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Institut für Pflanzengenetik
Logo Leibniz Universität Hannover
Institut für Pflanzengenetik
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AG Boch Research Focus

Bacterial plant pathogens and their weapons.

Two organisms fight to survive. The prokaryote aims to acquire nutrients whereas the eukaryote aims to protects the integrity of its cells.

Plants are well able to defende themselves and only specialized pathogens can colonize them. These pathogens have evolved sophisticated molecular weapons. Pseudomonas syringae and Xanthomonas bacteria use a type III secretion system (T3SS) to inject ca. 30 different effector proteins into plant cells (Fig. 1). These effectors sabotage the host cell from within (Fig. 2) and we study their molecular activities.

 

Fig. 1: Electron microscopy picture of a bacterial cell with type III secretion system and secreted effectors. 

 

 

 

Fig. 1: Electron microscopy picture of a bacterial cell with type III secretion system and secreted effectors. Picture by Ian Brown. Healthy and infected Arabidopsis thaliana leaves are shown below.

Fig.2: Plant cells under attack. (1) Bacterial effector proteins (blue ball) are injected via a type III secretion system (red) into plant cells. (2) Inside the cell, effectors interact with host components and travel to subcellular locations. (3) TALEs from Xanthomonas bind to promoters inside the plant nucleus and induce expression of plant genes.

TALEs (transcription activator-like effectors) from rice-pathogenic Xanthomonas oryzae induce plant SWEET sugar exporters (Fig. 3). X. oryzae strains can harbour up to 26 different TALEs and we explore which plant genes are targeted.

 

Fig. 3: TALEs are molecular gene switches. Different TALEs induce the rice OsSWEET14 gene. The bacteria spread through the rice leaf veins and cause water-soaked lesions (black arrow).

 

 

Genome Editing

We have cracked the code how TALEs recognize DNA-sequences. They bind DNA via a central repeat domain. Each repeat recognizes one bp via two amino acids (called RVD) (Fig. 4). Different RVDs recognize different bases and different TALEs contain different arrangements of repeats. This modularity has been a breakthrough for biotechnology, because it allows to design artificial proteins with any desired DNA-binding specificity.

 

Fig. 4: DNA-binding specificity of TALEs. Each 34-amino acid-repeat binds to one DNA bp and the amino acids at position 12 and 13 in each repeat determine specificity.

 

Genome editing is a technique to specifically modify any sequence in a eukaryotic cell. This method holds great prospects for targeted breeding in agriculture and livestock, personalized medicine, and a cure to heritable genetic disorders in humans.

TALENs (TALE-nuclease fusions) and CRISPR/Cas (Fig. 5) are very recently developed tools that have heralded a new age for genome editing with worldwide interest. We explore these techniques to develop plants with elevated pathogen resistance and other beneficial traits.

 

Fig. 5: TALEN and CRISPR/Cas are key tools for genome editing.

 

 

 

 

Publications

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Original Publications

Streubel, J., Baum, H., Grau, J., Stuttman, J., and Boch, J.  (2017): Dissection of TALE-dependent gene activation reveals that they induce transcription cooperatively and in both orientations. , PLoS ONE 12, e0173580
DOI: http://dx.doi.org/10.1371/journal.pone.0173580

Volohonsky, G., Hopp, A.-K., Saenger, M., Soichot, J., Scholze, H., Boch, J., Blandin, S.A., Marois, E.  (2017): Transgenic expression of the anti-parasitic factor TEP1 in the malaria mosquito Anopheles gambiae, PLoS Pathog. 13, e1006113 weitere Informationen
DOI: 10.1371/journal.ppat.1006113

Becker, S., Boch, J.  (2016): Single-molecule biophysics: TALEs spin along, but not around, Nat. Chem. Biol. 12, 766-768 weitere Informationen

Grau, J., Reschke, M., Erkes, A., Streubel, J., Morgan, R.D., Wilson, G.G., Koebnik, R. and Boch, J.  (2016): AnnoTALE: bioinformatics tools for identification, annotation, and nomenclature of TALEs from Xanthomonas genomic sequences, Sci. Rep. 6, 21077 weitere Informationen
DOI: 10.1038/srep21077

Hutin, M., Césari, S., Chalvon, V., Michel, C., Tran, T.T., Boch, J., Koebnik, R., Szurek, B., and Kroj, T.  (2016): Ectopic activation of the rice NLR heteropair RGA4/RGA5 confers resistance to bacterial blight and bacterial leaf streak diseases, Plant J. 88, 43-55 weitere Informationen

