Skip to main content

RETRACTED ARTICLE: Pathogen virulence of Phytophthora infestans: from gene to functional genomics

Physiology and Molecular Biology of Plants volume 19, pages 165–177 (2013)Cite this article

This article was retracted on 09 November 2014

Abstract

The oomycete, Phytophthora infestans, is one of the most important plant pathogens worldwide. Much of the pathogenic success of P. infestans, the potato late blight agent, relies on its ability to generate large amounts of sporangia from mycelia, which release zoospores that encyst and form infection structures. Until recently, little was known about the molecular basis of oomycete pathogenicity by the avirulence molecules that are perceived by host defenses. To understand the molecular mechanisms interplay in the pathogen and host interactions, knowledge of the genome structure was most important, which is available now after genome sequencing. The mechanism of biotrophic interaction between potato and P. infestans could be determined by understanding the effector biology of the pathogen, which is until now poorly understood. The recent availability of oomycete genome will help in understanding of the signal transduction pathways followed by apoplastic and cytoplasmic effectors for translocation into host cell. Finally based on genomics, novel strategies could be developed for effective management of the crop losses due to the late blight disease.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Ah Fong AM, Judelson HS (2004) The hAT -like DNA transposon DodoPi resides in a cluster of retro- and DNA transposons in the stramenopile Phytophthora infestans. Mol Genet Genomics 271:577–585

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Andrivon D (1995) Biology, ecology, and epidemiology of the potato late blight pathogenic soil. Phytopathol 85:1053–1056

    Google Scholar 

  • Armstrong MR, Whisson SC, Pritchard L (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc Natl Acad Sci USA 102:7766–7771

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bartnicki-Garcia S (1968) Cell wall chemistry, morphogenesis and taxonomy of fungi. Annu Rev Microbiol 2:88–108

    Google Scholar 

  • Bartnicki-Garcia S, Wang MC (1983) Biochemical aspects of morphogenesis in Phytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora: its biology, taxonomy, ecology, and pathology. Am Phytopathol Soc Press, St Paul, pp 121–138

    Google Scholar 

  • Birch PRJ, Rehmany AP, Pritchard L, Kamoun S, Beynon JL (2006) Trafficking arms: oomycete effectors enter host plant cell. Trends Microbiol 14:8–11

    PubMed  CAS  Google Scholar 

  • Bol JF, Linthorst HJM, Cornelissen BJC (1990) Plant pathogenesis-related proteins induced by virus infection. Annu Rev Phytopathol 28:113–138

    CAS  Google Scholar 

  • Bolker M (1998) Sex and crime:heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet Biol 25:143–156

    PubMed  CAS  Google Scholar 

  • Borkowska OB, Kedrak A, Truszczynski M, Rutkouska J (1998) Field examination of the Boviseptivac vaccine and measurement of the IgG anti Pasteurella multocida level by the ELISA. Bull Vet Inst (Pulawy) 42:21–31

    Google Scholar 

  • Bos JI, Chaparro-Garcia A, Quesada-Ocampo LM, McSpadden Gardener BB, Kamoun S (2009) Distinct amino acids of the Phytophthora infestans effector AVR3a condition activation of R3a hypersensitivity and suppression of cell death. Mol Plant Microbe Interact 22:269–281

    PubMed  CAS  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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bradshaw JE, Bryan GJ, Lees AK, McLean K, Solomon-Blackburn RM (2006) Mapping the R10 and R11 genes for resistance to late blight (Phytophthora infestans) present in the potato (Solanum tuberosum) R-gene differentials of black. Theor Appl Genet 112:744–751

    PubMed  CAS  Google Scholar 

  • Broglie K, Chet I, Holliday M, Cressman R, Biddle P, Knowlton S, Mauvais CJ, Broglie R (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254:1194–1197

    PubMed  CAS  Google Scholar 

  • Bulone V, Chanzy H, Gay L, Girard V, Fèvre M (1992) Characterisation of chitin and chitin synthase from the cellulosic cell wall fungus Saprolegnia monoica. Exp Mycol 16:8–21

    CAS  Google Scholar 

  • Catanzariti AM, Dodds PN, Lawrence GJ, Agliffe MA, Ellis JG (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18:243–256

