BACKGROUND: Downy mildews are the most speciose group of oomycetes and affect crops of great economic importance. So far, there is only a single deeply-sequenced downy mildew genome available, from Hyaloperonospora arabidopsidis. Further genomic resources for downy mildews are required to study their evolution, including pathogenicity effector proteins, such as RxLR effectors. Plasmopara halstedii is a devastating pathogen of sunflower and a potential pathosystem model to study downy mildews, as several Avr-genes and R-genes have been predicted and unlike Arabidopsis downy mildew, large quantities of almost contamination-free material can be obtained easily. RESULTS: Here a high-quality draft genome of Plasmopara halstedii is reported and analysed with respect to various aspects, including genome organisation, secondary metabolism, effector proteins and comparative genomics with other sequenced oomycetes. Interestingly, the present analyses revealed further variation of the RxLR motif, suggesting an important role of the conservation of the dEER-motif. Orthology analyses revealed the conservation of 28 RxLR-like core effectors among Phytophthora species. Only six putative RxLR-like effectors were shared by the two sequenced downy mildews, highlighting the fast and largely independent evolution of two of the three major downy mildew lineages. This is seemingly supported by phylogenomic results, in which downy mildews did not appear to be monophyletic. CONCLUSIONS: The genome resource will be useful for developing markers for monitoring the pathogen population and might provide the basis for new approaches to fight Phytophthora and downy mildew pathogens by targeting core pathogenicity effectors.

Biodiversity and Climate Research Centre Germany

Biosciences University of Exeter Stocker Road Exeter EX4 4QD UK

Center for Integrative Fungal Research Germany

Department of Botany Faculty of Science Palacký University Olomouc Šlechtitelů 11 78371 Olomouc Czech Republic

Department of Plant Pathology and Microbiology University of California Riverside CA 92521 USA

Institute of Ecology Evolution and Diversity Goethe University Max von Laue Str 9 60323 Frankfurt Germany

Integrative Fungal Research Senckenberganlage 25 D 60325 Frankfurt am Main Germany

Laboratory of Phytopathology Wageningen University Droevendaalsesteeg 1 NL 6708PB Wageningen The Netherlands

Max Planck Institute for Plant Breeding Research Carl von Linne´ Weg 10 Cologne 50829 Germany

Merck Stiftungsprofessur für Molekulare Biotechnologie Fachbereich Biowissenschaften and Buchmann Institute for Molecular Life Sciences Goethe Universität Frankfurt Max von Laue Str 9 60438 Frankfurt am Main Germany

Plant Microbe Interactions Department of Biology Utrecht University Padualaan 8 NL 3584 CH Utrecht The Netherlands

Present address Department of Plant Pathology North Carolina State University Raleigh Raleigh NC 27695 USA

Sainsbury Laboratory University of Cambridge Cambridge CB2 1LR UK

Senckenberg Gesellschaft für Naturforschung Senckenberganlage 25 60325 Frankfurt Germany

The Sainsbury Laboratory Norwich Research Park Norwich NR4 7UH UK

University of Hohenheim Institute of Botany 210 D 70593 Stuttgart Germany

Zobrazit více v PubMed

Thines M. Phylogeny and evolution of plant pathogenic oomycetes—a global overview. Eur J Plant Pathol. 2014;138(3):431–447. doi: 10.1007/s10658-013-0366-5. DOI

Kemen AC, Agler MT, Kemen E. Host–microbe and microbe–microbe interactions in the evolution of obligate plant parasitism. New Phytologist. 2015;206(4):1207–28. doi: 10.1111/nph.13284. PubMed DOI

Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL, Robert-Seilaniantz A, Bailey K, Holub E, Studholme DJ, Maclean D, et al. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol. 2011;9(7):e1001094. doi: 10.1371/journal.pbio.1001094. PubMed DOI PMC

Gascuel Q, Martinez Y, Boniface MC, Vear F, Pichon M, Godiard L. The sunflower downy mildew pathogen Plasmopara halstedii. Mol Plant Pathol. 2015;16(2):109–122. doi: 10.1111/mpp.12164. PubMed DOI PMC

Sackston WE. Downy mildew of sunflower. London: Academic; 1981.

Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, Kemen E, Thines M, Ah-Fong A, Anderson R, Badejoko W, et al. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science. 2010;330(6010):1549–1551. doi: 10.1126/science.1195203. PubMed DOI PMC

Links MG, Holub E, Jiang RH, Sharpe AG, Hegedus D, Beynon E, Sillito D, Clarke WE, Uzuhashi S, Borhan MH. De novo sequence assembly of Albugo candida reveals a small genome relative to other biotrophic oomycetes. BMC Genomics. 2011;12:503. doi: 10.1186/1471-2164-12-503. PubMed DOI PMC

van West P, and Vleeshouwers, V.G.A.A. The Phytophthora infestans -host interaction, vol. Chapter 9. Hoboken, New Jersey: Blackwell Scientific Publishers; 2004.

Yoshida K, Burbano HA, Krause J, Thines M, Weigel D, Kamoun S. Mining herbaria for plant pathogen genomes: back to the future. PLoS Pathog. 2014;10(4):e1004028. doi: 10.1371/journal.ppat.1004028. PubMed DOI PMC

Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, Lanz C, Martin FN, Kamoun S, Krause J, et al. The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife. 2013;2:e00731. PubMed PMC

Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, et al. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science. 2006;313(5791):1261–1266. doi: 10.1126/science.1128796. PubMed DOI

Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature. 2009;461(7262):393–398. doi: 10.1038/nature08358. PubMed DOI

Quinn L, O’Neill PA, Harrison J, Paskiewicz KH, McCracken AR, Cooke LR, Grant MR, Studholme DJ. Genome-wide sequencing of Phytophthora lateralis reveals genetic variation among isolates from Lawson cypress (Chamaecyparis lawsoniana) in Northern Ireland. FEMS Microbiol Lett. 2013;344(2):179–185. doi: 10.1111/1574-6968.12179. PubMed DOI

Lamour KH, Mudge J, Gobena D, Hurtado-Gonzales OP, Schmutz J, Kuo A, Miller NA, Rice BJ, Raffaele S, Cano LM, et al. Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Mol Plant Microbe Interact. 2012;25(10):1350–1360. doi: 10.1094/MPMI-02-12-0028-R. PubMed DOI PMC

Levesque CA, Brouwer H, Cano L, Hamilton JP, Holt C, Huitema E, Raffaele S, Robideau GP, Thines M, Win J, et al. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol. 2010;11(7):R73. doi: 10.1186/gb-2010-11-7-r73. PubMed DOI PMC

Jiang RH, de Bruijn I, Haas BJ, Belmonte R, Lobach L, Christie J, van den Ackerveken G, Bottin A, Bulone V, Diaz-Moreno SM, et al. Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica. PLoS Genet. 2013;9(6):e1003272. doi: 10.1371/journal.pgen.1003272. PubMed DOI PMC

Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stuber K, et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science. 2010;330(6010):1543–1546. doi: 10.1126/science.1194573. PubMed DOI

Tian M, Win J, Savory E, Burkhardt A, Held M, Brandizzi F, Day B. 454 Genome sequencing of Pseudoperonospora cubensis reveals effector proteins with a QXLR translocation motif. Mol Plant Microbe Interact. 2011;24(5):543–553. doi: 10.1094/MPMI-08-10-0185. PubMed DOI

Cooke DE, Drenth A, Duncan JM, Wagels G, Brasier CM. A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Biol. 2000;30(1):17–32. doi: 10.1006/fgbi.2000.1202. PubMed DOI

Goker M, Voglmayr H, Riethmuller A, Oberwinkler F. How do obligate parasites evolve? A multi-gene phylogenetic analysis of downy mildews. Fungal Genet Biol. 2007;44(2):105–122. doi: 10.1016/j.fgb.2006.07.005. PubMed DOI

