Identification and analysis of Phytophthora cactorum genes up-regulated during cyst germination and strawberry infection

Current Genetics

Volumn 57, Issue 5, 2011, Pages 297-315

  Chen, Xiaoren ^a,b   Klemsdal, Sonja Sletner ^a   Brurberg, May Bente ^a  

^a NORWEGIAN INSTITUTE OF BIOECONOMY RESEARCH   (Norway)

^b YANGZHOU UNIVERSITY   (China)

Author keywords

Differential display; Phytophthora cactorum; Real time PCR; RxLR effectors; SSH; Strawberry

Indexed keywords

ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DIFFERENTIAL DISPLAY; DNA LIBRARY; EFFECTOR SPECIFIC DIFFERENTIAL DISPLAY; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GENOME; HOST; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYTOPHTHORA CACTORUM; PLANT; PLANT DISEASE; PLANT GENE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRAWBERRY; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; UPREGULATION;

EXPRESSED SEQUENCE TAGS; FRAGARIA; GENE LIBRARY; MOLECULAR SEQUENCE DATA; NUCLEIC ACID HYBRIDIZATION; PHYTOPHTHORA; PLANT DISEASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION;

FRAGARIA X ANANASSA; PHYTOPHTHORA CACTORUM;

EID: 80054703101     PISSN: 01728083     EISSN: 14320983     Source Type: Journal    
DOI: 10.1007/s00294-011-0348-0     Document Type: Article

References (64)

1. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389 3402 9254694 10.1093/nar/25.17.3389 1:CAS:528:DyaK2sXlvFyhu7w%3D (Pubitemid 27359211)
2. K Beyer A Binder T Boller M Collinge 2001 Identification of potato genes induced during colonization by Phytophthora infestans Mol Plant Pathol 2 125 134 20573000 10.1046/j.1364-3703.2001.00059.x 1:CAS:528:DC%2BD3MXmtVyntLY%3D (Pubitemid 32664951)
3. PRJ Birch PC Boevink EM Gilroy I Hein L Pritchard SC Whisson 2008 Oomycete RXLR effectors: delivery functional redundancy, and durable disease resistance Curr Opin Plant Biol 11 373 379 18511334 10.1016/j.pbi.2008.04.005 1:CAS:528:DC%2BD1cXpsVamtb0%3D
4. Bouwmeester K, van Poppel PMJA, Govers F (2009) Genome biology cracks enigmas of oomycete plant pathogens. In: Parker JE (ed) Molecular aspects of plant disease resistance. Wiley-Blackwell, Oxford United Kingdom, pp 102-133
5. F Brunner S Rosahl J Lee JJ Rudd C Geiler S Kauppinen G Rasmussen D Scheel T Nurnberger 2002 Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases EMBO J 21 6681 6688 12485989 10.1093/emboj/cdf667 1:CAS:528:DC%2BD38XpslOhu7o%3D (Pubitemid 36014540)
6. XR Chen G Shen YL Wang XB Zheng YC Wang 2007 Identification of Phytophthora sojae genes upregulated during the early stage of soybean infection FEMS Microbiol Lett 269 280 288 17263843 10.1111/j.1574-6968.2007.00639.x 1:CAS:528:DC%2BD2sXktVOmsrw%3D (Pubitemid 46449734)
7. S Costanzo MD Ospina-Giraldo KL Deahl CJ Baker RW Jones 2007 Alternate intron processing of family 5 endoglucanase transcripts from the genus Phytophthora Curr Genet 52 115 123 17661047 10.1007/s00294-007-0144-z 1:CAS:528:DC%2BD2sXps1Glsrk%3D (Pubitemid 47343270)
8. TM Davis H Yu 1997 A linkage map of the diploid strawberry Fragaria vesca J Hered 88 215 221 1:CAS:528:DyaK2sXkt1emurY%3D (Pubitemid 27242218)
9. L Diatchenko YF Lau AP Campbell, et al. 1996 Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries Proc Natl Acad Sci USA 93 6025 6030 8650213 10.1073/pnas.93.12.6025 1:CAS:528:DyaK28Xjs1Ojsbk%3D (Pubitemid 26190796)
10. D Dou SD Kale X Wang RHY Jiang NA Bruce FD Arredondo X Zhang BM Tyler 2008 RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery Plant Cell 20 1930 1947 18621946 10.1105/tpc.107.056093 1:CAS:528:DC%2BD1cXhtVyrsbfP (Pubitemid 352844542)
11. T Ebstrup G Saalbach H Egsgaard 2005 A proteomics study of in vitro cyst germination and appressoria formation in Phytophthora infestans Proteomics 5 2839 2948 15996011 10.1002/pmic.200401173 1:CAS:528:DC%2BD2MXnvVWhtLY%3D (Pubitemid 41059761)
12. H Eikemo A Stensvand AM Tronsmo 2000 Evaluation of methods of screening strawberry cultivars for resistance to crown rot caused by Phytophthora cactorum Ann Appl Biol 137 237 244 10.1111/j.1744-7348.2000.tb00064.x (Pubitemid 32386140)
13. H Eikemo SS Klemsdal I Riisberg P Bonants A Stensvand AM Tronsmo 2004 Genetic variation between Phytophthora cactorum isolates differing in their ability to cause crown rot in strawberry Mycol Res 108 317 324 15185982 10.1017/S0953756204009244 1:CAS:528:DC%2BD2cXjsFCiur0%3D (Pubitemid 38681766)
14. H Eikemo MB Brurberg J Davik 2010 Resistance to Phytophthora cactorum in diploid Fragaria species HortScience 45 193 197
15. Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. APS Press, St Paul MN
16. AL Fabritius HS Judelson 2003 A mating-induced protein of Phytophthora infestans is a member of a family of elicitors with divergent structures and stage-specific patterns of expression Mol Plant-Microbe Interact 16 926 935 14558694 10.1094/MPMI.2003.16.10.926 1:CAS:528:DC%2BD3sXnsFyktb0%3D (Pubitemid 37143937)
17. KM Folta TM Davis 2006 Strawberry genes and genomes Crit Rev Plant Sci 25 399 415 10.1080/07352680600824831 1:CAS:528:DC%2BD28Xht1Sqsb7N (Pubitemid 44449278)