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    PubMed  CAS  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 USA 108:13323–13328

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cutt JR, Klessig DF (1992) Pathogenesis-related proteins. In: Boller T, Meins F (eds) Genes involved in plant defense. Springer, New York, pp 209–243

    Google Scholar 

  • Daly DC (1996) The blight is back. Nat History 105:31

    Google Scholar 

  • Damascene CM, Bishop JG, Ripoll DR, Win J, Kamoun S, Rose JK (2008) Structure of the glucanase inhibitor protein (GIP) family from Phytophthora species suggests co- evolution with plant endo—beta-1, 3- glucanases. Mol Plant Microbe Interact 21:820–830

    Google Scholar 

  • Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980–986

    PubMed  CAS  Google Scholar 

  • Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50:245–276

    PubMed  CAS  Google Scholar 

  • Dodds PN, Lawrence GJ, Catanzariti AM, Ayliye MA, Ellis JG (2004) The Melamspora lini Avrl567 avirulence genes are expressed in haustoria and their product are recognized inside plant cells. Plant Cell 16:755–768

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, Arredondo FD, Zhang X, Tyler BM (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen encoded machinery. Plant Cell 20:1930–1947

    PubMed  CAS  PubMed Central  Google Scholar 

  • Drenth A, Janssen EM, Govers F (1995) Formation and survival of oospores of Phytophthora infestans under natural conditions. Plant Pathol 44:86–94

    Google Scholar 

  • El Kharbotly A, Leonards Schippers C, Huigen DJ, Jacobsen E, Pereira A, Stiekema WJ, Salamini F, Gebhardt C (1994) Segregation analysis and RFLP mapping of the R1 and R3 alleles conferring race-specific resistance to Phytophthora infestans in progeny of dihaploid potato parents. Mol Gen Genet 242:749–754

    PubMed  CAS  Google Scholar 

  • Ellis JG, Dodds PN (2011) Showdown at the RXLR motif: serious differences of enter plant cells. Proc Natl Acad Sci USA 108:14381–14382

    PubMed  CAS  PubMed Central  Google Scholar 

  • Erwin DC, Ribeiro K (1996) Phytophthora diseases worldwide. Am Phytopathological Soc, St Paul, pp 54–58

    Google Scholar 

  • Frinking HD, Davidse LC, Limburg H (1987) Oospore formation by Phytophthora infestans in host tissue after inoculation with isolates of opposite mating type found in the Netherlands. Netherlands J Plant Pathol 93:147–149

    Google Scholar 

  • Fry W (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9:385–402

    PubMed  Google Scholar 

  • Gan PH, Rafiqi M, Ellis JG, Jones DA, Hardham AR, Dodds PN (2010) Lipid binding activities of flax rust AvrM and AvrL567 effectors. Plant Signal Behav 5:1272–1275

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gohre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46:189–215

    PubMed  Google Scholar 

  • Govers F, Gizen M (2006) Phytophthora genomics: the plant destroyers’ genome decoded. Mol Plant Microbe interact 19:1295–1301

    PubMed  CAS  Google Scholar 

  • Grenville-Briggs LJ, van West P (2005) The biotrophic stages of oomycete-plant interactions. In: Laskin AI, Bennett JW, Gadd GM (eds) Advances in applied microbiology 57. Academic, San Diego, pp 217–243

    Google Scholar 

  • Grenville-Briggs LJ et al (2008) Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of Potato. Plant Cell 20:720–738

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hahn M, Mend Gen K (2001) Signal and nutrient exchange at biotrophic plant–fungus interfaces. Curr Opin Plant Biol 4:322–327

    PubMed  CAS  Google Scholar 

  • Hanson K, Shattock RC (1998) Formation of oospores of Phytophthora infestans in cultivars of potato with different levels of race-nonspecific resistance. Plant Pathol 47:123–129

    Google Scholar 

  • Hass B et al (2009) The genome sequence of the Irish famine pathogen Phytophthora infestans. Nature 461:393–398

    Google Scholar 

  • Heath MC, Boller T (2002) Editorial overview: levels of complexity in plant interactions with herbivores, pathogens and mutualism. Curr Opin Plant Biol 5:277–278

