RNA-Seq Reveals Infection-Related Gene Expression Changes in Phytophthora capsici

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Chen, Xiao Ren ^a   Xing, Yu Ping ^a   Li, Yan Peng ^a   Tong, Yun Hui ^a   Xu, Jing You ^a  

^a YANGZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL DEATH; CONTROLLED STUDY; CRN GENE; CYST (RESTING STAGE); DNA LIBRARY; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; MYCELIUM; NICOTIANA BENTHAMIANA; NLP GENE; NONHUMAN; PATHOGENICITY; PHYTOPHTHORA CAPSICI; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; RXLR GENE; ZOOSPORE; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; MOLECULAR GENETICS; PHYTOPHTHORA; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

COMPLEMENTARY DNA; FUNGAL PROTEIN;

AMINO ACID SEQUENCE; DNA, COMPLEMENTARY; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; MOLECULAR SEQUENCE DATA; PHYTOPHTHORA; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, RNA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84883357008     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074588     Document Type: Article

References (79)

1. Erwin DC, Ribeiro OK (1996) Phytophthora Diseases Worldwide. St Paul MN: APS Press. 562 p.
2. Fry W, (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9: 385-402.
3. Rizzo DM, Garbelotto M, Hansen EM, (2005) Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annu Rev Phytopathol 43: 309-335.
4. Bouwmeester K, van Poppel PMJA, Govers F (2009) Genome biology cracks enigmas of oomycete plant pathogens. In: Parker JE, editor. Molecular aspects of plant disease resistance. Oxford: Wiley-Blackwell. pp. 102-133.
5. Hardham AR, (2007) Cell biology of plant-oomycete interactions. Cell Microbiol 9: 31-39.
6. Shan W, Marshall JS, Hardham AR, (2004) Gene expression in germinated cysts of Phytophthora nicotianae. Mol Plant Pathol 5: 317-330.
7. Judelson HS, Ah-Fong AM, Aux G, Avrova AO, Bruce C, 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.
8. Savidor A, Donahoo RS, Hurtado-Gonzales O, Land ML, Shah MB, et al. (2008) Cross-species global proteomics reveals conserved and unique processes in Phytophthora sojae and Phytophthora ramorum. Mol Cell Proteomics 7: 1501-1516.
9. Chen X, Klemsdal SS, Brurberg MB, (2011) Identification and analysis of Phytophthora cactorum genes up-regulated during cyst germination and strawberry infection. Curr Genet 57: 297-315.
10. Gevens AJ, Roberts PD, McGover RJ, Kucharek TA (2004) Vegetable diseases caused by Phytophthora capsici in Florida. University of Florida IFAS Extension. Available: http://edis.ifas.ufl.edu/pdffiles/VH/VH04500.pdf. Accessed 30 July 2013.
11. Gevens AJ, Donahoo RS, Lamour KH, Hausbeck MK, (2008) Characterization of Phytophthora capsici causing foliar and pod blight of snap bean in Michigan. Plant Dis 92: 201-209.
12. Ho HH, (1990) Taiwan Phytophthora. Bot Bull Acad Sinica 31: 89-106.
13. Babadoost M, Tian D, Islam SZ, Pavon C (2008) Challenges and options in managing Phytophthora blight (Phytophthora capsici) of cucurbits. In: Pitrat M, editor. Cucurbitaceae 2008, Proceedings of the IXth EUCARPIA meeting on genetics and breeding of Cucurbitaceae. Avignon (France), May 21-24th, 2008. pp. 399-406.
14. Lamour KH, Stam R, Jupe J, Huitema E, (2012) The oomycete broad-host-range pathogen Phytophthora capsici. Mol Plant Pathol 13: 329-337.
15. Wang Y, Bouwmeester K, van de Mortel JE, Shan W, Govers F, (2013) A novel Arabidopsis-oomycete pathosystem: differential interactions with Phytophthora capsici reveal a role for camalexin, indole glucosinolates and salicylic acid in defence. Plant Cell Environ 36: 1192-1203.
16. Kamoun S, (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44: 41-60.
17. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY, et al. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261-1266.
18. Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393-398.
19. Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, et al. (2010) Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549-1551.
20. Lévesque CA, Brouwer H, Cano L, Hamilton JP, Holt C, et al. (2010) Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11: R73.
21. Bozkurt TO, Schornack S, Banfield MJ, Kamoun S, (2012) Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol 15: 483-492.
22. Orsomando G, Lorenzi M, Raffaelli N, Dalla Rizza M, Mezzetti B, et al. (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.
23. Gijzen M, Nurnberger T, (2006) Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochem 67: 1800-1807.
24. Ottmann C, Luberacki B, Kufner I, Koch W, Brunner F, et al. (2009) A common toxin fold mediates microbial attack and plant defense. Proc Natl Acad Sci USA 106: 10359-10364.
25. Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, et al. (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17: 1839-1850.
26. Birch PR, Rehmany AP, Pritchard L, Kamoun S, Beynon JL, (2006) Trafficking arms: oomycete effectors enter host plant cells. Trends Microbiol 14: 8-11.
27. Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, et al. (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20: 1930-1947.
28. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, et al. (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142: 284-295.
