University of Dundee

Dr Edgar Huitema

Mechanisms of virulence acquisition during Phytophthora-host associations
Position: 
Senior Lecturer
Affiliation: 
Address: 
University of Dundee at JHI, Errol Road, Invergowrie, Dundee
Full Telephone: 
+44 (0) 1382 568921, int ext
Email: 

Research

Investigation of Phytophthora-host associations. Left panel: N. benthamiana leaf inoculated with P. capsici zoospores. P. capsici infection features an eary biotrophic stage, tissue darkening and necrosis, tissue maceration and sporulation. Right panel: Ectopic expression of pathogen genes in tobacco cells induces cell death. Secreted pathogen proteins target and modify host cellular components. Ectopic expression of such proteins often leads to phenotypic manifestations such as cell death, reflecting functional roles towards virulence.

For more information about the Huitema Lab, please visit our Group webpage.

Publications

Stam R, Motion GB, Martinez Heredia V, Boevink P, Huitema E. 2021. A conserved oomycete CRN effector targets tomato TCP14-2 to enhance virulence. Molecular Plant - Microbe Interactions. 34(3):309-318. https://doi.org/10.1094/MPMI-06-20-0172-R

Thilliez GJA, Armstrong M, Lim JT-Y, Baker K, Jouet A, Ward B, Oosterhout CV, Jones JDG, Huitema E, Birch P, Hein I. 2019. Pathogen enrichment sequencing (PenSeq) enables population genomic studies in oomycetes. New Phytologist. 221(3):1634-1648. https://doi.org/10.1111/nph.15441

Pham J, Stam R, Heredia VM, Csukai M, Huitema E. 2018. An NMRA-like protein regulates gene expression in Phytophthora capsici to drive the infection cycle on tomato. Molecular Plant - Microbe Interactions. 31(6):665-677. https://doi.org/10.1094/MPMI-07-17-0193-R

Amaro TMM, Thilliez GJA, Mcleod RA, Huitema E. 2018. Random mutagenesis screen shows that Phytophthora capsici CRN83_152 mediated cell death is not required for its virulence function(s). Molecular Plant Pathology. 19(5):1114-1126. https://doi.org/10.1111/mpp.12590

Amaro TMMM, Thilliez GJA, Motion GB, Huitema E. 2017. A Perspective on CRN Proteins in the Genomics Age: Evolution, Classification, Delivery and Function Revisited. Frontiers in Plant Science. 8:1-12. https://doi.org/10.3389/fpls.2017.00099

Cummins M, Huitema E. 2017. Effector-Decoy Pairs: Another Countermeasure Emerging during Host-Microbe Co-evolutionary Arms Races?. Molecular Plant. 10(5):662-664. https://doi.org/10.1016/j.molp.2017.03.008

Howden AJM, Stam R, Martinez Heredia V, Motion GB, Hodge K, ten Have S, Marques Monteiro Amaro TM, Huitema E. 2017. Quantitative analysis of the tomato nuclear proteome during Phytophthora capsici infection unveils regulators of immunity. New Phytologist. 215(1):309-322. https://doi.org/10.1111/nph.14540

Motion GB, Howden A, Huitema E, Jones S. 2015. DNA-binding protein prediction using plant specific support vector machines: validation and application of a new genome annotation tool. Nucleic Acids Research. 43(22):Article gvk805. https://doi.org/10.1093/nar/gkv805

Motion GB, Marques Monteiro Amaro TM, Kulagina N, Huitema E. 2015. Nuclear processes associated with plant immunity and pathogen susceptibility. Briefings in Functional Genomics. 14(4):243-252. https://doi.org/10.1093/bfgp/elv013

Lamour K, Hu J, Lefebvre V, Mudge J, Howden A, Huitema E. 2014. Illuminating the Phytophthora capsici Genome. Dean RA, Lichens-Park A, Kole C, editors. In Genomics of Plant-Associated Fungi and Oomycetes: Dicot Pathogens. Berlin: Springer . pp. 121-132. https://doi.org/10.1007/978-3-662-44056-8_6