    Google Scholar 

  • Helbert W, Sugiyama J, Ishihara M, Yamanaka S (1997) Characterization of native crystalline cellulose in the cell walls of oomycota. J Biotechnol 57:29–37

    CAS  Google Scholar 

  • Huang G, Gao B, Maier T, Allen R, Davis EL, Baum TJ, Hussey RS (2003) A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne iniognita. Mol Plant Microbe Interact 16:376–381

    PubMed  CAS  Google Scholar 

  • Huang SW, Vleeshouwers V, Werij JS, Hutten RCB, van Eck HJ, Visser RGF, Jacobsen E (2004) The R3 resistance to Phytophthora infestans in potato is conferred by two closely linked R genes with distinct specificities. Mol Plant Microbe Interact 17:428–435

    PubMed  CAS  Google Scholar 

  • Huang SW, van der Vossen EAG, Kuang HH, Vleeshouwers VGAA, Zhang NW, Borm TJA, van Eck HJ, Baker B, Jacobsen E, Visser RGF (2005) Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J 42:251–261

    PubMed  CAS  Google Scholar 

  • Huitema E, Bos JIB, Tian M, Win J, Waugh ME, Kamoun S (2004) Linking sequence to phenotype in Phytophthora-plant interactions. Trends Microbiol 12:193–200

    PubMed  CAS  Google Scholar 

  • Jeun YC, Buchenauer H (2001) Infection structures and localization of pathogenesis related protein AP24 in leaves of tomato plants exhibiting systemic acquired resistance against Phytophthora infestans after pre-treatment with 3-aminobutyric acid or tobacco necrosis virus. J Phytopathol 149:141–153

    CAS  Google Scholar 

  • Jiang RHY, Dawe AL, Weide R, van Staveren M, Peters S, Nuss DL, Govers F (2005) Elicitin genes in Phytophthora infestans are clustered and interspersed with various transposon- like elements. Mol Genet Genomics 273:20–32

    PubMed  CAS  Google Scholar 

  • Jiang RHY, Tyler BM, Govers F (2006) Comparative analysis of Phytophthora gene encoding secreted proteins reveals conserved synteny and lineage—specific gene duplications and deletions. Mol Plant Microbe interact 19:1311–1321

    PubMed  CAS  Google Scholar 

  • Jiang RH, Tripathy S, Govers F, Tyler BM (2008) RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proc Natl Acad Sci USA 105:4874–4879

    PubMed  CAS  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Judelson HS (2002) Sequence variation and genomic amplification of a family of Gypsy-like sequences in the oomycete genus Phytophthora. Mol Biol Evol 19:1313–1322

    PubMed  CAS  Google Scholar 

  • Judelson HS, Blanco FA (2005) The spores of Phytophthora: weapons of the plant destroyer. Nature Rev Microbiol 3:47–58

    CAS  Google Scholar 

  • Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A et al (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal hostcells. Cell 142:284–295

    PubMed  CAS  Google Scholar 

  • Kamoun S (2003) Molecular genetics of pathogenic oomycetes. Euk Cell 2:191–199

    CAS  Google Scholar 

  • Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44:41–60

    PubMed  CAS  Google Scholar 

  • Kamoun S (2007) Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol 10:358–365

    PubMed  CAS  Google Scholar 

  • Kamoun S, Goodwin SB (2007) Fungal and oomycete genes galore. New Phytol 173:713–717

    Google Scholar 

  • Kamoun S, Smart CD (2005) Late blight of potato and tomato in the genomics era. Plant Dis 89:692–699

    CAS  Google Scholar 

  • Kemen E, Kemen AC, Rafiqi M, Hempel V, Mendgen K, Hahn M, Voegele RT (2005) Identification of a protein from rust fungi transformed from haustoria into infected plant cell. Mol Plant Microbe Interact 18:1130–1139

    PubMed  CAS  Google Scholar 

  • Kronstad JW (1997) Virulence and cAMP in smuts, blasts and blights. Trends Plant Sci 2:193–199

    Google Scholar 

  • Lamour KH, Win J, Kamoun S (2007) Oomycete genomics: new insights and future directions. FEMS Microbiol Lett 274:1–8

