Identification of Plasmodiophora brassicae effectors — A challenging goal

References

• Hwang SF, Strelkov SE, Feng J, et al. Plasmodiophora brassicae: a review of an emerging pathogen of the Canadian canola (Brassica napus) crop. Mol Plant Pathol. 2012;13:105–113.
   PubMed Web of Science ®Google Scholar
• Strelkov SE, Hwang SF. Clubroot in the Canadian canola crop: 10 years into the outbreak. Can J Plant Pathol. 2014;36(S1):27–36.
   Web of Science ®Google Scholar
• Bhering AS, Do Carmo MGF, Matos TM, et al. Soil factors related to the severity of clubroot in Rio de Janeiro. Brazil Plant Disease. 2017;101:1345–1353.
   PubMed Web of Science ®Google Scholar
• Aist JR, Williams PH. The cytology and kinetics of cabbage root hair penetration by Plasmodiophora brassicae. Can J Bot. 1971;49:2023–2034.
   Google Scholar
• Burki F, Kudryavtsev A, Matz MV, et al. Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists. BMC Evol Biol. 2010;10:377.
   PubMed Web of Science ®Google Scholar
• Burki F, Keeling PJ. Rhizaria. Curr Biol. 2014;24(3):R103–7.
   PubMed Web of Science ®Google Scholar
• Kageyama K, Asano T. Life cycle of Plasmodiophora brassicae. J Plant Growth Regul. 2009;28(3):203–211.
   Web of Science ®Google Scholar
• Peng G, Lahlali R, Hwang SF, et al. Crop rotation, cultivar resistance, and fungicides/biofungicides for managing clubroot (Plasmodiophora brassicae) on canola. Can J Plant Pathol. 2014;36(S1):99–112.
   Web of Science ®Google Scholar
• Rahman H, Bennett RA, Seguin-Swartz G. Broadening genetic diversity in Brassica napus canola: development of canola-quality spring B. napus from B. napus × B. oleracea var. alboglabra interspecific crosses. Can J Plant Sci. 2014;95(1):29–41.
   Web of Science ®Google Scholar
• Fredua-Agyeman R, Hwang S-F, Strelkov SE, et al. Assessment of resistance to ‘new’ virulent populations of Plasmodiophora brassicae reveals potential loss of clubroot resistance genes from donor parent Brassica rapa L. ssp. rapifera (ECD 04) during doubled haploid production. Mol Plant Pathol. 2017. DOI:10.1111/ppa.12816
   Web of Science ®Google Scholar
• Rahman H, Shakir A, Hassan MJ. Breeding for clubroot resistant spring canola (Brassica napus L.) for the Canadian prairies: can the European winter canola cv. ‘Mendel’ be used as a source of resistance? Can J Plant Sci. 2011;91:447–458.
   Web of Science ®Google Scholar
• Matsumoto E, Ueno H, Aruga D, et al. Accumulation of three clubroot resistance genes through marker-assisted selection in Chinese Cabbage (Brassica rapa ssp. pekinensis). J Jpn Soc Hortic Sci. 2012;81:184–190.
   Web of Science ®Google Scholar
• Diederichsen E, Frauen M, Ludwig-Müller J. Clubroot disease management challenges from a German perspective. Can J Plant Pathol. 2014;36:85–98.
   Web of Science ®Google Scholar
• Ueno H, Matsumoto E, Aruga D, et al. Molecular characterization of the CRa gene conferring clubroot resistance in Brassica rapa. Plant Mol Biol. 2012;80:621–629.
   PubMed Web of Science ®Google Scholar
• Hatakeyama H, Suwabe K, Tomita RN, et al. Identification and characterization of Crr1a, a gene for resistance to clubroot disease (Plasmodiophora brassicae Woronin) In Brassica rapa L. PLoS ONE. 2013;8:e54745.
   PubMed Web of Science ®Google Scholar
• Figdore SS, Ferreira ME, Slocum MK, et al. Association of RFLP markers with trait loci affecting clubroot resistance and morphological characters in Brassica oleracea L. Euphytica. 1993;69:33–44.
   Web of Science ®Google Scholar
• Rocherieux J, Glory P, Giboulot A, et al. Isolate-specific and broad-spectrum QTLs are involved in the control of clubroot in Brassica oleracea. Theor Appl Genet. 2004;108:1555–1563.
   PubMed Web of Science ®Google Scholar
• Nagaoka T, Doullah MA, Matsumoto S, et al. Identification of QTLs that control clubroot resistance in Brassica oleracea and comparative analysis of clubroot resistance genes between B. rapa and B. oleracea. Theor Appl Genet. 2010;120:1335–1346.