Thines M, Choi YJ, Kemen E, Ploch S, Holub EB, Shin HD, Jones JD. A new species of Albugo parasitic to Arabidopsis thaliana reveals new evolutionary patterns in white blister rusts (Albuginaceae) Persoonia. 2009;22:123–128. doi: 10.3767/003158509X457931. PubMed DOI PMC

Runge F, Telle S, Ploch S, Savory E, Day B, Sharma R, Thines M. The inclusion of downy mildews in a multi-locus-dataset and its reanalysis reveals a high degree of paraphyly in Phytophthora. IMA Fungus. 2011;2(2):163–171. doi: 10.5598/imafungus.2011.02.02.07. PubMed DOI PMC

Pais M, Win J, Yoshida K, Etherington GJ, Cano LM, Raffaele S, Banfield MJ, Jones A, Kamoun S, Go Saunders D. From pathogen genomes to host plant processes: the power of plant parasitic oomycetes. Genome Biol. 2013;14(6):211. doi: 10.1186/gb-2013-14-6-211. PubMed DOI PMC

Seidl MF, Van den Ackerveken G, Govers F, Snel B. Reconstruction of oomycete genome evolution identifies differences in evolutionary trajectories leading to present-day large gene families. Genome Biol Evol. 2012;4(3):199–211. doi: 10.1093/gbe/evs003. PubMed DOI PMC

Meijer HJG, Hassen HH, Govers F. Phytophthora infestans has a plethora of phospholipase D enzymes including a subclass that has extracellular activity. PLoS One. 2011;6(3):e17767. doi: 10.1371/journal.pone.0017767. PubMed DOI PMC

Meijer HJG, Govers F. Genomewide analysis of phospholipid signaling genes in Phytophthora spp.: novelties and a missing link. Mol Plant-Microbe Interact. 2006;19(12):1337–1347. doi: 10.1094/MPMI-19-1337. PubMed DOI

Hua C, Meijer HJG, de Keijzer J, Zhao W, Wang Y, Govers F. GK4, a G-protein-coupled receptor with a phosphatidylinositol phosphate kinase domain in Phytophthora infestans, is involved in sporangia development and virulence. Mol Microbiol. 2013;88(2):352–370. doi: 10.1111/mmi.12190. PubMed DOI

Kamoun S. A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol. 2006;44:41–60. doi: 10.1146/annurev.phyto.44.070505.143436. PubMed DOI

Song J, Win J, Tian M, Schornack S, Kaschani F, Ilyas M, van der Hoorn RA, Kamoun S. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc Natl Acad Sci U S A. 2009;106(5):1654–1659. doi: 10.1073/pnas.0809201106. PubMed DOI PMC

Soanes DM, Talbot NJ. Moving targets: rapid evolution of oomycete effectors. Trends Microbiol. 2008;16(11):507–510. doi: 10.1016/j.tim.2008.08.002. PubMed DOI

Tian M, Huitema E, Da Cunha L, Torto-Alalibo T, Kamoun S. A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J. Biol. Chem. 2004;279(25):26370–26377. doi: 10.1074/jbc.M400941200. PubMed DOI

Tian M, Benedetti B, Kamoun S. A Second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol. 2005;138(3):1785–1793. doi: 10.1104/pp.105.061226. PubMed DOI PMC

Tian M, Win J, Song J, van der Hoorn R, van der Knaap E, Kamoun S. A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol. 2007;143(1):364–377. doi: 10.1104/pp.106.090050. PubMed DOI PMC

Torto-Alalibo T, Tian M, Gajendran K, Waugh ME, van West P, Kamoun S. Expressed sequence tags from the oomycete fish pathogen Saprolegnia parasitica reveal putative virulence factors. BMC Microbiol. 2005;5:46. doi: 10.1186/1471-2180-5-46. PubMed DOI PMC

Cheung F, Win J, Lang JM, Hamilton J, Vuong H, Leach JE, Kamoun S, Andre Levesque C, Tisserat N, Buell CR. Analysis of the Pythium ultimum transcriptome using Sanger and Pyrosequencing approaches. BMC Genomics. 2008;9:542. doi: 10.1186/1471-2164-9-542. PubMed DOI PMC

