We study the molecular interaction between different microbes and plants, focusing on (a) bacteria and (b) plant viruses. If you are interested to join us, please let us know!
The team is interested to learn how the different pathovars of the bacterium Xanthomonas campestris have adapted to colonize different plant tissue structures, i.e (i) 'the vasculature via hydathodes' - organelles present on the leaf margin - or (ii) 'the apoplastic space via stomata'. As model system, we use the model plant Arabidopsis thaliana. The lab uses advanced techniques like Phenomics, pan-genome analysis, genome-wide association studies, forward genetics screens and functional protein studies on bacterial virulence factors.
To this means, we developed a robust disease assay for X. campestris that stimulates ‘hydathode guttation and subsequent bacterial entry via re-uptake of guttation fluid (Van Hulten et al., 2019). This method allows us to dissect the genetic basis for bacterial ingress, both on the plant and bacterium side. We study the role of hydathodes as a passive and active immune barriere against bacteria. To study the disease progression in time, we have developped a bioluminescent reporter system that allows us to track the bacterial invasion via hydathodes and subsequent systemic spread in the vasculature. To image the immune response, we develop fluorescent reporter lines for the hydathode epithem tissue to compare its immune response to stomatal and apoplast immunity. In addition, these markers help us to visualize the integrity of the tissue.
We study Geminiviruses and Tospoviruses on Solanaceae, both Nicotiana benthamiana and tomato. Geminiviruses are ssDNA viruses that depend on the host DNA replication machinery for the replication of their viral DNA. We study the protein interaction between the essential viral protein Rep and the plant DNA replication machinery, in particular the DNA-clamp protein PCNA. Together with Wageningen University, we have performed a project to identify novel pro-viral factors for the Tospovirus Tomato spotted wilt virus (TSWV). We recently started a new collaboration studying two plant viruses that jointly cause Lettuce big-vein disease - a disease that is prominent in autumn and spring when the disease symptoms become visible as soon as the night temperature drops.
Key to the survival of any organism is the ability to defend itself. This defense response relies on transcriptional reprogramming in the first hours after invasion, and often results in programmed cell death and the accumulation of anti-microbial compounds. Our group revealed that SUMO acts as suppressor of plant immunity (Van den Burg et al., 2010). We found also that SUMO acts as 'hand-break' on plant growth via the ubiquitin E3 ligase COP1. This work also revealed that SUMO conjugation can trigger nuclear body formation, a process that closely resembles liquid-liquid phase seperations. In 2016, we reported on an evolutionary model of birth-and-death of SUMO paralogs in plants (Hammoudi et al., 2016). This model revealed that the paralog SUMO3 only recently evolved in the Brassicaceae plant family, while SUMO5 appears to be of ancient origin, as it ancestral gene emerged in hexaploidy event Gamma (that is near the base of the dicot species radiation ±120-135 mya). This evolutionary model elucidated as well that the Arabidopsis genes SUMO4/6 were only recently pseudogenized from an ancestral SUMO isoform. In a more recent effort, we demonstrated that SUMO impacts growth via two mechanisms at elevated ambient temperature (Hammoudi et al., 2018, Hammoudi, Beerens et al., 2021).
Molecular Plant Pathology is headed by Prof. dr. Martijn Rep. Within the University of Amsterdam, we are part of the Research theme Green Life Sciences within the Swammerdam Institute for Life Sciences (SILS), which consists of five disciplines: Molecular Plant Pathology, Plant Physiology, Plant Cell Biology, Plant Development & (Epi)Genetics, Plant Hormone Biology. Our researchers particpate in the education program of the MSc track Green Life Sciences (MSc Biological sciences) of our Faculty of Science. We participate in the Dutch graduate school Experimental Plant Sciences, which acts as a training and network platform for the PhD students and postdocs.
Former group members
Dr. Harrold A van den Burg is a molecular plant pathologist interested in basic and applied biology of plant-associated microbes that cause diseases on plants.
He graduated with a training in Biochemistry and Plant Pathology from Wageningen University (MSc Life Sciences, with distinction) in 1997. During his Ph.D. research (1997-2003) at Wageningen University, he discovered that fungal effectors act to shield the fungal cell wall by binding chitin (in the Laboratory of Phytopathology, Prof. Pierre JGM de Wit). For his postdoctoral research, Dr. van den Burg received a EU-Marie Curie fellowship to study Ubiquitin-dependent immune signaling in tomato (The Sainsbury Laboratory in Norwich (UK), Prof. Jonathan Jones).