Blanvillain-Baufumé, S., Reschke, M., Solé, M., Auguy, F., Doucoure, H., Szurek, B., Meynard, D., Portefaix, M., Cunnac, S., Guiderdoni, E., Boch, J., and Koebnik, R.  (2017): Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors, Plant Biotechnol. J. 15, 306-317 weitere Informationen
DOI: 10.1111/pbi.12613

Ordon, J., Gantner, J., Kemna, J., Schwalgun, L., Reschke, M., Streubel, J., Boch, J., and Stuttmann, J.  (2017): Generation of chromosomal deletions in dicotyledonous plants employing a user-friendly genome editing toolkit, Plant J. 89, 155-168 weitere Informationen
ISBN: 10.1111/tpj.13319

Geissler, R., Hauber, I., Funk, N., Richter, A., Behrens, M., Renner, I., Chemnitz, J., Hofmann-Sieber, H., Baum, H., van Lunzen, J., Boch, J., Hauber, J., and Behrens, S.E. (2015): Patient-adapted, specific activation of HIV-1 by customized TAL effectors (TALEs), a proof of principle study., Virology 488:248-254. weitere Informationen

Boch, J., Bonas, U., and Lahaye, T. (2014): TAL effectors - pathogen strategies and plant resistance engineering, New Phytol. 204, 823-832 weitere Informationen
DOI: 10.1111/nph.13015

Richter, A., Streubel, J., Blücher, C., Szurek, B., Reschke, M., Grau, J., and Boch, J. (2014): A TAL effector repeat architecture for frameshift binding., Nat. Commun. 5, 3447. weitere Informationen

Arrieta-Ortiz, M.L., Rodriguez-R., L.M., Perez-Quintero, A.L., Poulin, L., Diaz, A.C., Rojas, N.A., Trujillo, C., Restrepo Benavides, M., Bart, R., Boch, J., Boureau, T., Darrasse, A., David, P., Duge de Bernonville, T., Fontanilla, P., Gagnevin, L., Guerin, F., Jacques, M.-A., Lauber, E., Lefeuvre, P., Medina, C., Medina, E., Montenegro, N., Munoz Bodnar, A., Noel L.D., Ortiz Quinones, J.F., Osorio, D., Pardo, C., Patil, P.B., Poussier, S., Pruvost, O., Robene-Soustrade, I., Ryan, R.P., Tabima, J., Urrego Morales, O.G., Verniere, C., Carrere, S., Verdier, V., Szurek, B., Restrepo, S., Lopez, C., Koebnik, R., Bernal, A. (2013): Genomic survey of pathogenicity determinants and VNTR markers in the cassava bacterial pathogen Xanthomonas axonopodis pv. manihotis strain CIO151,  PLoS ONE 8, e79704 weitere Informationen
DOI: 10.1371/journal.pone.0079704

Grau, J., Boch, J., and Posch, S. (2013): TALENoffer: genome-wide TALEN off-target prediction. , Bioinformatics 29, 2931-2932. weitere Informationen

Grau, J., Wolf, A., Reschke, M., Bonas, U., Posch, S., and Boch, J.  (2013): Computational predictions provide insights into the biology of TAL effector target sites., PLoS Comp. Biol. 9, e1002962. weitere Informationen

Richter, A. and Boch, J. (2013): Designer TALEs team up for highly efficient gene induction. , Nat. Methods 10, 207-208. weitere Informationen

Streubel, J., Pesce, C., Hutin, M., Koebnik, R., Boch, J., and Szurek, B. (2013): Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. , New Phytol. 200, 808-819. weitere Informationen

Streubel, J., Richter, A., Reschke, M., and Boch, J.  (2013): TALEs - Proteine mit programmierbarer DNA-Bindespezifität. , BIOspektrum 19, 370-372. weitere Informationen

Nau-Wagner, G., Opper, D., Rolbetzki, A., Boch, J., Kempf, B., Hoffmann, T., and Bremer, E.  (2012): Genetic control of osmoadaptive glycine betaine synthesis in Bacillus subtilis through the choline-sensing and glycine betaine-responsive GbsR repressor. , J. Bacteriol. 194, 2703-2714. weitere Informationen

Streubel, J., Blücher, C., Landgraf, A., and Boch, J. (2012): TAL effector RVD specificities and efficiencies. , Nat. Biotechnol. 30, 593-595. weitere Informationen