Bouzidi MF, Parlange F, Nicolas P, Mouzeyar S. Expressed Sequence Tags from the oomycete Plasmopara halstedii, an obligate parasite of the sunflower. BMC Microbiol. 2007;7:110. doi: 10.1186/1471-2180-7-110. PubMed DOI PMC

Boutemy LS, King SR, Win J, Hughes RK, Clarke TA, Blumenschein TM, Kamoun S, Banfield MJ. Structures of Phytophthora RXLR effector proteins: a conserved but adaptable fold underpins functional diversity. J Biol Chem. 2011;286(41):35834–35842. doi: 10.1074/jbc.M111.262303. PubMed DOI PMC

Win J, Krasileva KV, Kamoun S, Shirasu K, Staskawicz BJ, Banfield MJ. Sequence divergent RXLR effectors share a structural fold conserved across plant pathogenic oomycete species. PLoS Pathog. 2012;8(1):e1002400. doi: 10.1371/journal.ppat.1002400. PubMed DOI PMC

Mestre P, Piron MC, Merdinoglu D. Identification of effector genes from the phytopathogenic Oomycete Plasmopara viticola through the analysis of gene expression in germinated zoospores. Fungal Biol. 2012;116(7):825–835. doi: 10.1016/j.funbio.2012.04.016. PubMed DOI

As-sadi F, Carrere S, Gascuel Q, Hourlier T, Rengel D, Le Paslier MC, Bordat A, Boniface MC, Brunel D, Gouzy J, et al. Transcriptomic analysis of the interaction between Helianthus annuus and its obligate parasite Plasmopara halstedii shows single nucleotide polymorphisms in CRN sequences. BMC Genomics. 2011;12:498. doi: 10.1186/1471-2164-12-498. PubMed DOI PMC

Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18(5):821–829. doi: 10.1101/gr.074492.107. PubMed DOI PMC

Parra G, Bradnam K, Korf I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics. 2007;23(9):1061–1067. doi: 10.1093/bioinformatics/btm071. PubMed DOI

Mi H, Lazareva-Ulitsky B, Loo R, Kejariwal A, Vandergriff J, Rabkin S, Guo N, Muruganujan A, Doremieux O, Campbell MJ, et al. The PANTHER database of protein families, subfamilies, functions and pathways. Nucleic Acids Res. 2005;33(Database issue):D284–288. doi: 10.1093/nar/gki078. PubMed DOI PMC

Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L, et al. InterPro: the integrative protein signature database. Nucleic Acids Res. 2009;37(Database issue):D211–215. doi: 10.1093/nar/gkn785. PubMed DOI PMC

Spring O. Homothallic sexual reproduction in Plasmopara halstedii, the downy mildew of sunflower. Helia. 2000;23(32):19–26.

Roy S, Kagda M, Judelson HS. Genome-wide prediction and functional validation of promoter motifs regulating gene expression in spore and infection stages of Phytophthora infestans. PLoS Pathog. 2013;9(3):e1003182. doi: 10.1371/journal.ppat.1003182. PubMed DOI PMC

Roy S, Poidevin L, Jiang T, Judelson HS. Novel core promoter elements in the oomycete pathogen Phytophthora infestans and their influence on expression detected by genome-wide analysis. BMC Genomics. 2013;14:106. doi: 10.1186/1471-2164-14-106. PubMed DOI PMC

Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37(Web Server issue):W202–208. doi: 10.1093/nar/gkp335. PubMed DOI PMC

Seidl MF, Wang R-P, Van den Ackerveken G, Govers F, Snel B. Bioinformatic Inference of Specific and General Transcription Factor Binding Sites in the Plant Pathogen Phytophthora infestans. PLoS One. 2013;7:e51295. doi: 10.1371/journal.pone.0051295. PubMed DOI PMC

Dolfini D, Zambelli F, Pavesi G, Mantovani R. A perspective of promoter architecture from the CCAAT box. Cell Cycle. 2009;8(24):4127–4137. doi: 10.4161/cc.8.24.10240. PubMed DOI

Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, Weber T. antiSMASH 2.0--a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res. 2013;41(Web Server issue):W204–212. doi: 10.1093/nar/gkt449. PubMed DOI PMC

Sieber SA, Marahiel MA. Molecular mechanisms underlying nonribosomal peptide synthesis: approaches to new antibiotics. Chem Rev. 2005;105(2):715–738. doi: 10.1021/cr0301191. PubMed DOI

Du L, Lou L. PKS and NRPS release mechanisms. Nat Prod Rep. 2010;27(2):255–278. doi: 10.1039/B912037H. PubMed DOI

Oome S, Van den Ackerveken G. Comparative and functional analysis of the widely occurring family of Nep1-like proteins. Mol Plant Microbe Interact. 2014;27(10):1081–94. doi: 10.1094/MPMI-04-14-0118-R. PubMed DOI

Cabral A, Oome S, Sander N, Kufner I, Nurnberger T, Van den Ackerveken G. Nontoxic Nep1-like proteins of the downy mildew pathogen Hyaloperonospora arabidopsidis: repression of necrosis-inducing activity by a surface-exposed region. Mol Plant Microbe Interact. 2012;25(5):697–708. doi: 10.1094/MPMI-10-11-0269. PubMed DOI

Stassen JH, Seidl MF, Vergeer PW, Nijman IJ, Snel B, Cuppen E, Van den Ackerveken G. Effector identification in the lettuce downy mildew Bremia lactucae by massively parallel transcriptome sequencing. Mol Plant Pathol. 2012;13(7):719–731. doi: 10.1111/j.1364-3703.2011.00780.x. PubMed DOI PMC

Dong S, Kong G, Qutob D, Yu X, Tang J, Kang J, Dai T, Wang H, Gijzen M, Wang Y. The NLP toxin family in Phytophthora sojae includes rapidly evolving groups that lack necrosis-inducing activity. Mol Plant Microbe Interact. 2012;25(7):896–909. doi: 10.1094/MPMI-01-12-0023-R. PubMed DOI

Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D, Thines M, Jiang RH, Zody MC, Kunjeti SG, Donofrio NM, et al. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science. 2010;330(6010):1540–1543. doi: 10.1126/science.1193070. PubMed DOI

Raffaele S, Kamoun S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol. 2012;10(6):417–430. PubMed

Judelson HS. Sexual Reproduction in Oomycetes: Biology, Diversity, and Contributions to Fitness. Inc. Hoboken: John Wiley & Sons; 2009.

Spring O, Zipper R. Evidence for asexual genetic recombination in sunflower downy mildew, Plasmopara halstedii. Mycol Res. 2006;110(Pt 6):657–663. doi: 10.1016/j.mycres.2006.03.009. PubMed DOI

Rozynek B, Spring O. Pathotypes of sunflower downy mildew in southern parts of Germany. HELIA. 2000;23(32):27–34.

Spring O, Bachofer M, Thines M, Riethmüller A, Göker M, Oberwinkler F. Intraspecific Relationship of Plasmopara halstedii Isolates Differing in Pathogenicity and Geographic Origin Based on ITS Sequence Data. Eur J Plant Pathol. 2006;114(3):309–315. doi: 10.1007/s10658-005-5996-9. DOI

Xiang Q, Judelson HS. Myb transcription factors in the oomycete Phytophthora with novel diversified DNA-binding domains and developmental stage-specific expression. Gene. 2010;453(1–2):1–8. doi: 10.1016/j.gene.2009.12.006. PubMed DOI

Bakthavatsalam D, Meijer HJG, Noegel AA, Govers F. Novel phosphatidylinositol phosphate kinases with a G-protein coupled receptor signature are shared by Dictyostelium and Phytophthora. Trends Microbiol. 2006;14(9):378–382. doi: 10.1016/j.tim.2006.07.006. PubMed DOI

Bode HB. Entomopathogenic bacteria as a source of secondary metabolites. Curr Opin Chem Biol. 2009;13(2):224–230. doi: 10.1016/j.cbpa.2009.02.037. PubMed DOI

