Skip to main content
SpringerLink
Log in

Evolution of Hyaloperonospora effectors: ATR1 effector homologs from sister species of the downy mildew pathogen H. arabidopsidis are not recognised by RPP1WsB

  • Original Article
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

Like other plant-pathogenic oomycetes, downy mildew species of the genus Hyaloperonospora manipulate their hosts by secreting effector proteins. Despite intense research efforts devoted to deciphering the virulence and avirulence activities of effectors in the H. arabidopsidis/Arabidopsis thaliana pathosystem, there is only a single study in this pathosystem on the variation of effectors and resistance genes in natural populations, and the evolution of these effectors in the context of pathogen evolution is studied even less. In this work, the identification of A rabidopsis t haliana recognised (ATR)1-homologs is reported in two sister species of H. arabidopsidis, H. thlaspeos-perfoliati, and H. crispula, which are specialized on the host plants Microthlaspi perfoliatum and Reseda lutea, respectively. ATR1-diversity within these sister species of H. arabidopsidis was evaluated, and the ATR1-homologs from different isolates of H. thlaspeos-perfoliati and H. crispula were tested to see if they would be recognised by the previously characterised RPP1-WsB protein from A. thaliana. None of the effectors from the sister species was recognised, suggesting that due to the adaptation to altered or new targets after a host jump, features of variable effectors might vary to a degree that recognition of orthologous Avr-causing effectors is no longer effective and probably does not contribute to non-host immunity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rehmany AP, Rose LE, Beynon JL (2004) Host–parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306:1957–1960

    Article  CAS  PubMed  Google Scholar 

  • Allen RL, Meitz JC, Baumber RE, Hall SA, Lee SC, Rose LE, Beynon JL (2008) Natural variation reveals key amino acids in a downy mildew effector that alters recognition specificity by an Arabidopsis resistance gene. Mol Plant Pathol 9:511–523

    Article  CAS  PubMed  Google Scholar 

  • Bailey K, Cevik V, Holton N, Byrne-Richardson J, Sohn KH, Coates M, Woods-Tör A, Aksoy HM, Hughes L, Baxter L, Jones JD, Beynon J, Holub EB, Tör M (2011) Molecular cloning of ATR5 (Emoy2) from Hyaloperonospora arabidopsidis, an avirulence determinant that triggers RPP5-mediated defense in Arabidopsis. Mol Plant Microbe Interact 24(7):827–838

    Article  CAS  PubMed  Google Scholar 

  • Boutemy LS, King SR, Win J, Hughes RK, Clarke TA, Blumenschein TM, Kamoun S, Banfield MJ (2011) Structures of phytophthora RXLR effector proteins: a conserved but adaptable fold underpins functional diversity. J Biol Chem 286:35834–35842

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bozkurt TO, Schornack S, Banfield M, Kamoun S (2012) Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol 15:1–10

    Article  Google Scholar 

  • Choi Y-J, Hong S-B, Shin H-D (2007) Re-consideration of Peronospora farinosa infecting Spinacia oleracea as distinct species, Peronospora effusa. Mycol Res 110:381–391

    Article  Google Scholar 

  • Choi Y-J, Shin HD, Thines M (2009) Two novel Peronospora species are associated with recent reports of downy mildew on sages. Mycol Res 13(Pt 12):1340–1350

    Article  Google Scholar 

  • Choi Y-J, Thines M, Han JG, Shin HD (2011) Mitochondrial phylogeny reveals intraspecific variation in Peronospora effusa, the spinach downy mildew pathogen. J Microbiol 49(6):1039–1043

    Article  PubMed  Google Scholar 

  • Choi Y-J, Beakes G, Glockling S, Kruse J, Nam B, Nigrelli L, Ploch S, Shin HD, Shivas RG, Telle S, Voglmayr H, Thines M (2015) Towards a universal barcode of oomycetes- a comparison of the cox1 and cox2 loci. Mol Ecol Resour. doi:10.1111/1755-0998

    PubMed  Google Scholar 

  • Chou S, Krasileva KV, Holton JM, Steinbrenner AD, Alber T, Staskawicz BJ (2011) Hyaloperonospora arabidopsidis ATR1 effector is a repeat protein with distributed recognition surfaces. Proc Natl Acad Sci U S A 108:13323–13328

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dangl JL, Holub EB, Debener T, Lehnackers H, Ritter C, Crute IR (1992) Genetic definition of loci involved in Arabidopsis pathogen interactions. In: Koncz C, Chua NH, Schell J (eds) Methods in arabidopsis research. World Scientific Pub, Singapore, pp 393–418

    Chapter  Google Scholar 

  • Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45:616–629

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Gäumann E (1918) Über die Formen der Peronospora parasitica (Pers.) Fries. Beih Bot Centralbl 35:395–533