    PubMed  CAS  Google Scholar 

  • Latijnhouwers M, Govers F (2003) A Phytophthora infestans G-Protein beta subunit is involved in sporangium formation. Euk Cell 2:971–977

    CAS  Google Scholar 

  • Latijnhouwers M, Ligterink W, Vleeshouwers VGAA, van West P, Govers F (2004) A Gα subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans. Mol Microbiol 51:925–936

    PubMed  CAS  Google Scholar 

  • Lee U, Ripflorido I, Hong S, Lurkindale JE, Waters E, Vierling (2007) The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J 49:115–127

    PubMed  CAS  Google Scholar 

  • Lengeler et al (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64:746–785

    PubMed  CAS  PubMed Central  Google Scholar 

  • Leonelli L, Pelton J, Schoeffler A, Dahlbeck D, Berger J, Wemmer DE, Staskawicz B (2011) Structural elucidation and functional characterization of the Hyaloperonospora arabidopsidis effector protein ATR13. PLoS Pathogens 7:e1002428

    PubMed  CAS  PubMed Central  Google Scholar 

  • Liu D et al (1994) Osmotin over expression in potato delays development of disease symptoms. Proc Natl Acad Sci USA 91:1888–1892

    PubMed  CAS  PubMed Central  Google Scholar 

  • Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Jul Cell 12:147–157

    CAS  Google Scholar 

  • Marguilis L, Schwartz KV (2000) Five kingdoms: an illustrated guide to the phyla of life on earth. W. H. Freeman and Co, New York

    Google Scholar 

  • Meijer HJG, Govers F (2006) Genomewide analysis of phospholipid signalling genes in Phytophthora spp. Novelties and a missing Link. Am Phytopathol Soc 19:1337–1347

    CAS  Google Scholar 

  • Morgan W, Kamoun S (2007) RXLR effectors of plant pathogenic oomycetes. Curr Opin Microbiol 10:332–338

    PubMed  CAS  Google Scholar 

  • Mosa AA, Kobayashi K, Ogoshi A, Kato M, Sato N (1991) Formation of oospores by Phytophthora infestans in inoculated potato tissues. Annu Phytopathol Soc Japan 57:334–338

    Google Scholar 

  • Ottmann C, Luberacki B, Kufner I, Koch W, Brunner F, Weyand M, Mattinen L, Pirhonen M, Seitz HU (2009) A common toxin fold mediates microbial attack and plant defence. Proc Natl Acad Sci USA 106:10359–10364

    PubMed  CAS  PubMed Central  Google Scholar 

  • Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Curr Opin Plant Biol 6:320–326

    PubMed  CAS  Google Scholar 

  • Plett JM, Kemppainen M, Kale SD, Kohler A, Legue V, Brun A et al (2011) A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol 21:1197–1203

    PubMed  CAS  Google Scholar 

  • Ponchet M, Panabieres F, Milat ML, Mikes V, Montillet JL, Suty L, Triantaphylides C, Trilly Y, Blein JP (1999) Are elicitins cryptograms in plant –oomycete communications? Cell Mol Life Sci 56:1020–1047

    PubMed  CAS  Google Scholar 

  • Portieles R et al (2010) NmDef02, a novel antimicrobial gene isolated from Nicotiana megalosiphon confers high-level pathogen resistance under greenhouse and field conditions. Plant Biotech J 8:678–690

    CAS  Google Scholar 

  • Qutob D, Tedman-Jones J, Gijzen M (2006) Effector-triggered immunity by the plant pathogen Phytophthora. Trends Microbiol 14:470–473

    PubMed  CAS  Google Scholar 

  • Rehmany AP et al (2005) Differential recognition of highly divergent downy mildew virulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17:1839–1850

    PubMed  CAS  PubMed Central  Google Scholar 

  • Robertson NF (1991) The challenge of Phytophthora infestans. Adv Plant Pathol 7:1–30

    Google Scholar 

  • Rose JK, Ham KS, Darvill AG, Albersheim P (2002) Molecular cloning a characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by plant pathogens. Plant Cell 14:1329–1345

    PubMed  CAS  PubMed Central  Google Scholar 

  • Saxena I, Brown R (2000) Cellulose synthases and related enzymes. Curr Opin Plant Biol 3:523–531

