The 124202 candidate effector of Melampsora larici-populina interacts with membranes in Nicotiana and Arabidopsis

References

• Alfano JR. 2009. Roadmap for future research on plant pathogen effectors. Mol Plant Pathol. 10:805–813.
   PubMed Web of Science ®Google Scholar
• Badel JL, Piquerez SJ, Greenshields D, Rallapalli G, Fabro G, Ishaque N, Jones JD. 2013. In planta effector competition assays detect Hyaloperonospora arabidopsidis effectors that contribute to virulence and localize to different plant subcellular compartments. Mol Plant-Microbe Interact. 26:745–757.
   PubMed Web of Science ®Google Scholar
• Bell E, Mullet JE. 1993. Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol. 103:1133–1137.
   PubMed Web of Science ®Google Scholar
• Bendahmane A, Farnham G, Moffett P, Baulcombe DC. 2002. Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J. 32:195–204.
   PubMed Web of Science ®Google Scholar
• Bohm H, Albert I, Fan L, Reinhard A, Nurnberger T. 2014. Immune receptor complexes at the plant cell surface. Curr Opin Plant Biol. 20:47–54.
   Google Scholar
• Brown CJ, Johnson AK, Dunker AK, Daughdrill GW. 2011. Evolution and disorder. Curr Opin Struct Biol. 21:441–446.
   PubMed Web of Science ®Google Scholar
• Caillaud MC, Piquerez SJ, Fabro G, Steinbrenner J, Ishaque N, Beynon J, Jones JD. 2012. Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant J. 69:252–265.
   PubMed Web of Science ®Google Scholar
• Catanzariti A-M, Dodds PN, Ellis JG. 2007. Avirulence proteins from haustoria-forming pathogens. FEMS Microbiol Lett. 269:181–188.
   PubMed Web of Science ®Google Scholar
• Catanzariti A-M, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG. 2006. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell. 18:243–256.
   PubMed Web of Science ®Google Scholar
• Catanzariti A-M, Dodds PN, Ve T, Kobe B, Ellis JG, Staskawicz BJ. 2010. The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Mol Plant-Microbe Interact. 23:49–57.
   PubMed Web of Science ®Google Scholar
• Cheng J, Sweredoski M, Baldi P. 2005. Accurate prediction of protein disordered regions by mining protein structure data. Data Mining Knowledge Discovery. 11:213–222.
   Web of Science ®Google Scholar
• Chevenet F, Brun C, Banuls AL, Jacq B, Christen R. 2006. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinform. 7:439.
   PubMed Web of Science ®Google Scholar
• Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal. 16:735–743.
   PubMed Web of Science ®Google Scholar
• Craxton M. 2004. Synaptotagmin gene content of the sequenced genomes. BMC Gen. 5:43.
   Web of Science ®Google Scholar
• Craxton M. 2007. Evolutionary genomics of plant genes encoding N-terminal-TM-C2 domain proteins and the similar FAM62 genes and synaptotagmin genes of metazoans. BMC Gen. 8:259.
   Web of Science ®Google Scholar
• De Silva K, Laska B, Brown C, Sederoff HW, Khodakovskaya M. 2011. Arabidopsis thaliana calcium-dependent lipid-binding protein (AtCLB): a novel repressor of abiotic stress response. J Exp Bot. 62:2679–2689.
   PubMed Web of Science ®Google Scholar
• Deng X, Eickholt J, Cheng J. 2009. PreDisorder: Ab initio sequence-based prediction of protein disordered regions. BMC Bioinform. 10:436.
   PubMed Web of Science ®Google Scholar
• Dereeper A, Audic S, Claverie J-M, Blanc G. 2010. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol. 10:8.
   PubMed Web of Science ®Google Scholar
• Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Gascuel O. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465–469.
   PubMed Web of Science ®Google Scholar
• Dunker AK, Oldfield CJ, Meng J, Romero P, Yang JY, Chen JW, Uversky VN. 2008. The unfoldomics decade: an update on intrinsically disordered proteins. BMC Gen. 9:S1.
   Google Scholar
• Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Martin F. 2011. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A. 108:9166–9171.
   PubMed Web of Science ®Google Scholar
• Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797.
   PubMed Web of Science ®Google Scholar
• Fernandez-Chacon R, Konigstorfer A, Gerber SH, Garcia J, Matos MF, Stevens CF, Sudhof TC. 2001. Synaptotagmin I functions as a calcium regulator of release probability. Nature. 410:41–49.
   PubMed Web of Science ®Google Scholar
• Fong JH, Shoemaker BA, Garbuzynskiy SO, Lobanov MY, Galzitskaya OV, Panchenko AR. 2009. Intrinsic disorder in protein interactions: insights from a comprehensive structural analysis. PLoS Comput Biol. 5:1–11.
   Web of Science ®Google Scholar
• Gao J, Xu D. 2012. Correlation between posttranslational modification and intrinsic disorder in protein Pac Symp Biocomputing. World Scientific; New Jersey, USA, p. 94–103.
