SFB 648:  Molecular Mechanisms of Information Processing in Plants

• Subject Area: Biology ; Medicine
• Term: from 2005 to 2016
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 5486253

• Final Report Year: 2017

Final Report Abstract

Plant growth, development and defense reactions are highly flexible processes which are regulated in response to external abiotic stimuli or biotic factors such as pathogens or herbivores. Adaptation of plants to environmental conditions involves effective sensing mechanisms as well as intracellular and intraorganismal information processing. Understanding the principles of information processing in plants and plant-pathogen interactions was one of the major goals of the CRC 648. Research projects were divided into three multidisciplinary and intersecting areas, which focused on the interaction of plants with phytopathogenic organisms (project area A), intracellular plant signaling networks (project area B) and signal processing events with a focus on epigenetic control mechanisms (project area C). Plant signaling and defense pathways involved in plant-pathogen interactions (project area A) were studied in response to infections by the bacterial tomato and pepper pathogen Xanthomonas campestris pv. vesicatoria, the fungus and cereal pathogen Colletotrichum graminicola, the oomycete Phytophthora infestans and Tomato Bushy Stunt Virus, which serves as a model system for the analysis of positivesense single-stranded RNA viruses. Research topics associated with pathogen-induced signal processing included bacterial adaptation to environmental conditions, delivery and functional characterization of bacterial effector proteins as well as viral replication mechanisms. The analysis of plant reactions in response to pathogen attack focused on the induction of basal defense reactions elicited by pathogenassociated molecular patterns (PAMPs) or viral RNAs. Major achievements include the elucidation of the function of the transcription activator-like (TAL) effector AvrBs3 and the cloning of the corresponding plant resistance gene. Furthermore, a cell-free plant system for the analysis of viral replication and virusinduced RNA silencing was developed, and plant proteins involved in PAMP recognition were identified. Research on intracellular signaling networks in plants (project area B) included the analysis of mitogenactivated protein kinase (MAPK) cascades and calcium signaling in response to environmental stimuli. In addition, the role of phosphoinositides and inositol-polyphosphates during plant defense and phytohormone signaling as well as the regulation of terpene biosynthesis in response to herbivory were studied. An additional research topic was the analysis of the plant Elongator complex, which is involved in tRNA modification and impacts on various plant pathways including leaf growth, development and defense responses. Important findings include the identification of chloroplastic calcium transporters and the discovery of novel MAPK substrates such as a member of the IQD protein family, which provides a link between MAPK and calcium signaling. IQD proteins are involved in signal processing and contribute to cell morphogenesis by their interaction with microtubules. The signal processing events studied in project area C included epigenetic mechanisms that control heterochromatic gene silencing and the role of Aurora kinases in cell-cycle control and epigenetic regulation. The establishment of a luciferase-based transgene assay system fostered the analysis of repeatdependent transcriptional gene silencing and led to the identification of new plant silencing suppressors. A new project in the last period of the CRC, which established Colletotrichum graminicola as a model system for epigenetic analyses, demonstrated that fungal virulence is under epigenetic control. A major scientific highlight was the identification of the first known protein-encoding gene on a plant B chromosome, which is a dispensable part of the nuclear genome and was considered to lack functional genes. The multi-disciplinary collaborations established between the different projects of this CRC with focus on genetics, epigenetics, biochemistry or cell biology significantly fostered a better understanding of fundamental questions in plant biology. The results provide an excellent basis for future research networks.

Publications

• (2006) The Arabidopsis SUVR4 protein is a nucleolar histone methyltransferase with preference for monomethylated H3K9. Nucl Acid Res 34: 5461-5470
  Thorstensen T, Fischer A, Sandvik SV, Johnson SS, Grini P, Reuter G and Aalen R
  
• (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318: 648-651
  Kay S, Hahn S, Marois E, Hause G and Bonas U
  
• (2007) Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318: 645-648
  Römer P, Hahn S, Jordan T, Strauß T, Bonas U and Lahaye T
  
• (2007) Prerequisites for terminal processing of thylakoidal Tat substrates J Biol Chem 282: 24455-24462
  Frielingsdorf S and Klösgen RB
  