Boch, J.  (2011): TALEs of genome targeting., Nat. Biotechnol. 29, 135-136. weitere Informationen

Geißler, R., Scholze, H., Hahn, S., Streubel, J., Bonas, U., Behrens, S.-E., and Boch, J. (2011): Transcriptional activators of human genes with programmable DNA-specificity. , PLoS ONE 6, e19509. weitere Informationen

Scholze, H. and Boch, J. (2011): TAL effectors are remote controls for gene activation., Curr. Opin. Microbiol. 14, 47-53. weitere Informationen

Yu, Y., Streubel, J., Balzergue, S., Champion, A., Boch, J., Koebnik, R., Feng, J.-X., Verdier, V., and Szurek, B. (2011): Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector which induces the rice nodulin-3 Os11N3 gene. , Mol. Plant-Microbe Interact. 24, 1102-1113. weitere Informationen

Boch, J. and Bonas, U. (2010): Xanthomonas AvrBs3 family-type III effectors: discovery and function. , Annu. Rev. Phytopathol. 48, 419-436. weitere Informationen

Morbitzer, R., Römer, P., Boch, J., and Lahaye, T.  (2010): Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors., Proc. Natl. Acad. Sci. USA 107, 21617-21622. weitere Informationen

Römer, P., Recht, S., Strauß, T., Elsaesser, J., Schornack, S., Boch, J., Wang, S., and Lahaye, T. (2010): Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen, Xanthomonas oryzae pv. oryzae. , New Phytol. 187, 1048-1057. weitere Informationen

Scholze, H. and Boch, J.  (2010): TAL effector-DNA specificity. , Virulence 1, 428-432. weitere Informationen

Boch, J., Scholze, H., Schornack S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A., and Bonas, U. (2009): Breaking the code of DNA binding specificity of TAL-type III effectors. , Science 326, 1509-1512; published online 29 October 2009 (10.1126/science.1178811). weitere Informationen

de Torres, M., Mansfield, J., Grabov, N., Brown, I.R., Ammouneh, H., Tsiamis, G., Forsyth, A., Robatzek, S., Grant, M., and Boch, J. (2006): Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis. , Plant J. 47, 368-382. weitere Informationen

Krause, A., Ramakumar, A., Bartels, D., Battistoni, F., Bekel, T., Boch, J., Böhm, M., Friedrich, F., Hurek, T., Krause, L., Linke, B., McHardy, A.C., Sarkar, A., Schneiker, S., Syed, A.A., Thauer, R., Vorhölter, F.J., Weidner, S., Pühler, A., Reinhold-Hurek, B., Kaiser, O., and Goesmann, A. (2006): Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. strain BH72., Nat. Biotechnol. 24, 1385-1391. weitere Informationen

Landgraf, A., Weingart, H., Tsiamis, H., and Boch, J. (2006): Different versions of Pseudomonas syringae pv. tomato DC3000 exist due to the activity of an effector transposon. , Mol. Plant Pathol. 7, 355-364. weitere Informationen

Kabisch, U., Landgraf, A., Krause, J., Bonas, U., and Boch, J.  (2005): Type III secretion chaperones ShcS1 and ShcO1 from Pseudomonas syringae pv. tomato DC3000 bind more than one effector., Microbiology 151, 269-280.

Kay, S., Boch, J., and Bonas, U.  (2005): Characterization of AvrBs3-like effectors from a Brassaceae pathogen reveals virulence and avirulence activities and a protein with a novel repeat architecture., Mol. Plant-Microbe Interact. 18, 838-848. weitere Informationen

Thieme, F., Koebnik, R., Bekel, T., Berger, C., Boch, J., Büttner, D., Caldana, C., Gaigalat, L., Goesmann, A., Kay, S., Kirchner, O., Lanz, C., Linke, B., McHardy, A. C., Meyer, F., Mittenhuber, G., Nies, D. H., Niesbach-Klösgen, U., Patschkowski, T., Rückert, C., Rupp, O., Schneiker, S., Schuster, S. C., Vorhölter, F., Weber, E., Pühler, A., Bonas, U., Bartels, D., and Kaiser, O.  (2005): Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence., J. Bacteriol. 187, 7254-7266. weitere Informationen

Boch, J., Joardar, V., Gao, L., Robertson, T.L., Lim, M., and Kunkel, B.N. (2002): Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. , Mol. Microbiol. 44, 73-88. weitere Informationen