   Google Scholar
• Geppert M, Goda Y, Hammer RE, Li C, Rosahl TW, Stevens CF, Südhof TC. 1994. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell. 79:717–727.
   PubMed Web of Science ®Google Scholar
• Giraldo MC, Valent B. 2013. Filamentous plant pathogen effectors in action. Nat Rev Microbiol. 11:800–814.
   PubMed Web of Science ®Google Scholar
• Hacquard S, Joly DL, Lin YC, Tisserant E, Feau N, Delaruelle C, Duplessis S. 2012. A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust). Mol Plant Microbe Interact. 25:279–293.
   PubMed Web of Science ®Google Scholar
• Hacquard S, Petre B, Frey P, Hecker A, Rouhier N, Duplessis S. 2011. The poplar-poplar rust interaction: insights from genomics and transcriptomics. J Pathog. 2011:716041.
   PubMedGoogle Scholar
• Hecker J, Yang JY, Cheng J. 2008. Protein disorder prediction at multiple levels of sensitivity and specificity. BMC Gen. 9:S9.
   Google Scholar
• Helfer S. 2014. Rust fungi and global change. New Phytol. 201:770–780.
   PubMed Web of Science ®Google Scholar
• Hicks SW, Galan JE. 2013. Exploitation of eukaryotic subcellular targeting mechanisms by bacterial effectors. Nat Rev Microbiol. 11:316–326.
   PubMed Web of Science ®Google Scholar
• Huelsenbeck JP, Ronquist F. 2001. MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics. 17:754–755.
   PubMed Web of Science ®Google Scholar
• Ispolatov I, Yuryev A, Mazo I, Maslov S. 2005. Binding properties and evolution of homodimers in protein-protein interaction networks. Nucleic Acids Res. 33:3629–3635.
   PubMed Web of Science ®Google Scholar
• Joly DL, Feau N, Tanguay P, Hamelin RC. 2010. Comparative analysis of secreted protein evolution using expressed sequence tags from four poplar leaf rusts (Melampsora ssp). BMC Gen. 11:422.
   Web of Science ®Google Scholar
• Karimi M, Inze D, Depicker A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7:193–195.
   PubMed Web of Science ®Google Scholar
• Kim YC, Kim SY, Choi D, Ryu CM, Park JM. 2008. Molecular characterization of a pepper C2 domain-containing SRC2 protein implicated in resistance against host and non-host pathogens and abiotic stresses. Planta. 227:1169–1179.
   PubMed Web of Science ®Google Scholar
• Koeck M, Hardham AR, Dodds PN. 2011. The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell Microbiol. 13:1849–1857.
   PubMed Web of Science ®Google Scholar
• Kurotani A, Tokmakov AA, Kuroda Y, Fukami Y, Shinozaki K, Sakurai T. 2014. Correlations between predicted protein disorder and post-translational modifications in plants. Bioinformatics. 30:1095–1103.
   Web of Science ®Google Scholar
• Lewis JD, Lazarowitz SG. 2010. Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci U S A. 107:2491–2496.
   PubMed Web of Science ®Google Scholar
• Light S, Sagit R, Sachenkova O, Ekman D, Elofsson A. 2013. Protein expansion is primarily due to indels in intrinsically disordered regions. Mol Biol Evol. 30:2645–2653.
   PubMed Web of Science ®Google Scholar
• Liu Z, Guo F, Zhang J, Wang J, Lu L, Li D, He F. 2013. Proteome-wide prediction of self-interacting proteins based on multiple properties. Mol Cell Proteomics. 12:1689–1700.
   PubMed Web of Science ®Google Scholar
• Marianayagam NJ, Sunde M, Matthews JM. 2004. The power of two: protein dimerization in biology. Trends Biochem Sci. 29:618–625.
   PubMed Web of Science ®Google Scholar
• Marin M, Uversky VN, Ott T. 2013. Intrinsic disorder in pathogen effectors: protein flexibility as an evolutionary hallmark in a molecular arms race. Plant Cell. 25:3153–3157.
   PubMed Web of Science ®Google Scholar
• Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP. 2007. The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant-Microbe Interact. 20:816–831.
   PubMed Web of Science ®Google Scholar
• Mireault C, Paris L-E, Germain H. 2014. Enhancement of the Arabidopsis floral dip method with XIAMETER OFX-0309 as alternative to Silwet L-77 surfactant. Botany. 92:523–525.
   Web of Science ®Google Scholar
• Mukhtar MS, Carvunis A-R, Dreze M, Epple P, Steinbrenner J, Moore J, Dangl JL. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science (New York, N.Y.). 333:596–601.
   PubMed Web of Science ®Google Scholar
• Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol. 302:205–217.
   PubMed Web of Science ®Google Scholar
• Petre B, Kamoun S. 2014. How do filamentous pathogens deliver effector proteins into plant cells? PLoS Biol. 12:e1001801.
