growth by ethylene signalling components is required for the beneficial interaction between the two symbionts.
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