In 2005, he was awared both an EMBO long-term fellowship and a NWO-Veni grant to develop a new research line at Molecular Plant Pathology in Amsterdam (with Dr. Frank LW Takken). This work initially focused on the role of the protein modification SUMO in plant immunity. In 2011, he started as Assistant professor, after receiving a NWO-Vidi fellowship, and he was promoted Associate professor in 2019.
The long-term research goal of Dr. Van den Burg is to unravel pathogenicity strategies of bacteria and plant viruses and to translate this knowledge on important crop diseases into breeding solutions for growers. The work in the lab is supported by different grants from the Dutch government with the aim to boost knowledge transfer to the industry (e.g. Topsector T&U).
Since 2015 his group studies both Bacterial Pathogenesis and Plant Virology. The lab developed for this purpose advanced high throughput methods for real-time imaging of bacteria inside plants.
The work on bacterial pathogenesis is focussed on the host entry mechanisms by the bacterium Xanthomonas campestris, where the group compares Xanthomonas strains that infect only the vasculature with strains that exclusively infect the apoplast via stomata.
The studies on plant virology are focussed on identifying host proteins that are manipulated by viral proteins to unravel pathways and/or processes that are manipulated by specific plant viruses during replication. The group studies different DNA and RNA viruses (e.g. Geminiviruses, Tospoviruses).
Helderman TA, Deurhof L, Bertran A, Richard MMS, Kormelink R, Prins M, Joosten MHAJ , Van den Burg HA* (2021). The Ribosomal Protein S6 (RPS6) family act as a pro-viral factor for Tomato spotted wilt orthotospovirus infectivity in Nicotiana benthamiana, Mol. Plant Pathol. doi:10.1111/mpp.13169
Helderman TA, Deurhof L, Bertran A, Boeren S, Fokkens L, Kormelink R, Joosten MHAJ , Prins M, Van den Burg HA* (2021). An isoform of the eukaryotic Translation Elongation Factor 1A (eEF1a) acts as a pro-viral factor required for Tomato spotted wilt virus disease in Nicotiana benthamiana, Viruses 13: 2190. doi: 10.3390/v13112190
Ingole KD, Kasera, M, van den Burg HA*, and Bhattacharjee S*. (2021) Antagonism between SUMO1/2 and SUMO3 regulates SUMO conjugate levels and fine-tunes immunity. J. Exp. Bot. 72: 6640-6658. doi: 10.1093/jxb/erab296 . * corresponding authors.
Hammoudi V*, Beerens B*, Jonker MJ, Helderman TA, Vlachakis G, Giesbers M, Kwaaitaal M, van den Burg HA (2021). The protein modifier SUMO is critical for integrity of the Arabidopsis shoot apex at warm ambient temperatures. J. Exp. Bot. 72: 7531–7548, doi: 10.1093/jxb/erab262, * shared 1st author.
Moretti C, Rezzonico F, Dorfei B, Cortese C, Moreno-Pérez A, Van den Burg HA, Onofri A, Firrao G, Ramos C, Smits THM, Buonaurio R (2021) Synergistic interaction between the type III secretion system of the endophytic bacterium Pantoea agglomerans DAPP-PG734 and the virulence of the causal agent of Olive knot Pseudomonas savastanoi pv. savastanoi DAPP-PG722. Mol. Plant Pathol. 22: 1209-1225; doi: 10.1111/mpp.13105
Trabalza S, Buonaurio R, Del Pino RM, Palmerini CA, van den Burg HA, Moretti C (2021). A Spectrofluorophotometrical method based on Fura-2-AM probe to determine cytosolic Ca2+ level in Pseudomonas syringae complex bacterial cells. Bio Protocols 11:e3949. doi: 10.21769/BioProtoc.3949.
Fang Q, Zhang Y, Zhang Y, Fan N, van den Burg HA, Huang CF 5 (2020). Regulation of Aluminum Resistance in Arabidopsis Involves the SUMOylation of the Zinc Finger Transcription Factor STOP1. Plant Cell 32: 3921-3938. doi: 10.1105/tpc.20.00687
Maio F, Helderman TA, Arroyo-Mateos M, van der Wolf M, Boeren S, Prins M, van den Burg HA* (2020). Identification of Tomato Proteins That Interact With Replication Initiator Protein (Rep) of the Geminivirus TYLCV. Frontiers in Plant Sciences 15;11;1069. doi: 10.3389/fpls.2020.01069
van Hulten M, Chatterjee S, van den Burg HA* (2019). Infection Assay for Xanthomonas campestris pv. campestris in Arabidopsis thaliana Mimicking Natural Entry via Hydathodes. Methods Mol. Biol. 991: 159–185.