Jupe J, Stam R, Howden AJM, Morris JA, Zhang R, Hedley PE, Huitema E. 2013. Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biology. 14(6):R63. https://doi.org/10.1186/gb-2013-14-6-r63

Stam R, Jupe J, Howden AJM, Morris JA, Boevink PC, Hedley PE, Huitema E. 2013. Identification and Characterisation CRN Effectors in Phytophthora capsici Shows Modularity and Functional Diversity. PLoS ONE. 8(3):Article e59517. https://doi.org/10.1371/journal.pone.0059517

Stam R, Howden AJM, Delgado Cerezo M, Amaro TMMM, Motion GB, Pham J, Huitema E. 2013. Characterization of cell death inducing Phytophthora capsici CRN effectors suggests diverse activities in the host nucleus. Frontiers in Plant Science. 4:Article 387. https://doi.org/10.3389/fpls.2013.00387

Howden AJM, Huitema E. 2012. Effector-triggered post-translational modifications and their role in suppression of plant immunity. Frontiers in Plant Science. 3(July):Article 160. https://doi.org/10.3389/fpls.2012.00160

Lamour KH, Stam R, Jupe J, Huitema E. 2012. The oomycete broad-host-range pathogen Phytophthora capsici. Molecular Plant Pathology. 13(4):329-337. https://doi.org/10.1111/j.1364-3703.2011.00754.x

Lamour KH, Mudge J, Gobena D, Hurtado-Gonzales OP, Schmutz J, Kuo A, Miller NA, Rice BJ, Raffaele S, Cano LM, Bharti AK, Donahoo RS, Finley S, Huitema E, Hulvey J, Platt D, Salamov A, Savidor A, Sharma R, Stam R, Storey D, Thines M, Win J, Haas BJ, Dinwiddie DL, Jenkins J, Knight JR, Affourtit JP, Han CS, Chertkov O, Lindquist EA, Detter C, Grigoriev IV, Kamoun S, Kingsmore SF. 2012. Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Molecular Plant - Microbe Interactions. 25(10):1350-60. https://doi.org/10.1094/MPMI-02-12-0028-R

Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M, Oliva R, Cano LM, Jones AME, Huitema E, van der Hoorn RAL, Kamoun S. 2011. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proceedings of the National Academy of Sciences of the United States of America. 108(51):20832-20837. https://doi.org/10.1073/pnas.1112708109

Green S, Studholme DJ, Laue BE, Dorati F, Lovell H, Arnold D, Cottrell JE, Bridgett S, Blaxter M, Huitema E, Thwaites R, Sharp PM, Jackson RW, Kamoun S. 2010. Comparative Genome Analysis Provides Insights into the Evolution and Adaptation of Pseudomonas syringae pv. aesculi on Aesculus hippocastanum. PLoS ONE. 5(4):-. https://doi.org/10.1371/journal.pone.0010224

Hughes HV, Huitema E, Pritchard S, Keiler KC, Brun YV, Viollier PH. 2010. Protein localization and dynamics within a bacterial organelle. Proceedings of the National Academy of Sciences of the United States of America. 107(12):5599-5604. https://doi.org/10.1073/pnas.0909119107

Levesque CA, Brouwer H, Cano L, Hamilton JP, Holt C, Huitema E, Raffaele S, Robideau GP, Thines M, Win J, Zerillo MM, Beakes GW, Boore JL, Busam D, Dumas B, Ferriera S, Fuerstenberg SI, Gachon CMM, Gaulin E, Govers F, Grenville-Briggs L, Horner N, Hostetler J, Jiang RHY, Johnson J, Krajaejun T, Lin H, Meijer HJG, Moore B, Morris P, Phuntmart V, Puiu D, Shetty J, Stajich JE, Tripathy S, Wawra S, van West P, Whitty BR, Coutinho PM, Henrissat B, Martin F, Thomas PD, Tyler BM, De Vries RP, Kamoun S, Yandell M, Tisserat N, Buell CR. 2010. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biology. 11(7):-. https://doi.org/10.1186/gb-2010-11-7-r73

