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Publications - Stress and Develop Biology

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Publications

Ortmann, S.; Marx, J.; Lampe, C.; Handrick, V.; Ehnert, T.-M.; Zinecker, S.; Reimers, M.; Bonas, U.; Erickson, J.; A conserved microtubule-binding region in Xanthomonas XopL is indispensable for induced plant cell death reactions PLOS Pathog. 19, e1011263, (2023) DOI: 10.1371/journal.ppat.1011263

Pathogenic Xanthomonas bacteria cause disease on more than 400 plant species. These Gram-negative bacteria utilize the type III secretion system to inject type III effector proteins (T3Es) directly into the plant cell cytosol where they can manipulate plant pathways to promote virulence. The host range of a given Xanthomonas species is limited, and T3E repertoires are specialized during interactions with specific plant species. Some effectors, however, are retained across most strains, such as Xanthomonas Outer Protein L (XopL). As an ‘ancestral’ effector, XopL contributes to the virulence of multiple xanthomonads, infecting diverse plant species. XopL homologs harbor a combination of a leucine-rich-repeat (LRR) domain and an XL-box which has E3 ligase activity. Despite similar domain structure there is evidence to suggest that XopL function has diverged, exemplified by the finding that XopLs expressed in plants often display bacterial species-dependent differences in their sub-cellular localization and plant cell death reactions. We found that XopL from X. euvesicatoria (XopLXe) directly associates with plant microtubules (MTs) and causes strong cell death in agroinfection assays in N. benthamiana. Localization of XopLXe homologs from three additional Xanthomonas species, of diverse infection strategy and plant host, revealed that the distantly related X. campestris pv. campestris harbors a XopL (XopLXcc) that fails to localize to MTs and to cause plant cell death. Comparative sequence analyses of MT-binding XopLs and XopLXcc identified a proline-rich-region (PRR)/α-helical region important for MT localization. Functional analyses of XopLXe truncations and amino acid exchanges within the PRR suggest that MT-localized XopL activity is required for plant cell death reactions. This study exemplifies how the study of a T3E within the context of a genus rather than a single species can shed light on how effector localization is linked to biochemical activity.
Publications

Blüher, D.; Laha, D.; Thieme, S.; Hofer, A.; Eschen-Lippold, L.; Masch, A.; Balcke, G.; Pavlovic, I.; Nagel, O.; Schonsky, A.; Hinkelmann, R.; Wörner, J.; Parvin, N.; Greiner, R.; Weber, S.; Tissier, A.; Schutkowski, M.; Lee, J.; Jessen, H.; Schaaf, G.; Bonas, U.; A 1-phytase type III effector interferes with plant hormone signaling Nat. Commun. 8, 2159, (2017) DOI: 10.1038/s41467-017-02195-8

Most Gram-negative phytopathogenic bacteria inject type III effector (T3E) proteins into plant cells to manipulate signaling pathways to the pathogen’s benefit. In resistant plants, specialized immune receptors recognize single T3Es or their biochemical activities, thus halting pathogen ingress. However, molecular function and mode of recognition for most T3Es remains elusive. Here, we show that the Xanthomonas T3E XopH possesses phytase activity, i.e., dephosphorylates phytate (myo-inositol-hexakisphosphate, InsP6), the major phosphate storage compound in plants, which is also involved in pathogen defense. A combination of biochemical approaches, including a new NMR-based method to discriminate inositol polyphosphate enantiomers, identifies XopH as a naturally occurring 1-phytase that dephosphorylates InsP6 at C1. Infection of Nicotiana benthamiana and pepper by Xanthomonas results in a XopH-dependent conversion of InsP6 to InsP5. 1-phytase activity is required for XopH-mediated immunity of plants carrying the Bs7 resistance gene, and for induction of jasmonate- and ethylene-responsive genes in N. benthamiana.
Publications

Singer, A. U.; Schulze, S.; Skarina, T.; Xu, X.; Cui, H.; Eschen-Lippold, L.; Egler, M.; Srikumar, T.; Raught, B.; Lee, J.; Scheel, D.; Savchenko, A.; Bonas, U.; A Pathogen Type III Effector with a Novel E3 Ubiquitin Ligase Architecture PLOS Pathog. 9, e1003121, (2013) DOI: 10.1371/journal.ppat.1003121

Type III effectors are virulence factors of Gram-negative bacterial pathogens delivered directly into host cells by the type III secretion nanomachine where they manipulate host cell processes such as the innate immunity and gene expression. Here, we show that the novel type III effector XopL from the model plant pathogen Xanthomonas campestris pv. vesicatoria exhibits E3 ubiquitin ligase activity in vitro and in planta, induces plant cell death and subverts plant immunity. E3 ligase activity is associated with the C-terminal region of XopL, which specifically interacts with plant E2 ubiquitin conjugating enzymes and mediates formation of predominantly K11-linked polyubiquitin chains. The crystal structure of the XopL C-terminal domain revealed a single domain with a novel fold, termed XL-box, not present in any previously characterized E3 ligase. Mutation of amino acids in the central cavity of the XL-box disrupts E3 ligase activity and prevents XopL-induced plant cell death. The lack of cysteine residues in the XL-box suggests the absence of thioester-linked ubiquitin-E3 ligase intermediates and a non-catalytic mechanism for XopL-mediated ubiquitination. The crystal structure of the N-terminal region of XopL confirmed the presence of a leucine-rich repeat (LRR) domain, which may serve as a protein-protein interaction module for ubiquitination target recognition. While the E3 ligase activity is required to provoke plant cell death, suppression of PAMP responses solely depends on the N-terminal LRR domain. Taken together, the unique structural fold of the E3 ubiquitin ligase domain within the Xanthomonas XopL is unprecedented and highlights the variation in bacterial pathogen effectors mimicking this eukaryote-specific activity.
Publications

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.
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