• (2007) Salicylic acid affects susceptibility of Solanum tuberosum to Phytophthora infestans. Mol Plant-Microbe Interact 20: 1346-1352
  Halim VA, Eschen-Lippold E, Altmann, S, Birschwilks M, Scheel D and Rosahl S
  
• (2008) Bs3 resistance gene and methods of use. Patent No. PCT/US2008/077639
  Bonas U, Lahaye T and Römer P
  
• (2008) HpaC controls substrate specificity of the Xanthomonas type III secretion system. PLoS Path 4: e1000094
  Lorenz C, Schulz S, Wolsch T, Rossier-Conway O, Bonas U and Büttner D
  
• (2009) Aurora1 phosphorylation activity on histone H3 and its cross-talk with other posttranslational histone modifications in Arabidopsis. Plant J 59: 221-230
  Demidov D, Hesse S, Tewes A, Rutten T, Fuchs J, Ashtiyani RK, Lein S, Fischer A, Reuter G and Houben A
  
• (2009) Breaking the code of DNA-binding specificity of TAL-type III effectors. Science 326: 1509-1512
  Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A and Bonas U
  
• (2009) Epigenetic programming via histone methylation at WRKY53 controls leaf senescence in Arabidopsis thaliana. Plant J 58: 333-346
  Ay N, Irmler K, Fischer A, Uhlemann R, Reuter G and Humbeck K
  
• (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci USA 106: 8067-8072
  Bethke G, Unthan T, Uhrig JF, Pöschl Y, Gust AA, Scheel D and Lee J
  
• (2009) Recognition of AvrBs3-like proteins is mediated by specific binding to promoters of matching pepper Bs3 alleles. Plant Physiol 150: 1697-1712
  Römer P, Strauss T, Hahn S, Scholze H, Morbitzer R, Grau J, Bonas U and Lahaye T
  
• (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci USA 106: 13213-13218
  Degenhardt J, Hiltpold I, Köllner T G, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR and Turlings TCJ
  
• (2010) Elongator function in tRNA wobble uridine modification is conserved between yeast and plants. Mol Microbiol 76: 1082-1094
  Mehlgarten C, Jablonowski D, Wrackmeyer U, Tschitschmann S, Sondermann D, Jäger G, Gong Z, Byström AS, Schaffrath R and Breunig KD
  
• (2010) Functional characterization of the Xcs and Xps type II secretion ATPase HrcN from the plant pathogen Xanthomonas campestris pv. vesicatoria. New Phytol 187: 983-1002
  Szczesny R, Jordan M, Schramm C, Schulz S, Cogez V, Bonas U and Büttner D
  
• (2010) Herbivoreinduced SABATH methyltransferases of maize that methylate anthranilic acid using S-adenosyl-L- methionine. Plant Physiol 153: 1795-1807
  Köllner TG, Lenk C, Zhao N, Seidl-Adams I, Gershenzon J, Chen F and Degenhardt J
  
• (2010) Modular DNA-binding domains and methods of use. Patent No. PCT/IB2010/000154
  Bonas U, Boch J, Schornack S and Lahaye T
  
• (2010) Pathogen-inducible promoters and their use in enhancing the disease resistance of plants. Patent No. PCT/US2009/063791
  Lahaye T, Römer P, Schornack S, Boch J and Bonas U
  
• (2010) Polynucleotides encoding caryophyllene synthase and uses thereof. European Patent Office WO2010049506 A2
  Degenhardt J, Köllner TG, Gershenzon J, Crocoll C, Turlings TCJ, Hiltpold I
  
• (2010) Suppression of the AvrBs1- specific hypersensitive response by the YopJ effector homolog AvrBsT from Xanthomonas depends on a SNF1-related kinase. New Phytol 187: 1058-1074
  Szczesny R, Büttner D, Escolar L, Schulze S, Seiferth A and Bonas U
  
• (2011) Secretion of early and late substrates of the type III secretion system from Xanthomonas is controlled by HpaC and the C-terminal domain of HrcU. Mol Microbiol 79: 447-467
  Lorenz C and Büttner D
  