Oliva R, Win J, Raffaele S, Boutemy L, Bozkurt TO, Chaparro-Garcia A, Segretin ME, Stam R, Schornack S, Cano LM, van Damme M, Huitema E, Thines M, Banfield MJ, Kamoun S. 2010. Recent developments in effector biology of filamentous plant pathogens. Cellular Microbiology. 12(6):705-715. https://doi.org/10.1111/j.1462-5822.2010.01471.x

Oliva R, Win J, Raffaele S, Boutemy L, Bozkurt TO, Chaparro-Garcia A, Segretin ME, Stam R, Schornack S, Cano LM, van Damme M, Huitema E, Thines M, Banfield MJ, Kamoun S. 2010. Recent developments in effector biology of filamentous plant pathogens (vol 12, pg 705, 2010). Cellular Microbiology. 12(7):1015-1015. https://doi.org/10.1111/j.1462-5822.2010.01484.x

Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M, Thines M, Gaulin E, Kamoun S, Huitema E. 2010. Ancient class of translocated oomycete effectors targets the host nucleus. Proceedings of the National Academy of Sciences of the United States of America. 107(40):17421-17426. https://doi.org/10.1073/pnas.1008491107

Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, Bozkurt TO, Ah-Fong AMV, Alvarado L, Anderson VL, Armstrong MR, Avrova A, Baxter L, Beynon J, Boevink PC, Bollmann SR, Bos JIB, Bulone V, Cai G, Cakir C, Carrington JC, Chawner M, Conti L, Costanzo S, Ewan R, Fahlgren N, Fischbach MA, Fugelstad J, Gilroy EM, Gnerre S, Green PJ, Grenville-Briggs LJ, Griffith J, Gruenwald NJ, Horn K, Horner NR, Hu C-H, Huitema E, Jeong D-H, Jones AME, Jones JDG, Jones RW, Karlsson EK, Kunjeti SG, Lamour K, Liu Z, Ma L, MacLean D, Chibucos MC, McDonald H, McWalters J, Meijer HJG, Morgan W, Morris PF, Munro CA, O'Neill K, Ospina-Giraldo M, Pinzon A, Pritchard L, Ramsahoye B, Ren Q, Restrepo S, Roy S, Sadanandom A, Savidor A, Schornack S, Schwartz DC, Schumann UD, Schwessinger B, Seyer L, Sharpe T, Silvar C, Song J, Studholme DJ, Sykes S, Thines M, van de Vondervoort PJI, Phuntumart V, Wawra S, Weide R, Win J, Young C, Zhou S, Fry W, Meyers BC, van West P, Ristaino J, Govers F, Birch PRJ, Whisson SC, Judelson HS, Nusbaum C. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature. 461(7262):393-398. https://doi.org/10.1038/nature08358

Schornack S, Fuchs R, Huitema E, Rothbauer U, Lipka V, Kamoun S. 2009. Protein mislocalization in plant cells using a GFP-binding chromobody. Plant Journal. 60(4):744-754. https://doi.org/10.1111/j.1365-313X.2009.03982.x

Schornack S, Huitema E, Cano LM, Bozkurt TO, Oliva R, van Damme M, Schwizer S, Raffaele S, Chaparro-Garcia A, Farrer R, Segretin ME, Bos JIB, Haas BJ, Zody MC, Nusbaum C, Win J, Thines M, Kamoun S. 2009. Ten things to know about oomycete effectors. Molecular Plant Pathology. 10(6):795-803. https://doi.org/10.1111/j.1364-3703.2009.00593.x

Huitema E, Viollier PH. 2007. Break on through to the other side: outer membrane penetration of the nascent flagellum by a stop-polymerization mechanism. Genes & Development. 21(18):2253-2257. https://doi.org/10.1101/gad.1600807

Bos JIB, Kanneganti T-D, Young C, Cakir C, Huitema E, Win J, Armstrong MR, Birch PRJ, Kamoun S. 2006. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant Journal. 48(2):165-176. https://doi.org/10.1111/j.1365-313X.2006.02866.x

Huitema E, Pritchard S, Matteson D, Radhakrishnan SK, Viollier PH. 2006. Bacterial birth scar proteins mark future flagellum assembly site. Cell. 124(5):1025-1037