18. LJ Grenville-Briggs AO Avrova RJ Hay CR Bruce SC Whisson P van West 2010 Identification of appressorial and mycelial cell wall proteins and a survey of the membrane proteome of Phytophthora infestans Fung Biol 114 702 723 10.1016/j.funbio.2010.06.003 1:CAS:528:DC%2BC3cXhtVymtLnO
19. S Grouffaud P van West AO Avrova PRJ Birch SC Whisson 2008 Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans Microbiology 154 3743 3751 19047742 10.1099/mic.0.2008/021964-0 1:CAS:528:DC%2BD1MXhsVCisQ%3D%3D
20. BJ Haas S Kamoun MC Zody, et al. 2009 Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans Nature 461 393 398 19741609 10.1038/nature08358 1:CAS:528:DC%2BD1MXhtFSnt7vM
21. J Hantula A Lilja P Parikka 1997 Genetic variation and host specificity of Phytophthora cactorum isolated in Europe Mycol Res 101 565 572 10.1017/S0953756296002900 (Pubitemid 28199160)
22. AR Hardham 1992 Cell biology of pathogenesis Ann Rev Plant Phys 43 491 526 10.1146/annurev.pp.43.060192.002423
23. AR Hardham 2001 The cell biology behind Phytophthora pathogenicity Australas Plant Pathol 30 91 98 10.1071/AP01006
24. JC Huet M Mansion JC Pernollet 1993 Amino acid sequence of the α-elicitin secreted by Phytophthora cactorum Phytochemistry 34 1261 1264 7764283 10.1016/0031-9422(91)80012-P 1:CAS:528:DyaK2cXpvFOnsg%3D%3D (Pubitemid 2019308)
25. E Huitema TA Torto A Styer S Kamoun 2003 Combined ESTs from plant-microbe interactions: using GC counting to determine the species of origin Methods Mol Biol 236 79 84 14501059 1:CAS:528:DC%2BD3sXnsVSgsbo%3D
26. RHY Jiang S Tripathy F Govers BM Tyler 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 18344324 10.1073/pnas.0709303105 1:CAS:528:DC%2BD1cXkt12qtb8%3D (Pubitemid 351753839)
27. HS Judelson AMV Ah-Fong G Aux, et al. 2008 Gene expression profiling during asexual development of the late blight pathogen Phytophthora infestans reveals a highly dynamic transcriptome Mol Plant-Microbe Interact 21 433 447 18321189 10.1094/MPMI-21-4-0433 1:CAS:528:DC%2BD1cXjsFOru7o%3D (Pubitemid 351522785)
28. SD Kale B Gu DG Capelluto D Dou E Feldman A Rumore FD Arredondo R Hanlon I Fudal T Rouxel CB Lawrence W Shan BM Tyler 2010 External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells Cell 142 284 295 20655469 10.1016/j.cell.2010.06.008 1:CAS:528:DC%2BC3cXpsVaiu7c%3D
29. S Kamoun 2003 Molecular genetics of pathogenic oomycetes Eukaryot Cell 2 191 199 12684368 10.1128/EC.2.2.191-199.2003 1:CAS:528:DC%2BD3sXjtFSmsLY%3D (Pubitemid 36562358)
30. S Kamoun 2006 A catalogue of the effector secretome of plant pathogenic oomycetes Ann Rev Phytopathol 44 41 60 10.1146/annurev.phyto.44.070505.143436 1:CAS:528:DC%2BD28XhtVylsLnO (Pubitemid 44435697)
31. JY Le Berre G Engler F Panabieres 2008 Exploration of the late stages of the tomato-Phytophthora parasitica interactions through histological analysis and generation of expressed sequence tags New Phytol 177 480 492 18028297 1:CAS:528:DC%2BD1cXhvFGlurk%3D (Pubitemid 350295777)
32. P Liang JD Meade AB Pardee 2007 A protocol for differential display of mRNA expression using either fluorescent or radioactive labeling Nat Protoc 2 457 470 17406608 10.1038/nprot.2007.46 1:CAS:528:DC%2BD2sXhtFGntbjE (Pubitemid 47040008)
33. AM Mayer RC Staples NL Gil-ad 2001 Mechanisms of survival of necrotrophic fungal plant pathogens in hosts expressing the hypersensitive response Phytochemistry 58 33 41 11524110 10.1016/S0031-9422(01)00187-X 1:CAS:528:DC%2BD3MXmt1yjsLs%3D (Pubitemid 32750846)
34. HW Mewes D Frishman U Güldener G Mannhaupt K Mayer M Mokrejs B Morgenstern M Münsterkötter S Rudd B Weil 2002 MIPS: a database for genomes and protein sequences Nucleic Acids Res 30 31 34 11752246 10.1093/nar/30.1.31 1:CAS:528:DC%2BD38Xht12ksbg%3D (Pubitemid 34679496)