Maio F, Arroyo-Mateos M, Bobay BG, Bejarano ER, Prins M, van den Burg HA* (2019). A Lysine Residue Essential for Geminivirus Replication Also Controls Nuclear Localization of the Tomato Yellow Leaf Curl Virus Rep Protein. J. Virol. 93: e01910-18.
Hammoudi V, Fokkens L, Beerens B, Vlachakis G, Chatterjee S, Arroyo-Mateos M, Wackers PFK, Jonker MJ, and van den Burg HA* (2018). The Arabidopsis SUMO E3 ligase SIZ1 mediates the temperature dependent trade-off between plant immunity and growth, PLoS Genetics 4: e1007157.
Arroyo-Mateos M, Sabarit B, Maio F, et al. (2018). Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites (2018). J. Virol. 92: e00611-18.
Mazur MJ, Spears BJ, Djajasaputra, A, Van der Gragt M, Vlachakis G, Beerens B, Gassmann W and van den Burg HA* (2017). Arabidopsis TCP Transcription Factors Interact with the SUMO Conjugating Machinery in Nuclear Foci. Frontiers in Plant Sciences, doi.org/10.3389/fpls.2017.02043
Hansen LL, van den Burg HA, van Ooijen G (2017). Sumoylation Contributes to Timekeeping and Temperature Compensation of the Plant Circadian Clock. J. Biol. Rhythms. Nov 1:748730417737633. doi: 10.1177/0748730417737633.
Hansen LL, Imrie L, Le Bihan T, van den Burg HA, van Ooijen G (2017) Sumoylation of the Plant Clock Transcription Factor CCA1 Suppresses DNA Binding. J. Biol. Rhythms. Nov 1:748730417737695. doi: 10.1177/0748730417737695.
Hammoudi V, Vlachakis G, de Jonge R, Breit TM, van den Burg HA* (2017) Genetic characterization of T-DNA insertions in the genome of the Arabidopsis thaliana sumo1/2 knock-down line, Plant Signal. Behav. 12(3): e1293216. doi: 10.1080/15592324.2017.1293216.
Zhao T, Holmer R, de Bruijn S, Angenent GC, van den Burg HA, Schranz ME (2017) Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation. Plant Cell. 29: 1278-1292. doi: 10.1105/tpc.17.00312
Hammoudi V, Vlachakis G, Schranz ME, van den Burg HA* (2016) Whole-genome duplications followed by tandem duplications drive diversification of the protein modifier SUMO in Angiosperms, New Phytol. 211: 172-85. doi: 10.1111/nph.13911
Ilyas M, Horger AC, Bozkurt TO, van den Burg HA, Kaschani F, Kaiser M, Belhaj K, Smoker M, Joosten MJHA, Kamoun S, and van der Hoorn RAL (2015), Functional Divergence of Two Secreted Immune Proteases of Tomato, Current Biology 25: 1-7.
Ma L, van den Burg HA, Cornelissen BJC and Takken FLW (2013) Molecular Basis of Effector Recognition by Plant NB-LRR Proteins, chapter 2 page 23-40. In Wiley-Blackwell, editor Sessa, G. eds. ISBN-13: 978-0470959503
De Wit, P.J.G.M.*, van der Burgt, A., Ökmen, B., Stergiopoulos, I., Abd-Elsalam, K., Aerts, A.L., Bahkali, A.H.A., Beenen, H.G., Chettri, P., Cox, M.P., Datema, E., de Vries, R.P., Dhillon, B., Ganley, A.R., Griffiths, S., Guo, Y., Hamelin, R.C., Henrissat, B., Kabir, M.S., Karimi Jashni, M., Kema, G., Klaubauf, S., Lapidus, A., Levasseur, A., Lindquist, E., Mehrabi, R., Ohm, R.A., Owen, T., Salamov, A., Schwelm, A., Schijlen, E., Sun, H., van den Burg, H.A., van Ham, R.C.H.J., Zhang, S., Goodwin, S.B., Grigoriev, I.V., Collemare, J., and Bradshaw, R.E.* (2012). The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genetics, 8:e1003088.
Stergiopoulos, I., van den Burg, H.A. , Ökmen, B., Beenen, H., Van Liere, S., Kema, G.H.J. and De Wit, P.J.G.M (2010).Tomato Cf resistance proteinsmediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots , Proc. Natl. Acad. Sci. USA .107: 7610-7615.
van Ooijen, G., Vossen, J.H., van den Burg, H.A., Roels, W., Cornelissen, B.J.C. and Takken F.L.W. (2010) HSP17 interacts with, and is required for function and stability of tomato resistance protein I-2, Plant Journal 63:563-572 .
de Wit, P.J.G.M., Mehrabi, R., van den Burg, H.A. and Stergiopoulos, I. (2009) , Fungal effector proteins: past, presence and future, Mol. Plant Pathol. 10(6):735-747.
van den Burg, H.A., and Takken, F.L.W. (2009) . Does chromatin remodeling mark systemic acquired resistance? Trends Plant Sci. 14, 286-294.
van den Burg, H.A., Tsitsigiannis, D.I., Rowland, O., Lo, J., Rallapalli, G., MacLean, D., Takken, F.L.W., and Jones, J.D.G. (2008) . The F-Box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato, Plant Cell 20 , 697-719.