    Google Scholar 

  • Gäumann E (1923) Beiträge zu einer Monographie der Gattung Peronospora Corda. Beitr Kryptogamenfl Schweiz 5:1–360

    Google Scholar 

  • Glowacki S, Macioszek VK, Kononowicz AK (2011) R proteins as fundamentals of plant innate immunity. Cell Mol Biol Lett 16:1–24

    Article  CAS  PubMed  Google Scholar 

  • Göker M, Voglmayr H, Riethmüller A, Weiß M, Oberwinkler F (2003) Taxonomic aspects of Peronosporaceae inferred from Bayesian molecular phylogenetics. Can J Bot 81:672–683

    Article  Google Scholar 

  • Göker M, Voglmayr H, Blázquéz GG, Oberwinkler F (2009) Species delimitation in downy mildews: the case of Hyaloperonospora in the light of nuclear ribosomal ITS and LSU sequences. Mycol Res 113:308–325

    Article  PubMed  Google Scholar 

  • Goritschnig S, Krasileva KV, Dahlbeck D, Staskawicz BJ (2012) Computational prediction and molecular characterization of an Oomycete effector and the cognate Arabidopsis resistance gene. PLoS Genet 8(2), e1002502

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hall S, Allen RL, Baumber RE, Baxter LA, Fisher K, Bittner-Eddy PD, Rose LE, Holub EB, Beynon JL (2009) Maintenance of genetic variation in plants and pathogens involves complex networks of gene-for-gene interactions. Mol Plant Pathol 10(4):449–457

    Article  CAS  PubMed  Google Scholar 

  • Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580

    Article  CAS  PubMed  Google Scholar 

  • Hogenhout SA, Van der Hoorn RA, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact 22(2):115–122

    Article  CAS  PubMed  Google Scholar 

  • Holsters M, Silva B, Van Vliet F, Genetello C, Block M, Dhaese P, Depicker A, Inzé D, Engler G, Villarroel R, Van Montagu M, Schell J (1980) The functional organization of the nopaline A. tumefaciens plasmid pTiC58. Plasmid 3:212–223

    Article  CAS  PubMed  Google Scholar 

  • Holub EB, Beynon JL, Crute IR (1994) Phenotypic and genotypic characterization of interactions between isolates of Peronospora parasitica and accessions of Arabidopsis thaliana. Mol Plant-Microbe Interact 7:223–239

    Article  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329

    Article  CAS  PubMed  Google Scholar 

  • Krasileva KV, Dahlbeck D, Staskawicz BJ (2010) Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22(7):2444–2458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krasileva KV, Zheng C, Leonelli L, Goritschnig S, Dahlbeck D, Staskawicz BJ (2011) Global analysis of Arabidopsis/downy mildew interactions reveals prevalence of incomplete resistance and rapid evolution of pathogen recognition. PLoS One 6(12), e28765

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685

    Article  CAS  PubMed  Google Scholar 

  • Lindbo JA (2007) TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol 145:1232–1240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, Tasan M, Galli M, Hao T, Nishimura MT, Pevzner SJ, Donovan SE, Ghamsari L, Santhanam B, Romero V, Poulin MM, Gebreab F, Gutierrez BJ, Tam S, Monachello D, Boxem M, Harbort CJ, McDonald N, Gai L, Chen H, He Y, European Union Effectoromics Consortium, Vandenhaute J, Roth FP, Hill DE, Ecker JR, Vidal M, Beynon J, Braun P, Dangl JL (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333(6042):596–601

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rehmany AP, Lynn JR, Tör M, Holub EB, Beynon JL (2000) A comparison of Peronospora parasitica (downy mildew) isolates from Arabidopsis thaliana and Brassica oleracea using amplified fragment length polymorphism and internal transcribed spacer 1 sequence analyses. Fungal Genet Biol 30:95–103

    Article  CAS  PubMed  Google Scholar 

  • Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, Whisson SC, Kamoun S, Tyler BM, Birch PR, Beynon JL (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17:1839–1850

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rentel MC, Leonelli L, Dahlbeck D, Zhao B, Staskawicz BJ (2008) Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens. Proc Natl Acad Sci U S A 105:1091–1096

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Riethmüller A, Voglmayr H, Göker M, Weiß M, Oberwinkler F (2002) Phylogenetic relationships of the downy mildews (Peronosporales) and related groups based on nuclear large subunit ribosomal DNA sequences. Mycologia 94:834–849

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 J, Haas BJ, Zody MC, Nusbaum C, Win J, Thines M, Kamoun S (2010) Ten things to know about oomycete effectors. Mol Plant Pathol 10(6):795–803

    Article  Google Scholar 

  • Sharma R, Mishra B, Runge F, Thines M (2014) 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 6:2034–2049