Huitema E, Viollier PH. 2006. A rnyxobacterial S-motility protein dances with poles. Trends in Microbiology. 14(6):247-248. https://doi.org/10.1016/j.tim.2006.04.002

Kanneganti T-D, Huitema E, Cakir C, Kamoun S. 2006. Synergistic interactions of the plant cell death pathways induced by Phytophthora infestans Nep1-like protein PiNPP1.1 and INF1 elicitin. Molecular Plant - Microbe Interactions. 19(8):854-863. https://doi.org/10.1094/MPMI-19-0854

Huitema E, Vleeshouwers VGAA, Cakir C, Kamoun S, Govers F. 2005. Differences in intensity and specificity of hypersensitive response induction in Nicotiana spp. by INN, INF2A, and INF2B of Phytophthora infestans. Molecular Plant - Microbe Interactions. 18(3):183-193. https://doi.org/10.1094/MPMI-18-0183

Randall TA, Dwyer RA, Huitema E, Beyer K, Cvitanich C, Kelkar H, Ah Fong AMV, Gates K, Roberts S, Yatzkan E, Gaffney T, Law M, Testa A, Torto-Alalibo T, Zhang M, Zheng L, Mueller E, Windass J, Binder A, Birch PRJ, Gisi U, Govers F, Gow NA, Mauch F, van West P, Waugh ME, Yu J, Boller T, Kamoun S, Lam ST, Judelson HS. 2005. Large-scale gene discovery in the oomycete Phytophthora infestans reveals likely components of phytopathogenicity shared with true fungi. Molecular Plant - Microbe Interactions. 18(3):229-243. https://doi.org/10.1094 / MPMI -18-0229

Huitema E, Dong S, Hamada W, Kamoun S. 2004. Dissection of nonhost resistance of Arabidopsis to Phytophthora infestans. Phytopathology. 94(6):S159.

Huitema E, Bos JIB, Tian M, Win J, Waugh ME, Kamoun S. 2004. Linking sequence to phenotype in Phytophthora-plant interactions. Trends in Microbiology. 12(4):193-200. https://doi.org/10.1016/j.tim.2004.02.008

Tian M, Huitema E, da Cunha L, Torto-Alalibo T, Kamoun S. 2004. A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. Journal of Biological Chemistry. 279(25):26370-26377

Huitema E, Vleeshouwers VGAA, Francis DM, Kamoun S. 2003. Active defence responses associated with non-host resistance of Arabidopsis thaliana to the oomycete pathogen Phytophthora infestans. Molecular Plant Pathology. 4(6):487-500. https://doi.org/10.1046/J.1364-3703.2003.00195.X

Kamoun S, Hamada W, Huitema E. 2003. Agrosuppression: a bioassay for the hypersensitive response suited to high-throughput screening. Molecular Plant - Microbe Interactions. 16(1):7-13.

Qutob D, Huitema E, Gijzen M, Kamoun S. 2003. Variation in structure and activity among elicitins from Phytophthora sojae. Molecular Plant Pathology. 4(2):119-124. https://doi.org/10.1046/j.1364-3703.2003.00158.x

Torto TA, Li S, Styer A, Huitema E, Testa A, Gow NAR, van West P, Kamoun S. 2003. EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Research. 13(7):1675-1685. https://doi.org/10.1101/gr.910003

Kamoun S, Dong S, Hamada W, Huitema E, Kinney D, Morgan WR, Styer A, Testa A, Torto TA. 2002. From sequence to phenotype: functional genomics of Phytophthora. Canadian Journal of Plant Pathology. 24(1):6-9. https://doi.org/10.1080/07060660109506963

Kamoun S, Dong SJ, Huitema E, Torto GA, van West P, Vleeshouwers VGAA, Govers F. 2000. Dissection of nonhost resistance of Nicotiana to Phytophthora infestans. de Wit PJGM, Bisseling T, Stiekema WJ, editors. In Biology of plant-microbe interactions. St. Paul: International Society for Molecular Plant-Microbe Interactions. pp. 180-185.