    PubMed  CAS  Google Scholar 

  • Schumann GL, D’Archy CJ (2000) Late blight of potato and tomato. The plant health instructor. doi:10.1094/PHI-I-2000-0724-01.[http://www.apsnet.org]

  • Seok Jun M, Ardales EY, Shin D, Han S, Lee HE, Park SR (2009) The EREBP-gene from Solanum tuberosum confers resistance against Oomycetes and a bacterial pathogen in transgenic potato and tobacco plants. Fruits, Vegetable and Cereal Science and Biotechnology 3. Global Sci. Books 1:72–79

    Google Scholar 

  • Shaan W, Cao M, Leung D, Tyler BM (2004) The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance genes Rps1b. Mol Plant Microbe interact 17:394–403

    Google Scholar 

  • Shi X et al (2012) A potato pathogenesis-related protein gene, StPRp27, contributes to race-nonspecific resistance against Phytophthora infestans. Mol Biol Rep 39:1909–1916

    PubMed  CAS  Google Scholar 

  • Song J et al (2003) Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc Natl Acad Sci USA 100:9128–9133

    PubMed  CAS  PubMed Central  Google Scholar 

  • Strittmatter P, Nakamura F, Strittmatter SM (1998) GAP-43 augmentation of G protein- mediated signal transduction is regulated by both phosphorylation and palmitoylation. J Neurochem 70:983–992

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Thomma BPHJ, Cammue BPA, Thevissen K (2002) Plant defensins. Planta 216:193–202

    PubMed  CAS  Google Scholar 

  • Tian M, Kamoun S (2005) A two disulfide bridge Kazal domain from Phytophthora exhibits stable inhibitory activity against serine proteases of the subtilisin family. BMC Biochem 6:15

    PubMed  PubMed Central  Google Scholar 

  • 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 P69 B. J Biochem 279:26370–26377

    CAS  Google Scholar 

  • Tian M, Benedetti B, Kamoun S (2005) A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol 138:1785–1793

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tian M, Win J, Song J, van der Hoorn R, van der Knaap E, Kamoun S (2007) A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol 143:364–377

    PubMed  CAS  PubMed Central  Google Scholar 

  • Torto TA, Li SA, Styler A, Huitema E, Testa A et al (2003) EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Res 13:1675–1685

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tyler BM (2009) Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell Microbiol 11:13–20

    PubMed  CAS  Google Scholar 

  • Tyler BH et al (2006) Phytophthora genome sequence uncovers evolutionary origins and mechanism of pathogenesis. Science 313:1261–1266

    PubMed  CAS  Google Scholar 

  • Van Poppel PMJA, Guo J, van de Vandervoort PJI, Jung MWJ, Birch PRJ, Whisson SC, Govers F (2008) The Phytophthora infestans avirulence gene Avr4 encodes an RXLR-dEER effector. Mol Plant-Microbe Interact 21:1460–1470

    PubMed  Google Scholar 

  • Van West P, Appiah AA, Gow NAR (2003) Advances in research on root pathogenic oomycetes. Physiol Mol Plant Pathol 62:99–113

    Google Scholar 

  • Vleeshouwers VG et al (2008) Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes. PLoS One 3:e2875

    PubMed  PubMed Central  Google Scholar 

  • Walker C, van West P (2007) Zoospore development in the oomycetes. Fungal Biol Rev 21:10–18

    Google Scholar 

  • Whisson SC et al (2007) A translocation signal for delivery of oomycete effector proteins inside host plant cells. Nature 450:115–118

    PubMed  CAS  Google Scholar 

  • Win J, Kenneganti TD, Torto-Alalibo T, Kamoun S (2006) Computational and comparative analysis of 150 full-length cDNA sequences from the oomycete plant—pathogen Phytophthora infestans. Fungal Genet Biol 43:20–33

    PubMed  CAS  Google Scholar 

  • Win J et al (2007) Adaptive evolution has targeted the C- terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 19:2349–2369

    PubMed  CAS  PubMed Central  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 Pathogens 8:e1002400