• (2011) The SUVR4 histone lysine methyltransferase binds ubiquitin and converts H3K9me1 to H3K9me3 on transposon chromatin in Arabidopsis. PloS Genetics 7: e1001325
  Veiseth SV, Rahman MA, Yap KL, Fischer A, Egge-Jacobsen W, Reuter G, Zhou M-M, Aalen H and Thorstensen T
  
• (2012) Activation of defense against Phytophthora infestans in potato by down-regulation of syntaxin gene expression. New Phytol 193: 985-996
  Eschen-Lippold L, Landgraf R, Smolka U, Schulze S, Heilmann M, Heilmann I, Hause G and Rosahl S
  (See online at https://doi.org/10.1111/j.1469-8137.2011.04024.x)
• (2012) Analysis of new type III effectors from Xanthomonas uncovers XopB and XopS as suppressors of plant immunity. New Phytol 195: 894-911
  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 and Bonas U
  (See online at https://doi.org/10.1111/j.1469-8137.2012.04210.x)
• (2012) Remodeling of cytokinin metabolism at infection sites of Colletotrichum graminicola on maize leaves. Mol-Plant-Microbe Interact 25: 1073-1082
  Behr M, Motyka V, Weihmann F, Malbeck J, Deising HB and Wirsel SG
  (See online at https://doi.org/10.1094/MPMI-01-12-0012-R)
• (2012) Variable regions of PI4P 5-kinases direct PtdIns(4,5)P2 towards alternative regulatory functions in tobacco pollen tubes. Front Plant Sci 2: 114
  Stenzel I, Ischebeck T, Quint M and Heilmann I
  (See online at https://doi.org/10.3389/fpls.2011.00114)
• (2012). IDN2 has a role downstream of siRNA formation in RNA- directed DNA methylation. Epigenetics 7: 950-960
  Finke A, Kuhlmann M and Mette MF
  (See online at https://doi.org/10.4161/epi.21237)
• (2013) A pathogen type III effector with a novel E3 ubiquitin ligase architecture. PLoS Pathog 9: e1003121
  Singer AU, Schulze S, Skarina T, Xu X, Cui H, Eschen-Lippold L, Egler M, Srikumar T, Raught B, Lee J, Scheel D, Savchenko A and Bonas U
  (See online at https://doi.org/10.1371/journal.ppat.1003121)
• (2013) AGO/RISC-mediated antiviral RNA silencing in a plant in vitro system. Nucleic Acids Res 41: 5090-5103
  Schuck J, Gursinsky T, Pantaleo V, Burgyán J and Behrens SE
  (See online at https://doi.org/10.1093/nar/gkt193)
• (2014) Altered expression of Aurora kinases in Arabidopsis results in aneu- and polyploidization. Plant J 80: 449-461
  Demidov D, Lermontova I, Weiss O, Fuchs J, Rutten T, Kumke K, Sharbel TF, Van Damme D, De Storme N, Geelen D and Houben A
  (See online at https://doi.org/10.1111/tpj.12647)
• (2014) Repeat 1 of TAL effectors affects target specificity for the base at position zero. Nucleic Acids Res 42: 7160-7169
  Schreiber T and Bonas U
  (See online at https://doi.org/10.1093/nar/gku341)
• (2014) The ABC transporter ABCG1 is required for suberin formation in potato tuber periderm. Plant Cell 26: 3403-3411
  Landgraf R, Smolka U, Altmann S, Eschen-Lippold L, Senning M, Sonnewald S, Weigel B, Frolova N, Strehmel N, Hause G, Scheel D, Böttcher C and Rosahl S
  (See online at https://doi.org/10.1105/tpc.114.124776)
• (2014) The Arabidopsis thaliana mitogen-activated protein kinases MPK3 and MPK6 target a subclass of 'VQ-motif'-containing proteins to regulate immune responses. New Phytol 203: 592-606
  Pecher P, Eschen-Lippold L, Herklotz S, Kuhle K, Naumann K, Bethke G, Uhrig J, Weyhe M, Scheel D and Lee J
  (See online at https://doi.org/10.1111/nph.12817)
• (2015) Homeologs of the Nicotiana benthamiana antiviral ARGONAUTE1 show different susceptibilities to microRNA168- mediated control. Plant Physiol 168: 938-952