Jackson, R.W., Mansfield, J.W., Ammouneh, H., Dutton, L.C., Wharton, B., Ortiz-Barredo, A., Arnold, D.L., Tsiamis, G., Sesma, A., Butcher, D., Boch, J., Kim, Y.J., Martin, G.B., Tegli, S., Murillo, J., and Vivian, A.  (2002): Location and activity of members of a family of virPphA homologues in pathovars of Pseudomonas syringae and P. savastanoi. , Mol. Plant Pathol. 3, 205-216. weitere Informationen

Chen, Z., Kloek, A.P., Boch, J., Katagiri, F., and Kunkel, B.N. (2000): The Pseudomonas syringae avrRpt2 gene product promotes pathogen virulence from inside plant cells. , Mol. Plant-Microbe Interact. 13, 1312-1321. weitere Informationen

Nennstiel, D., Boch, J., and Bonas, U. (2000): Bakterielle Phytopathogenese - Xanthomonas als Modellorganismus. , Biospektrum 6, 23-26.

Ullrich, M.S., Schergaut, M., Boch, J., and Ullrich, B.  (2000): Temperature-responsive genetic loci in the plant pathogen Pseudomonas syringae pv. glycinea., Microbiology 146, 2457-2468. weitere Informationen

Kappes, R.M., Kempf, B., Kneip, S., Boch, J., Gade, J., Meier-Wagner, J., and Bremer, E.  (1999): Two evolutionarily closely related ABC transporters mediate the uptake of choline for synthesis of the osmoprotectant glycine betaine in Bacillus subtilis., Mol. Microbiol. 32, 203-216. weitere Informationen

Nau-Wagner, G., Boch, J., Le Good, J.A., and Bremer, E.  (1999): High-affinity transport of choline-O-sulfate and its use as a compatible solute in Bacillus subtilis., Appl. Environ. Microbiol. 65, 560-568. weitere Informationen

Boch, J., Verbsky, M.L., Robertson, T.L., Larkin, J.C., and Kunkel, B.N. (1998): Analysis of resistance gene-mediated defense responses in Arabidopsis thaliana plants carrying a mutation in CPR5., Mol. Plant-Microbe Interact. 11, 1196-1206. weitere Informationen

Hettwer, U., Jaeckel, F.R., Boch, J., Meyer, M., Rudolph, K., and Ullrich, M.S. (1998): Cloning, nucleotide sequence, and expression in Escherichia coli of levansucrase genes from the plant pathogens Pseudomonas syringae pv. glycinea and P. syringae pv. phaseolicola. , Appl. Environ. Microbiol. 64, 3180-3187. weitere Informationen

Boch, J., Nau-Wagner, G., Kneip, S., and Bremer, E.  (1997): Glycine betaine aldehyde dehydrogenase from Bacillus subtilis: characterization of an enzyme required for the synthesis of the osmoprotectant glycine betaine., Arch. Microbiol. 168, 282-289. weitere Informationen

Boch, J., Kempf, B., Schmid, R., and Bremer, E. (1996): Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes., J. Bacteriol.. 178, 5121-5129. weitere Informationen

Boch, J., Kempf, B., and Bremer, E.  (1994): Osmoregulation in Bacillus subtilis: synthesis of the osmoprotectant glycine betaine from exogenously provided choline. , J. Bacteriol. 176, 5364-5371. weitere Informationen

Book Articles

Richter, A., Streubel, J., Boch, J.  (2016): TAL effector DNA-binding principles and specificitiy., TALENs - Methods and Protocols, R. Kühn, W. Wurst, B. Wefers, eds., (New York: Springer), Methods in Molecular Biology, Vol. 1338, pp. 9-25. weitere Informationen

Richter, A., Streubel, J., and Boch, J. (2015): TAL effector DNA-binding principles and specificity., In R. Kühn, W. Wurst, B. Wefers (Eds.), TALENs: Methods and Protocols. Methods in Molecuar Biology. Vol. 1338, New York: Springer. pp. 9-25 weitere Informationen

Boch, J.  (2009): The art of manipulation: bacterial type III effectors and their plant targets. , In Plant pathogenic bacteria: genomics and molecular biology, R.W. Jackson, ed (Norfolk, UK: Caister Academic Press), pp. 241-271. weitere Informationen

Boch, J., and Bonas, U. (2001): Gram-negative plant pathogenic bacteria., In Emerging Bacterial Pathogens, I. Mühldorfer and K.P. Schäfer, eds (Basel: Karger), pp. 186-196. weitere Informationen