Bolker M, Basse CW, Schirawski J. Ustilago maydis secondary metabolism-from genomics to biochemistry. Fungal Genet Biol. 2008;45(Suppl 1):S88–93. doi: 10.1016/j.fgb.2008.05.007. PubMed DOI

Waskiewicz A, Golinski P, Karolewski Z, Irzykowska L, Bocianowski J, Kostecki M, Weber Z. Formation of fumonisins and other secondary metabolites by Fusarium oxysporum and F. proliferatum: a comparative study. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2010;27(5):608–615. doi: 10.1080/19440040903551947. PubMed DOI

Spring O, Haas K. The fatty acid composition of Plasmopara halstedii and its taxonomic significance. Eur J Plant Pathol. 2002;108:263–267. doi: 10.1023/A:1015173900047. DOI

Yousef LF, Wojno M, Dick WA, Dick RP. Lipid profiling of the soybean pathogen Phytophthora sojae using Fatty Acid Methyl Esters (FAMEs) Fungal Biol. 2012;116(5):613–619. doi: 10.1016/j.funbio.2012.02.009. PubMed DOI

Keller NP, Turner G, Bennett JW. Fungal secondary metabolism - from biochemistry to genomics. Nat Rev Microbiol. 2005;3(12):937–947. doi: 10.1038/nrmicro1286. PubMed DOI

Schneider P, Weber M, Rosenberger K, Hoffmeister D. A one-pot chemoenzymatic synthesis for the universal precursor of antidiabetes and antiviral bis-indolylquinones. Chem. Biol. 2007;14(6):635–644. doi: 10.1016/j.chembiol.2007.05.005. PubMed DOI

Forseth RR, Amaike S, Schwenk D, Affeldt KJ, Hoffmeister D, Schroeder FC, Keller NP. Homologous NRPS-like gene clusters mediate redundant small-molecule biosynthesis in Aspergillus flavus. Angewandte Chemie. 2013;52(5):1590–1594. doi: 10.1002/anie.201207456. PubMed DOI PMC

Cohen Y, Sackston WE. Disappearance of IAA in the presence of tissues of sunflowers infected by Plasmopara halstedii. Can J Bot. 1974;52(4):861–866. doi: 10.1139/b74-108. DOI

Benz A, Spring O. Identification and characterization of an auxin-degrading enzyme in downy mildew infected sunflower. Physiol. Mol. Plant Pathol. 1995;46(3):163–175. doi: 10.1006/pmpp.1995.1013. DOI

Sharma R, Mishra B, Runge F, Thines M. Gene loss rather than gene gain is associated with a host jump from Monocots to Dicots in the Smut Fungus Melanopsichium pennsylvanicum. Genome Biol Evol. 2014;6(8):2034–2049. doi: 10.1093/gbe/evu148. PubMed DOI PMC

Feng BZ, Zhu XP, Fu L, Lv RF, Storey D, Tooley P, Zhang XG. Characterization of necrosis-inducing NLP proteins in Phytophthora capsici. BMC Plant Biol. 2014;14:126. doi: 10.1186/1471-2229-14-126. PubMed DOI PMC

Lee SJ, Rose JK. Mediation of the transition from biotrophy to necrotrophy in hemibiotrophic plant pathogens by secreted effector proteins. Plant Signal. Behav. 2010;5(6):769–772. doi: 10.4161/psb.5.6.11778. PubMed DOI PMC

Qutob D, Kamoun S, Gijzen M. Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J. 2002;32(3):361–373. doi: 10.1046/j.1365-313X.2002.01439.x. PubMed DOI

Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M, Thines M, Gaulin E, Kamoun S, Huitema E. Ancient class of translocated oomycete effectors targets the host nucleus. Proc Natl Acad Sci U S A. 2010;107(40):17421–17426. doi: 10.1073/pnas.1008491107. PubMed DOI PMC

Win J, Morgan W, Bos J, Krasileva KV, Cano LM, Chaparro-Garcia A, Ammar R, Staskawicz BJ, Kamoun S. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell. 2007;19(8):2349–2369. doi: 10.1105/tpc.107.051037. PubMed DOI PMC