   PubMed Web of Science ®Google Scholar
• Petre B, Saunders DG, Sklenar J, Lorrain C, Win J, Duplessis S, Kamoun S. 2015. Candidate effector proteins of the rust pathogen Melampsora larici-populina target diverse plant cell compartments. Mol Plant-Microbe Interact. 28:689–700.
   PubMed Web of Science ®Google Scholar
• Rafiqi M, Gan PH, Ravensdale M, Lawrence GJ, Ellis JG, Jones DA, Dodds PN. 2010. Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell. 22:2017–2032.
   PubMed Web of Science ®Google Scholar
• Sakamoto M, Tomita R, Kobayashi K. 2009. A protein containing an XYPPX repeat and a C2 domain is associated with virally induced hypersensitive cell death in plants. FEBS Lett. 583:2552–2556.
   PubMed Web of Science ®Google Scholar
• Sannigrahi P, Ragauskas AJ, Tuskan GA. 2010. Poplar as a feedstock for biofuels: a review of compositional characteristics. Biofuels, Bioproducts, Biorefining. 4:209–226.
   Web of Science ®Google Scholar
• Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Botella MA. 2008. Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell. 20:3374–3388.
   PubMed Web of Science ®Google Scholar
• Scheglmann D, Werner K, Eiselt G, Klinger R. 2002. Role of paired basic residues of protein C-termini in phospholipid binding. Protein Eng. 15:521–528.
   PubMedGoogle Scholar
• Schippers JH, Nunes-Nesi A, Apetrei R, Hille J, Fernie AR, Dijkwel PP. 2008. Arabidopsis onset of leaf death5 mutation of quinolinate synthase affects nicotinamide adenine dinucleotide biosynthesis and causes early ageing. Plant Cell. 20:2909–2925.
   PubMed Web of Science ®Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH image to imageJ: 25 years of image analysis. Nat Methods. 9:671–675.
   PubMed Web of Science ®Google Scholar
• Schornack S, Van Damme M, Bozkurt TO, Cano LM, Smoker M, Thines M, Huitema E. 2010. Ancient class of translocated oomycete effectors targets the host nucleus. Proc Natl Acad Sci U S A. 107:17421–17426.
   PubMed Web of Science ®Google Scholar
• Sparkes IA, Runions J, Kearns A, Hawes C. 2006. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc. 1:2019–2025.
   PubMed Web of Science ®Google Scholar
• Stahelin RV. 2009. Lipid binding domains: more than simple lipid effectors. J Lipid Res. 50:S299–304.
   Google Scholar
• Taylor G. 2002. Populus: Arabidopsis for forestry. Do we need a model tree? Ann Bot. 90:681–689.
   PubMed Web of Science ®Google Scholar
• Thieme F, Szczesny R, Urban A, Kirchner O, Hause G, Bonas U. 2007. New type III effectors from Xanthomonas campestris pv. vesicatoria trigger plant reactions dependent on a conserved N-myristoylation motif. Mol Plant Microbe Interact. 20:1250–1261.
   PubMed Web of Science ®Google Scholar
• Ve T, Williams SJ, Catanzariti AM, Rafiqi M, Rahman M, Ellis JG, Kobe B. 2013. Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity. Proc Natl Acad Sci U S A. 110:17594–17599.
   PubMed Web of Science ®Google Scholar
• Voinnet O, Pinto YM, Baulcombe DC. 1999. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci U S A. 96:14147–14152.
   PubMed Web of Science ®Google Scholar
• Voinnet O, Rivas S, Mestre P, Baulcombe D. 2003. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33:949–956.
   PubMed Web of Science ®Google Scholar
• Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 18:691–699.
   PubMed Web of Science ®Google Scholar
• Wilkerson CG, Mansfield SD, Lu F, Withers S, Park JY, Karlen SD, Ralph J. 2014. Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science. 344:90–93.
   PubMed Web of Science ®Google Scholar
• Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K, Dong S, Kamoun S. 2012. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb Symp Quant Biol. 77:235–247.
   PubMedGoogle Scholar
• Yamazaki T, Takata N, Uemura M, Kawamura Y. 2010. Arabidopsis synaptotagmin SYT1, a type I signal-anchor protein, requires tandem C2 domains for delivery to the plasma membrane. J Biol Chem. 285:23165–23176.
   PubMed Web of Science ®Google Scholar
• Yang H, Li Y, Hua J. 2006. The C2 domain protein BAP1 negatively regulates defense responses in Arabidopsis. Plant J. 48:238–248.
   PubMed Web of Science ®Google Scholar
• Yang H, Yang S, Li Y, Hua J. 2007. The Arabidopsis BAP1 and BAP2 genes are general inhibitors of programmed cell death. Plant Physiol. 145:135–146.
   PubMed Web of Science ®Google Scholar
• Zhang G, Sun YF, Li YM, Dong YL, Huang XL, Yu YT, Kang ZS. 2013. Characterization of a wheat C2 domain protein encoding gene regulated by stripe rust and abiotic stresses. Biologia Plant. 57:701–710.
   Web of Science ®Google Scholar