35. G Nicastro G Orsomando E Ferrari, et al. 2009 Solution structure of the phytotoxic protein PcF: the first characterized member of the Phytophthora PcF toxin family Protein Sci 18 1786 1791 19554629 10.1002/pro.168 1:CAS:528:DC%2BD1MXpt1Cmur4%3D
36. SK Oh S Kamoun D Choi 2010 Oomycetes RXLR effectors function as both activator and suppressor of plant immunity Plant Pathol J 26 209 215 10.5423/PPJ.2010.26.3.209 1:CAS:528:DC%2BC3cXhtlKgt7rJ
37. G Orsomando M Lorenzi N Raffaelli MD Rizza B Mezzetti S Ruggieri 2001 Phytotoxic protein PcF purification, characterization, and cDNA sequencing of a novel hydroxyproline-containing factor secreted by the strawberry pathogen Phytophthora cactorum J Biol Chem 276 21578 21584 11262411 10.1074/jbc. M101377200 1:CAS:528:DC%2BD3MXksFGksr8%3D
38. G Orsomando M Lorenzi E Ferrari C de Chiara A Spisni S Ruggieri 2003 PcF protein from Phytophthora cactorum and its recombinant homologous elicit phenylalanine ammonia lyase activation in tomato Cell Mol Life Sci 60 1470 1476 12943233 10.1007/s00018-003-3079-7 1:CAS:528:DC%2BD3sXms1WitrY%3D (Pubitemid 36900528)
39. MW Pfaffl 2001 A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res 29 e45 11328886 10.1093/nar/29.9.e45 1:STN:280:DC%2BD38nis12jtw%3D%3D
40. MW Pfaffl GW Horgan L Dempfle 2002 Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR Nucleic Acids Res 30 e36 11972351 10.1093/nar/30.9.e36
41. MW Pfaffl A Tichopad C Prgomet TP Neuvians 2004 Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations Biotechnol Lett 26 509 515 15127793 10.1023/B:BILE.0000019559.84305.47 1:CAS:528:DC%2BD2cXhvF2mtLk%3D (Pubitemid 38448421)
42. D Qutob PT Hraber BW Sobral M Gijzen 2000 Comparative analysis of expressed sequences in Phytophthora sojae Plant Physiol 123 243 254 10806241 10.1104/pp.123.1.243 1:CAS:528:DC%2BD3cXjsFemsrc%3D
43. Y Raftoyannis MW Dick 2006 Zoospore encystment and pathogenicity of Phytophthora and Pythium species on plant roots Microbiol Res 161 1 8 16338584 10.1016/j.micres.2005.04.003 (Pubitemid 41773107)
44. TA Randall RA Dwyer E Huitema, et al. 2005 Large-scale gene discovery in the oomycete Phytophthora infestans reveals likely components of phytopathogenicity shared with true fungi Mol Plant-Microbe Interact 18 229 243 15782637 10.1094/MPMI-18-0229 (Pubitemid 40263618)
45. AP Rehmany A Gordon LE Rose RL Allen MR Armstrong SC Whisson S Kamoun BM Tyler PRJ Birch JL Beynon 2005 Differential recognization of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines Plant Cell 17 1839 1850 15894715 10.1105/tpc.105.031807 1:CAS:528:DC%2BD2MXlsVynsrk%3D
46. B Reinhold-Hurek T Maes S Gemmer MV Montagu T Hurek 2006 An endoglucanase is involved in infection of rice roots by the not-cellulose-metabolizing endophyte Azoarcus sp strain BH72 Mol Plant-Microbe Interact 19 181 188 16529380 10.1094/MPMI-19-0181 1:CAS:528:DC%2BD28XhtVCntLs%3D (Pubitemid 43172832)
47. M Rousseau-Gueutin E Lerceteau-Köhler L Barrot DJ Sargent A Monfort D Simpson P Arus G Guerin B Denoyes-Rothan 2008 Comparative genetic mapping between octoploid and diploid Fragaria species reveals a high level of colinearity between their genomes and the essential disomic behavior of the cultivated octoploid strawberry Genetics 179 2045 2060 18660542 10.1534/genetics.107.083840
48. M Rousseau-Gueutin A Gaston A Ainouche ML Ainouche K Olbricht G Staudt L Richard B Denoyes-Rothan 2009 Tracking the evolutionary history of polyploidy in Fragaria L (strawberry): new insights from phylogenetic analyses of low-copy nuclear genes Mol Phylogenet Evol 51 515 530 19166953 10.1016/j.ympev.2008.12. 024 1:CAS:528:DC%2BD1MXlslajs7s%3D