Van Ooijen, G. , van den Burg H.A., Cornelissen,B.J.C., Takken F.L.W. (2007) Structure and Function of Resistance Proteins in Solanaceous Plants, Ann. Rev. Phytopathol. 40, 43-72.
van den Burg, H.A. , Harrison, S., Joosten, M.H.A.J., Vervoort, J. and de Wit, P.J.G.M. (2006) . Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection, Mol. Plant-Microbe Interact. 19, 1420-1430.
van den Burg, H.A. , Spronk, C.A.E.M., Boeren, S., Kennedy, M.A. Visser, J.P.C., Vuister, G.W., de Wit, P.J.G.M., and Vervoort, J. (2004) . Binding of the AVR4 elicitor of Cladosporium fulvum to chitotriose units is facilitated by positive allosteric protein-protein interactions , J. Biol. Chem. 279, 16786-16796.
van 't Slot, K.A.E., van den Burg, H.A. , Kloks, C.P.A.M., Hilbers, C.W., Knogge, W., and Papavoine, C.H.M. (2003) Solution structure of the fungal plant disease resistance-triggeringprotein NIP1 shows a novelbeta-sheet fold, J. Biol. Chem. 278, 45730-45736.
van den Burg,H.A. , Westerink, N.,Francoijs, K.-J., Roth,R.,Woestenenk, E., Boeren, S., de Wit, P.J.G.M., Joosten, M.H.A.J., and Vervoort, J. (2003) . Natural disulfide bond disrupted mutants of AVR4 of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, thereby, circumventing Cf-4mediated resistance, J. Biol. Chem. 278, 27340-27346.
Westerink, N., Roth, R., van den Burg, H.A. , de Wit , P.J.G.M., and Joosten, M.H.A.J. (2002) . The AVR4 elicitor protein of Cladosporium fulvum binds to fungal components with high affinity, Mol. Plant-Microbe Interact. 15, 1219-1227.
Rivas, S., Mucyn, T., van den Burg, H.A. , Vervoort, J., and Jones, J.D.G. (2002) . An ~400 kDa membrane-associated complex that contains one molecule of the resistance protein Cf-4, Plant J. 29,783-796.
de Wit, P.J.G.M., Brandtwagt, B.F., van den Burg, H.A. , Cai, X., van der Hoorn, R.A.L., de Jong, C.F., van Klooster, J., de Kock, M.J.D., Kruijt, M., Lindhout, W.H., Luderer, R., Takken, F.L., Westerink, N., Vervoort, J., and Joosten, M.H.A.J . (2002) .The molecular basis of co-evolution between Cladosporium fulvum and tomato, Antonie Van Leeuwenhoek 81, 409-412.
van den Burg, H.A. , de Wit, P.J.G.M., and Vervoort, J. (2001) . Efficient 13C/15N- double labeling of the avirulence protein AVR4in a methanol-utilizing strain (Mut(+)) of Pichia pastoris , J. Biomol. NMR 20, 251-261.
van den Hooven, H.W., van den Burg, H.A. , Vossen, P., Boeren, S., de Wit, P.J.G.M., and Vervoort, J. (2001) . Disulfide bond structure of the AVR9 elicitor of the fungal tomato pathogen Cladosporium fulvum : Evidence for a cystine knot, Biochemistry 40, 3458-3466.
Visser, A.J.W.G., van den Berg, P.A.W., Visser, N.V., van Hoek, A., van den Burg, H.A. , Parsonage, D., and Claiborne, A. (1998) . Time-resolved fluorescence of Flavin Adenine Dinucleotide in wild-type and mutant NADH Peroxidase. Elucidation of quenching sites and discovery of a new fluorescence depolarization mechanism, J. Phy. Chem B 102, 10431-10439.
van den Burg, H.A., de Wit, P.J.G.M., and Vervoort, J. (inventors) publication date 06/26/2003;Filing date:07/26/2002). Efficient 13C/15N double labeling of proteins in a methanol-utilizing strain (Mut+) of Pichia pastoris, US patent 20030119109.