   PubMed Web of Science ®Google Scholar
• Lee J, Izzah NK, Choi BS, et al. Genotyping-by-sequencing map permits identification of clubroot resistance QTLs and revision of the reference genome assembly in cabbage (Brassica oleracea L.). DNA Res. 2015;23:29–41.
   PubMed Web of Science ®Google Scholar
• Schwelm A, Fogelqvist J, Knaust A, et al. The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. Sci Rep. 2015;5:11153.
   PubMed Web of Science ®Google Scholar
• Rolfe SA, Strelkov SE, Links MG, et al. The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp. BMC Genomics. 2016;17:272.
   PubMed Web of Science ®Google Scholar
• Vleeshouwers VGAA, Oliver RP. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Molecular Plant-Microbe Interactions. 2014;27(3):196–206.
   PubMed Web of Science ®Google Scholar
• Cano LM, Raffaele S, Haugen RH, et al. Major transcriptome reprogramming underlies floral mimicry induced by the rust fungus Puccinia monoica in Boechera stricta. PLoS One. 2013;8:e75293.
   PubMed Web of Science ®Google Scholar
• Sugio A, Kingdom HN, MacLean AM, et al. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. PNAS. 2011;108(48):E1254–E1263.
   PubMed Web of Science ®Google Scholar
• Nemri A, Saunders DGO, Anderson C, et al. The genome sequence and effector complement of the flax rust pathogen Melampsora lini. Front Plant Sci. 2014;5. DOI:10.3389/fpls.2014.00098.
   Web of Science ®Google Scholar
• Dodds PN, Lawrence GJ, Catanzariti A-M, et al. The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are Recognized inside plant cells. Plant Cell. 2004;16:755–768.
   PubMed Web of Science ®Google Scholar
• Van Esse HP, Bolton MD, Stergiopoulos I, et al. The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Molecular Plant-Microbe Interactions. 2007;20(9):1092–1101.
   PubMed Web of Science ®Google Scholar
• Salcedo A, Rutter W, Wang S, et al. Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99. Science. 2017;358:1604–1606.
   PubMed Web of Science ®Google Scholar
• Chen J, Upadhyaya NM, Ortiz D, et al. Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat. Science. 2017;358:1607–1610.
   PubMed Web of Science ®Google Scholar
• Mago R, Zhang P, Vautrin S, et al. The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus. Nat Plants. 2015;1:15186.
   PubMed Web of Science ®Google Scholar
• Dodds PN, Rathjen JP. Plant immunity: towards an integrated view of plant– pathogen interactions. Nat Rev Genet. 2010;11(8):539–548.
   PubMed Web of Science ®Google Scholar
• Jones JDG, Dangl JL. The plant immune system. Nature. 2006;444:323–329.
   PubMed Web of Science ®Google Scholar
• Siemens J, González MC, Wolf S, et al. Extracellular invertase is involved in the regulation of clubroot disease in Arabidopsis thaliana. Mol Plant Pathol. 2011;12:247–262.
   PubMed Web of Science ®Google Scholar
• Duplessis S, Cuomo CA, Lin Y-C, et al. Obligate biotrophy features unravelled by the genomic analysis of rust fungi. Proc Natl Acad Sci USA. 2011;108:9166–9171.
   PubMed Web of Science ®Google Scholar
• Hacquard S, Joly DL, Lin Y-C, et al. A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust). Molecular Plant Microbe Interactions. 2012;25:279–293.
   PubMed Web of Science ®Google Scholar
• Ludwig-Müller J, Jülken S, Geib K, et al. A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid. Mol Plant Pathol. 2015;16(4):349–364.
   PubMed Web of Science ®Google Scholar
• Dempsey DA, Vlot AC, Wildermuth MC, et al. Salicylic acid biosynthesis and metabolism. In: Torii K, editor. The Arabidopsis Book. Vol. 9. Rockville, MD: The American Society of Plant Biologists; 2011. p. e0156.
   Google Scholar
• Seskar M, Shulaev V, Raskin I. Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol. 1998;116:387–392.
   Web of Science ®Google Scholar
• Djamei A, Schipper K, Rabe F, et al. Metabolic priming by a secreted fungal effector. Nature. 2011;478:395–398.
   PubMed Web of Science ®Google Scholar
• Lo Presti L, Lanver D, Schweizer G, et al. Fungal effectors and plant susceptibility. Annu Rev Plant Biol. 2015;66:513–545.
   PubMed Web of Science ®Google Scholar
• Stergiopoulos I, De Wit PJGM. Fungal effector proteins. Annu Rev Phytopathol. 2009;47:233–263.
   PubMed Web of Science ®Google Scholar
• De Carvalho M, Nascimento LC, Darben LM, et al. Prediction of the in planta Phakopsora pachyrhizi secretome and potential effector families. Mol Plant Pathol. 2017;18(3):363–377.