  Gursinsky T, Pirovano W, Gambino G, Friedrich S, Behrens SE and Pantaleo V
  (See online at https://doi.org/10.1104/pp.15.00070)
• (2016) Arabidopsis thaliana DM2h (R8) within the Landsberg RPP1-like resistancel locus underlies three different cases of EDS1-conditioned autoimmunity. PLoS Genet 12: e1005990
  Stuttmann J, Peine N, Garcia AV, Wagner C, Choudhury SR, Wang Y, James GV, Griebel T, Alcazar R, Tsuda K, Schneeberger K and Parker JE
  (See online at https://doi.org/10.1371/journal.pgen.1005990)
• (2016) Bacterial AvrRpt2-like cysteine proteases block activation of the Arabidopsis mitogen-activated protein kinases, MPK4 and MPK11. Plant Physiol 171: 2223-2238
  Eschen-Lippold L, Jiang X, Elmore J M, Mackey D, Shan L, Coaker G, Scheel D and Lee J
  (See online at https://doi.org/10.1104/pp.16.00336)
• (2016) Characterization of biosynthetic pathways for the production of the volatile homoterpenes DMNT and TMTT in Zea mays. Plant Cell 28: 2651-2665
  Richter A, Schaff C, Zhang Z, Lipka AE, Tian F, Köllner TG, Schnee C, Preiß S, Irmisch S, Jander G, Boland W, Gershenzon J, Buckler ES and Degenhardt J
  (See online at https://doi.org/10.1105/tpc.15.00919)
• (2016) Generation of chromosomal deletions in dicotyledonous plants employing a user-friendly genome editing toolkit. Plant J 89: 155-168
  Ordon J, Gantner J, Kemna J, Schwalgun L, Reschke M, Streubel J, Boch J and Stuttmann J
  (See online at https://doi.org/10.1111/tpj.13319)
• (2016) Non-host resistance induced by the Xanthomonas effector XopQ is widespread within the genus Nicotiana and functionally depends on EDS1. Front Plant Sci 7: 1796
  Adlung N, Prochaska H, Thieme S, Banik A, Blüher D, John P, Nagel O, Schulze S, Gantner J, Delker C, Stuttmann J and Bonas, U
  (See online at https://doi.org/10.3389/fpls.2016.01796)
• (2016) Structural basis for tRNA modification by Elp3 from Dehalococcoides mccartyi. Nat Struct Biol 23: 794-802
  Glatt S, Zabel R, Kolaj-Robin O, Onuma OF, Baudin F, Graziadei A, Taverniti V, Lin TY, Baymann F, Séraphin B, Breunig KD and Müller CW
  (See online at https://doi.org/10.1038/nsmb.3265)
• (2017) Architecture of the yeast Elongator complex, EMBO Rep 18: 264-279
  Dauden MI, Kosinski J, Kolaj-Robin O., Desfosses A., Ori A, Faux C, Hoffmann NA, Onuma OF, Breunig KD, Beck M, Sachse C, Seraphin B, Glatt S and Müller CW
  (See online at https://doi.org/10.15252/embr.201643353)
• (2017) Rye B chromosomes encode a functional Argonaute-like protein with in vitro slicer activities similar to its A chromosome paralog. New Phytol 213: 916-928
  Ma W, Gabriel TS, Martis MM, Gursinsky T, Schubert V, Vrana J, Dolezel J, Grundlach H, Altschmied L, Scholz U, Himmelbach A, Behrens SE, Banaei-Moghaddam AM and Houben A
  (See online at https://doi.org/10.1111/nph.14110)
• (2017) The IQD family of calmodulin-binding proteins links calcium signaling to MTs, membrane subdomains, and the nucleus. Plant Physiol 173: 1692-1708
  Bürstenbinder K, Möller B, Plötner R, Stamm G, Hause G, Mitra, D and Abel S
  (See online at https://doi.org/10.1104/pp.16.01743)
• (2017) The predicted lytic transglycosylase HpaH from Xanthomonas campestris pv. vesicatoria associates with the type III secretion system and promotes effector protein translocation. Infect Immunol 85: e00788-16
  Hausner J, Hartmann N, Jordan M and Büttner D
  (See online at https://doi.org/10.1128/IAI.00788-16)