  • Slusarenko AJ, Schlaich NL (2003) Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Mol Plant Pathol 4:159–170

    Article  PubMed  Google Scholar 

  • Sökücü A, Thines M (2014) A molecular phylogeny of Basidiophora reveals several apparently host-specific lineages on Astereae. Mycol Progress 13:1137–1143

    Article  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75(5):758–771

    Article  Google Scholar 

  • Sumit R, Sahu BB, Xu M, Sandhu D, Bhattacharyya MK (2012) Arabidopsis non-host resistance gene PSS1 confers immunity against an oomycete and a fungal pathogen but not a bacterial pathogen that cause diseases in soybean. BMC Plant Biol 12:87

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thines M, Kamoun S (2010) Oomycete–plant coevolution: recent advances and future prospects. Curr Opin Plant Biol 13:427–433

    Article  PubMed  Google Scholar 

  • Thines M, Voglmayr H, Göker M (2009) Taxonomy and phylogeny of the downy mildews (Peronosporaceae). In: Lamour K, Kamoun S (eds) Oomycete genetics and genomics: diversity, interaction and research tools. John Wiley and Sons, Hoboken, pp 47–75

    Chapter  Google Scholar 

  • Voglmayr H (2003) Phylogenetic relationships of Peronospora and related genera based on nuclear ribosomal ITS sequences. Mycol Res 107:1132–1142

    Article  CAS  PubMed  Google Scholar 

  • Voglmayr H, Constantinescu O (2008) Revision and reclassification of three Plasmopara species based on morphological and molecular phylogenetic data. Mycol Res 112:487–501

    Article  CAS  PubMed  Google Scholar 

  • Voglmayr H, Riethmüller A, Göker M, Weiß M, Oberwinkler F (2004) Phylogenetic relationships of Plasmopara, Bremia and other genera of downy mildews with pyriform haustoria based on Bayesian analysis of partial LSU rDNA sequence data. Mycol Res 108:1011–1024

    Article  CAS  PubMed  Google Scholar 

  • Weigel D, Glazebrook J (2006) Transformation of agrobacterium using electroporation. CSH Protoc. doi:10.1101/pdb.prot4665

  • Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, Hein I, Toth IK, Pritchard L, Birch PR (2007) A translocation signal for elivery of oomycete effector proteins into host plant cells. Nature 450:115–118

    Article  CAS  PubMed  Google Scholar 

  • Win J, Krasileva KV, Kamoun S, Shirasu K, Staskawicz BJ, Banfield MJ (2012) Sequence divergent RXLR effectors share a structural fold conserved across plant pathogenic oomycete species. PLoS Pathog 8, e1002400

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yerkes WD, Shaw CG (1959) Taxonomy of the Peronospora species on Cruciferae and Chenopodiaceae. Phytopathol 49:499–507

    Google Scholar 

Download references

Acknowledgments

Funding by the LOEWE initiative of the state of Hessen in the framework of the Cluster for Integrative Fungal Research (IPF) and the Biodiversity and Climate Research Centre (BiK-F), as well as from the Max Planck Society and the Gatsby Charitable Foundation are gratefully acknowledged. We are grateful to Ksenia Krasileva and Brian Staskawicz for providing biological material.

Author information

Authors and Affiliations

  1. Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, D-60325, Frankfurt am Main, Germany

    Irina Solovyeva, Sebastian Ploch & Marco Thines

  2. Institute of Botany 210, University of Hohenheim, D-70593, Stuttgart, Germany

    Angelika Schmuker

  3. The Sainsbury Laboratory, Norwich Research Park, NR4 7UH, UK

    Liliana M. Cano, Mireille van Damme & Sophien Kamoun

  4. Integrative Fungal Research Cluster (IPF), Georg-Voigt-Str. 14-16, D-60325, Frankfurt am Main, Germany

    Marco Thines

  5. Department of Biosciences, Institute of Ecology, Evolution and Diversity, Goethe University Frankfurt am Main, Max-von-Laue-Str. 9, D-60438, Frankfurt am Main, Germany

    Marco Thines

  6. Laboratory of Phytopathology, Wageningen University, 6708 PB, Wageningen, The Netherlands

    Mireille van Damme

Authors
  1. Irina Solovyeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angelika Schmuker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liliana M. Cano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mireille van Damme
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sebastian Ploch
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sophien Kamoun
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marco Thines
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Irina Solovyeva or Marco Thines.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Table 1

(DOC 30 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Solovyeva, I., Schmuker, A., Cano, L.M. et al. Evolution of Hyaloperonospora effectors: ATR1 effector homologs from sister species of the downy mildew pathogen H. arabidopsidis are not recognised by RPP1WsB . Mycol Progress 14, 53 (2015). https://doi.org/10.1007/s11557-015-1074-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11557-015-1074-7

Keywords

Search

Navigation