   PubMed Web of Science ®Google Scholar
• Rafiqi M, Gan PHP, Ravensdale M, et al. Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell. 2010;22:2017–2032.
   PubMed Web of Science ®Google Scholar
• Yaeno T, Li H, Chaparro-Garcia A, et al. Phosphatidyl inositol monophosphate-binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. Proc Natl Acad Sci USA. 2011;108:14682–14687.
   PubMed Web of Science ®Google Scholar
• Kale SD, Gu B, Capelluto DG, et al. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell. 2010;142:284–295.
   PubMed Web of Science ®Google Scholar
• Xiang J, Li X, Yin L, et al. A candidate RxLR effector from Plasmopara viticola can elicit immune responses in Nicotiana benthamiana. BMC Plant Biology. 2017;17:75.
   PubMed Web of Science ®Google Scholar
• Wirthmueller L, Maqbool A, Banfield MJ. On the front line: structural insights into plant-pathogen interactions. Nat Rev Microbiol. 2013;11:761–776.
   PubMed Web of Science ®Google Scholar
• Van Den Burg HA, Spronk CAEM, Boeren S, et al. Binding of the AVR4 elicitor of Cladosporium fulvum to chitotriose units is facilitated by positive allosteric protein- protein interactions: the chitin-binding site of Avr4 represents a novel binding site on the folding scaffold shared between the invertebrate and the plant chitin-binding domain. J Biol Chem. 2004;279:16786–16796.
   PubMed Web of Science ®Google Scholar
• Van Den Burg HA, Harrison SJ, Joosten MHAJ, et al. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Molecular Plant-Microbe Interaction. 2006;19:1420–1430.
   PubMed Web of Science ®Google Scholar
• Bolton MD, Van Esse HP, Vossen JH, et al. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol. 2008;69:119–136.
   PubMed Web of Science ®Google Scholar
• Spanu PD, Abbott JC, Amselem J, et al. Genome expansion and gene loss in powdery mildew fungi reveal trade offs in extreme parasitism. Science. 2010;330:1543–1546.
   PubMed Web of Science ®Google Scholar
• Rooney HCE, Van’t Klooster JW, Van Der Hoorn RAL, et al. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science. 2005;308:1783–1786.
   PubMed Web of Science ®Google Scholar
• Pallaghy PK, Nielsen KJ, Craik DJ, et al. A common structural motif incorporating a cysteine knot and a triple-stranded Î2-sheet in toxic and inhibitory polypeptides. Protein Sci. 1994;3:1833–1839.
   PubMed Web of Science ®Google Scholar
• Van Den Hooven HW, Van Den Burg HA, Vossen P, et al. Disulfide bond structure of the AVR9 elicitor of the fungal tomato pathogen Cladosporium fulvum: evidence for a cystine knot. Biochemistry. 2001;40:3458–3466.
   PubMed Web of Science ®Google Scholar
• Bulman S, Siemens J, Ridgway HJ, et al. Identification of genes from the obligate intracellular plant pathogen, Plasmodiophora brassicae. FEMS Microbiol Lett. 2006;264:198–204.
   PubMed Web of Science ®Google Scholar
• Feng J, Hwang RU, Hwang S-F, et al. Molecular characterization of a serine protease Pro1 from Plasmodiophora brassicae that stimulates resting spore germination. Plant Pathology. 2010;11(4):503–512.
   Web of Science ®Google Scholar
• Moxham SE, Buczacki ST. Structure of the resting spore wall of Plasmodiophora brassicae revealed by electron microscopy and chemical digestion. Trans Br Mycological Soc. 1983;81:221–231.
   Web of Science ®Google Scholar
• Gurlebeck D, Thieme F, Bonas U. Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. J Plant Physiol. 2006;163:233–255.
   PubMed Web of Science ®Google Scholar
• Poueymiro M, Genin S. Secreted proteins from Ralstonia solanacearum: a hundred tricks to kill a plant. Curr Opin Microbiol. 2009;12:44–52.
   PubMed Web of Science ®Google Scholar
• Bai X, Correa VR, Toruño TY, et al. AY-WB phytoplasma secretes a protein that targets plant cell nuclei. Molecular Plant Microbe Interaction. 2009;22:18–30.
   PubMed Web of Science ®Google Scholar
• Caillaud M-C, Piquerez SJM, Fabro G, et al. Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant J. 2012;69:252–265.
   PubMed Web of Science ®Google Scholar
• Vargas WA, Sanz-Martín JM, Rech GE, et al. A fungal effector with host nuclear localization and DNA-binding properties is required for maize anthracnose development. Molecular Plant Microbe Interaction. 2016;29:83–95.