    PubMed  CAS  PubMed Central  Google Scholar 

  • Woloshuk CP, Meulenhoff JS, Sela Buurlage M, van den Elzen PJM, Cornelissen BJ (1991) Cornelissen pathogen-induced proteins with inhibitory activity toward Phytophthora infestans. Plant Cell 3:619–628

    PubMed  CAS  PubMed Central  Google Scholar 

  • Xu JR, Peng Y-L, Dickman M, Band Sharon A (2006) The dawn of fungal pathogen genomics. Annu Rev Phytopathol 44:337–366

    PubMed  CAS  Google Scholar 

  • Yaeno T, Li Hua, Chaparro-Garcia et al (2011) Phosphatidylinositol 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 108:14682–14687

  • Zadoks JC (2008) The potato murrain on the European continent and the revolutions of 1848. Potato Res 51:5–45

    Google Scholar 

  • Zhu B, Chen THH, Li PH (1996) Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for an osmotin-like protein. Planta 198:70–77

    PubMed  CAS  Google Scholar 

Download references

Author information

Affiliations

  1. Central potato Research Institute, Shimla, H.P, India, 171001

    Suman Sanju, Aditi Thakur, Sundresha Siddappa & B. P. Singh

  2. Department of Biosciences and Biotechnology, Banasthali University (Rajasthan), Tonk, India, 304022

    Nidhi Srivastava

  3. Department of Biological Sciences, School of Basic Sciences, SHIATS, Naini, Allahabad, India, 211007

    Pradeep Shukla

  4. National Research Centre for Plant Biotechnology, IARI campus, Pusa, New Delhi—12, India

    Rohini Sreevathsa

Authors
  1. Suman Sanju
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aditi Thakur
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sundresha Siddappa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rohini Sreevathsa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nidhi Srivastava
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pradeep Shukla
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. B. P. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rohini Sreevathsa.

Additional information

Suman Sanju and Aditi Thakur contributed equally.

The authors hereby retract their review article titled "Pathogen virulence of Phytophthora infestans: from gene to functional genomics" (Sanju et al., 2013), previously published in print and online versions of the journal Physiology and Molecular Biology of Plants, due to unattributed use of some text from articles previously published elsewhere without permission (Govers, F. and Gizjen, M., 2006), (Huitema, E. et al, 2005), (Kamoun, S. 2003), (Widmark, A.-K., 2010). This decision was taken to avoid repetition and for the upkeep of professional ethics. All authors sincerely apologize for the inconvenience caused. Reference List Sanju, S., Thakur, A., Siddappa, S., Sreevathsa. R., Srivastava, N., Shukla, P. and Singh, B. P. (2013). Pathogen virulence of Phytophthora infestans: from gene to functional genomics. Physiology and Molecular Biology of Plants, 19(2):165-177 Widmark, A.-K. (2010). The Late Blight Pathogen, Phytophthora infestans. Interaction with the Potato Plant and Inoculum Sources. Doctoral thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden. Govers, F. and Gizjen, M. (2006).Phytophthora Genomics: The Plant Destroyers' Genome Decoded. Molecular Plant-Microbe Interactions 19 (12): 1295-1301 Kamoun S. (2003). Molecular genetics of pathogenic oomycetes. Eukaryotic Cell, 2:191-199. Huitema, E., Vleeshouwers, V.G.A.A., Cakir, C., Kamoun, S., and Govers, F. (2005). Differences in intensity and specificity of hypersensitive response induction in Nicotiana spp. by INF1, INF2A and INF2B of Phytophthora infestans. Molecular Plant-Microbe Interactions, 18:183-193.

An erratum to this article can be found online at http://dx.doi.org/10.1007/s12298-014-0263-1.

An erratum to this article is available at http://dx.doi.org/10.1007/s12298-014-0263-1.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sanju, S., Thakur, A., Siddappa, S. et al. RETRACTED ARTICLE: Pathogen virulence of Phytophthora infestans: from gene to functional genomics. Physiol Mol Biol Plants 19, 165–177 (2013). https://doi.org/10.1007/s12298-012-0157-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-012-0157-z

Keywords

  • Phytophthora infestans
  • Oomycetes
  • GPCR
  • Signal molecule
  • Effectors
  • RXLR –dEER
  • Crinklers