Thines M, Kamoun S. Oomycete-plant coevolution: recent advances and future prospects. Curr Opin Plant Biol. 2010;13(4):427–433. doi: 10.1016/j.pbi.2010.04.001. PubMed DOI

Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, et al. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature. 2007;450(7166):115–118. doi: 10.1038/nature06203. PubMed DOI

van West P, de Bruijn I, Minor KL, Phillips AJ, Robertson EJ, Wawra S, Bain J, Anderson VL, Secombes CJ. The putative RxLR effector protein SpHtp1 from the fish pathogenic oomycete Saprolegnia parasitica is translocated into fish cells. FEMS Microbiol Lett. 2010;310(2):127–137. doi: 10.1111/j.1574-6968.2010.02055.x. PubMed DOI

Thines M, Voglmayr H. An Introduction to the White Blister Rusts (Albuginales) In: Lamour K, Kamoun S, editors. Oomycete Genetics and Genomics: Diversity, Interactions, and Research Tools. Hoboken: John Wiley & Sons; 2008.

Bailey H, Dagenbach D, Jennings JM. The locus of the benefits of repetition-lag memory training. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. 2011;18(5):577–593. doi: 10.1080/13825585.2011.591921. PubMed DOI

Yaeno T, Shirasu K. The RXLR motif of oomycete effectors is not a sufficient element for binding to phosphatidylinositol monophosphates. Plant Signal Behav. 2013;8(4):e23865. doi: 10.4161/psb.23865. PubMed DOI PMC

Dou D, Kale SD, Wang X, Jiang RH, Bruce NA, Arredondo FD, Zhang X, Tyler BM. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell. 2008;20(7):1930–1947. doi: 10.1105/tpc.107.056093. PubMed DOI PMC

Hemetsberger C, Mueller AN, Matei A, Herrberger C, Hensel G, Kumlehn J, Mishra B, Sharma R, Thines M, Huckelhoven R, et al. The fungal core effector Pep1 is conserved across smuts of dicots and monocots. New Phytol. 2015;206(3):1116–26. doi: 10.1111/nph.13304. PubMed DOI

Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estrano C, Haldar K. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science. 2004;306(5703):1934–1937. doi: 10.1126/science.1102737. PubMed DOI

Bhattacharjee S, Hiller NL, Liolios K, Win J, Kanneganti TD, Young C, Kamoun S, Haldar K. The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog. 2006;2(5):e50. doi: 10.1371/journal.ppat.0020050. PubMed DOI PMC

Marti M, Good RT, Rug M, Knuepfer E, Cowman AF. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science. 2004;306(5703):1930–1933. doi: 10.1126/science.1102452. PubMed DOI

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Sharma R, Thines M. FastQFS – A tool for evaluating and filtering paired-end sequencing data generated from high throughput sequencing. Mycological Progress. 2015;14:60.

Sharma R, Gassel S, Steiger S, Xia X, Bauer R, Sandmann G, Thines M. The genome of the basal agaricomycete Xanthophyllomyces dendrorhous provides insights into the organization of its acetyl-CoA derived pathways and the evolution of Agaricomycotina. BMC Genomics. 2015;16(1):233. doi: 10.1186/s12864-015-1380-0. PubMed DOI PMC

team RDc . R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2008.

Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674–3676. doi: 10.1093/bioinformatics/bti610. PubMed DOI

Nielsen H, Engelbrecht J, Brunak S, von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997;10(1):1–6. doi: 10.1093/protein/10.1.1. PubMed DOI

Li L, Stoeckert CJ, Jr, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13(9):2178–2189. doi: 10.1101/gr.1224503. PubMed DOI PMC

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22(21):2688–2690. doi: 10.1093/bioinformatics/btl446. PubMed DOI

Gaulin E, Madoui MA, Bottin A, Jacquet C, Mathe C, Couloux A, Wincker P, Dumas B. Transcriptome of Aphanomyces euteiches: new oomycete putative pathogenicity factors and metabolic pathways. Plos One. 2008;3:e1723. doi: 10.1371/journal.pone.0001723. PubMed DOI PMC