49. AS Sahai MS Manocha 2006 Chitinases of fungi and plants: their involvement in morphogenesis and host-parasite interaction FEMS Microbiol Rev 11 317 338 10.1111/j.1574-6976.1993.tb00004.x
50. D Sargent TM Davis K Tobutt M Wilkinson N Battey D Simpson 2004 A genetic linkage map of microsatellite gene specific and morphological markers in diploid Fragaria Theor Appl Genet 109 1385 1391 15290052 10.1007/s00122-004- 1767-9 1:CAS:528:DC%2BD2cXhtVahtbfJ (Pubitemid 40059260)
51. A Savidor RS Donahoo O Hurtado-Gonzales ML Land MB Shah KH Lamour WH McDonald 2008 Cross-species global proteomics reveals conserved and unique processes in Phytophthora sojae and Phytophthora ramorum Mol Cell Proteomics 7 1501 1516 18316789 10.1074/mcp.M700431-MCP200 1:CAS:528:DC%2BD1cXhtVSrs7vP
52. S Schornack M van Damme TO Bozkurt LM Cano M Smoker M Thines E Gaulin S Kamoun E Huitema 2010 Ancient class of translocated oomycete effectors targets the host nucleus Proc Natl Acad Sci USA 107 17421 17426 20847293 10.1073/pnas.1008491107 1:CAS:528:DC%2BC3cXht12ltrfF
53. W Shan JS Marshall AR Hardham 2004 Gene expression in germinated cysts of Phytophthora nicotianae Mol Plant Pathol 5 317 330 20565599 10.1111/j.1364-3703.2004.00231.x 1:CAS:528:DC%2BD2cXmsl2nsrg%3D (Pubitemid 38940767)
54. V Shulaev SS Korban B Sosinski, et al. 2008 Multiple models for Rosaceae genomics Plant Physiol 147 985 1003 18487361 10.1104/pp.107.115618 1:CAS:528:DC%2BD1cXoslyisro%3D (Pubitemid 352844258)
55. V Shulaev DJ Sargent RN Crowhurst, et al. 2011 The genome of woodland strawberry (Fragaria vesca) Nat Genet 43 109 116 21186353 10.1038/ng.740 1:CAS:528:DC%2BC3cXhs1WisrnE
56. JP Slovin K Schmitt KM Folta 2009 An inbred line of the diploid strawberry Fragaria vesca f. semperflorens for genomic and molecular genetic studies in the Rosaceae Plant Methods 5 15 19878589 10.1186/1746-4811-5-15
57. MA Torres JDG Jones JL Dangl 2006 Reactive oxygen species signaling in response to pathogens Plant Physiol 141 373 378 16760490 10.1104/pp.106.079467 1:CAS:528:DC%2BD28Xmt1aksbs%3D (Pubitemid 43974530)
58. TA Torto S Li A Styer E Huitema A Testa NAR Gow P van West S Kamoun 2003 EST mining and functional expression assays identify extracellular effector proteins from Phytophthora Genome Res 13 675 685 10.1101/gr.910003 (Pubitemid 36874485)
59. TA Torto-Alalibo S Tripathy BM Smith, et al. 2007 Expressed sequence tags from Phytophthora sojae reveal genes specific to development and infection Mol Plant-Microbe Interact 20 781 793 17601166 10.1094/MPMI-20-7-0781 (Pubitemid 46944972)
60. BM Tyler S Tripathy X Zhang, et al. 2006 Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis Science 313 1261 1266 16946064 10.1126/science.1128796 1:CAS:528:DC%2BD28XoslOnur8%3D (Pubitemid 44330944)
61. Z Wang Y Wang X Chen G Shen Z Zhang X Zheng 2006 Differential screening reveals genes differentially expressed in low- and high-virulence near-isogenic Phytophthora sojae lines Fung Genet Biol 43 826 839 10.1016/j.fgb.2006.06.001 1:CAS:528:DC%2BD28Xht1SgsL7I (Pubitemid 46107297)
62. SC Whisson PC Boevink L Moleleki, et al. 2007 A translocation signal for delivery of oomycete effector proteins inside host plant cells Nature 450 115 118 17914356 10.1038/nature06203 1:CAS:528:DC%2BD2sXht1CgtbbJ (Pubitemid 350070562)
63. J Win W Morgan J Bos KV Krasileva LM Cano A Chaparro-Garcia R Ammar BJ Staskawicz S Kamoun 2007 Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes Plant Cell 19 2349 2369 17675403 10.1105/tpc.107.051037 1:CAS:528:DC%2BD2sXhtFyisbjN (Pubitemid 47583830)
64. HZ Yan RF Liou 2006 Selection of internal control genes for real-time quantitative RT-PCR assays in the oomycete plant pathogen Phytophthora parasitica Fungal Genet Biol 43 430 438 16531084 10.1016/j.fgb.2006.01.010 1:CAS:528:DC%2BD28Xks1WrsbY%3D (Pubitemid 43668998)