   PubMed Web of Science ®Google Scholar
• Quentin M, Abad P, Favery B. Plant parasitic nematode effectors target host defense and nuclear functions to establish feeding cells. Front Plant Sci. 2013;4:53.
   PubMed Web of Science ®Google Scholar
• Espinosa A, Alfano JR. Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity. Cell Microbiol. 2004;6:1027–1040.
   PubMed Web of Science ®Google Scholar
• Marti M, Good RT, Rug M, et al. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science. 2004;306:1930–1933.
   PubMed Web of Science ®Google Scholar
• Noon JB, Qi M, Sill1 DN, et al. A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity. New Phytologist. 2016;212:444–460.
   PubMed Web of Science ®Google Scholar
• Schwelm A, Badstöber J, Bulman S, et al. Not in your usual Top 10: protists that infect plants and algae. Mol Plant Pathol. 2017. DOI:10.1111/mpp.12580
   PubMed Web of Science ®Google Scholar
• Legreve A, Vanpee B, Delfosse P, et al. Host range of tropical and sub-tropical isolates of Polymyxa graminis. Eur J Plant Pathol. 2000;106:379–389.
   Web of Science ®Google Scholar
• Legreve A, Delfosse P, Maraite H. Phylogenetic analysis of Polymyxa species based on nuclear 5.8S and internal transcribed spacers ribosomal DNA sequences. Mycology Res. 2002;106:138–147.
   Web of Science ®Google Scholar
• Bulman S, Candy JM, Fiers M, et al. Genomics of biotrophic, plant-infecting plasmodiophorids using in vitro dual cultures. Protist. 2011;162:449–461.
   PubMed Web of Science ®Google Scholar
• Gutiérrez PA, Alzate JF, Montoya MM. Analysis of carbohydrate metabolism genes of Spongospora subterranea using 454 pyrosequencing. Revista Facultad Nacional De Agronomía Medellín. 2014;67:7247–7260.
   Google Scholar
• Gutiérrez P, Bulman S, Alzate JF, et al. Mitochondrial genome sequence of the potato powdery scab pathogen Spongospora subterranea. Mitochondrial DNA. Part A, DNA Mapping, Sequencing, and Analysis. 2016;27:58–59.
   PubMedGoogle Scholar
• Bulman S, Braselton JP. Rhizaria: phytomyxea. In: (Mclaughlin DJ, Spatafora JW, editors. The Mycota VII, Part A, Systematics and Evolution. Berlin (Germany): Springer-Verlag; 2014. p. 99–112.
   Google Scholar
• Malinowski R, Smith JA, Fleming AJ, et al. Gall formation in clubroot-infected Arabidopsis results from an increase in existing meristematic activities of the host but is not essential for the completion of the pathogen life cycle. Plant J. 2012;71:226–238.
   PubMed Web of Science ®Google Scholar
• Zuccaro A, Lahrmann U, GüLdener U, et al. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog. 2011;7:e1002290.
   PubMed Web of Science ®Google Scholar
• Ye W, Wang Y, Wang Y. Bioinformatics analysis reveals abundant short alpha-helices as a common structural feature of oomycete RxLR effector proteins. PLoSONE. 2015;10:e0135240.
   PubMed Web of Science ®Google Scholar
• Irani S, Trost B, Waldner M, et al. Transcriptome analysis of response to Plasmodiophora brassicae infection in the Arabidopsis shoot and root. BMC Genomics. 2018;19:23.
   PubMed Web of Science ®Google Scholar
• Seifbarghi S, Borhan MH, Wei Y, et al. Changes in the Sclerotinia sclerotiorum transcriptome during infection of Brassica napus. BMC Genomics. 2017;18:266.
   PubMed Web of Science ®Google Scholar
• Bulman S, Richter F, Marschollek S, et al. Arabidopsis thaliana expressing PbBSMT, a gene encoding a SABATH-type methyltransferase from the plant pathogenic protist Plasmodiophora brassicae, show leaf chlorosis and altered host susceptibility. Plant Biol. 2018. DOI:10.1111/plb.12728
   PubMed Web of Science ®Google Scholar
• Bolger AM, Lohse M, Usadel B. Trimmomatic:A flexible trimmer for Illumina Sequence Data. Bioinformatics. 2014;30(15):2114–2120..
   Web of Science ®Google Scholar
• Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21.
   PubMed Web of Science ®Google Scholar
• Petersen TN, Brunak S, Von Heijne G, et al. SignalP4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785–786.
   PubMed Web of Science ®Google Scholar
• Horton P, Park K-J, Obayashi T, et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007;35:W585–W587.
   PubMed Web of Science ®Google Scholar
• Emanuelsson O, Nielsen H, Brunak S, et al. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol. 2000;300:1005–1016.
   PubMed Web of Science ®Google Scholar