29. Kelley BS, Lee S, Damasceno CMB, Chakravarthy S, Kim B, et al. (2010) A secreted effector protein (SNE1) from Phytophthora infestans is a broadly acting suppressor of programmed cell death. Plant J 62: 357-366.
30. Bailey K, Cevik V, Holton NJ, Byrne-Richardson J, Sohn KH, et al. (2011) Molecular cloning of ATR5(Emoy2) from Hyaloperonospora arabidopsidis, an avirulence determinant that triggers RPP5-mediated defense in Arabidopsis. Mol Plant-Microbe Interact 24: 827-838.
31. Tian M, Win J, Savory E, Burkhardt A, Held M, et al. (2011) 454 genome sequencing of Pseudoperonospora cubensis reveals effector proteins with a putative QXLR translocation motif. Mol Plant-Microbe Interact 24: 543-553.
32. Bos JIB, Kanneganti TD, Young C, Cakir C, Huitema E, et al. (2006) The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J 48: 165-176.
33. Van Poppel PM, Jiang RHY, Sliwka J, Govers F, (2009) Recognition of Phytophthora infestans Avr4 by potato R4 is triggered by C-terminal domains comprising W motifs. Mol Plant Pathol 10: 611-620.
34. Torto TA, Li S, Styer 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.
35. Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M, et al. (2010) Ancient class of translocated oomycete effectors targets the host nucleus. Proc Natl Acad Sci USA 107: 17421-17426.
36. Stam R, Jupe J, Howden AJM, Morris JA, Boevink PC, et al. (2013) Identification and characterisation CRN Effectors in Phytophthora capsici shows modularity and functional diversity. PLoS ONE 8: e59517.
37. Liu T, Ye W, Ru Y, Yang X, Gu B, et al. (2011) Two host cytoplasmic effectors are required for pathogenesis of Phytophthora sojae by suppression of host defenses. Plant Physiol 155: 490-501.
38. van Damme M, Bozkurt TO, Cakir C, Schornack S, Sklenar J, et al. (2012) The Irish potato famine pathogen Phytophthora infestans translocates the CRN8 kinase into host plant cells. PLoS Pathog 8: e1002875.
39. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW, (1995) Serial analysis of gene expression. Science 270: 484-487.
40. Schena M, Shalon D, Davis RW, Brown PO, (1995) Quantitative monitoring of gene-expression patterns with a complementary DNA microarray. Science 270: 467-470.
41. Lockhart DJ, Dong H, Byrne MC, Follettie MT, Gallo MV, et al. (1996) Expression monitoring by hybridization to highdensity oligonucleotide arrays. Nat Biotechnol 14: 1675-1680.
42. Boguski MS, Tolstoshev CM, Bassett DE, (1994) Gene discovery in dbEST. Science 265: 1993-1994.
43. Asmann YW, Wallace B, Thompson EA, (2008) Transcriptome profiling using next-generation sequencing. Gastroenterology 135: 1466-1468.
44. Mardis ER, (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24: 133-141.
45. Randall TA, Dwyer RA, Huitema E, Beyer K, Cvitanich C, 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.
46. Araki F, Miyagi Y, (1977) Effects of fungicides on penetration by Pyricularia oryzae as evaluated by an improved cellophane method. J Pestic Sci 2: 457-461.
47. Winnepenninckx B, Backeljau T, de Wachter R, (1996) Investigation of molluscan phylogeny on the basis of 18S rRNA sequences. Mol Biol Evol 13: 1306-1313.
48. Kent WJ, (2002) BLAT--the BLAST-like alignment tool. Genome Res 12: 656-664.
49. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
50. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M, (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: W182-185.
51. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
52. Romualdi C, Bortoluzzi S, D'Alessi F, Danieli GA, (2003) IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiol Genomics 12: 159-162.
53. Benjamini Y, Yekutieli D, (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29: 1165-1188.
54. Yan HZ, Liou RF, (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.
55. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
56. Jones L, Hamilton AJ, Voinnet O, Thomas CL, Maule AJ, et al. (1999) RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell 11: 2291-2301.
57. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
58. Lacomme C, Santa Cruz S, (1999) Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc Natl Acad Sci USA 96: 7956-7961.
59. Wang Q, Han C, Ferreira AO, Yu X, Ye W, et al. (2011) Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 23: 2064-2086.
60. Yu X, Tang J, Wang Q, Ye W, Tao K, et al. (2012) The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol 196: 247-260.
61. Qutob D, Kamoun S, Gijzen M, (2002) Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J 32: 361-373.
62. Armstrong MR, Whisson SC, Pritchard L, Bos JI, Venter E, et al. (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.
63. Hogenhout SA, Van der Hoorn RAL, Terauchi R, Kamoun S, (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant-Microbe Interact 22: 115-122.
64. Blair JE, Coffey MD, Park S-Y, Geiser DM, Kang S, (2008) A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genet Biol 45: 266-277.
65. Fellbrich G, Romanski A, Varet A, Blume B, Brunner F, et al. (2002) NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J 32: 375-390.
66. Dou D, Kale SD, Wang X, Chen Y, Wang Q, et al. (2008) Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20: 1118-1133.
67. Dong S, Kong G, Qutob D, Yu X, Tang J, et al. (2012) The NLP toxin family in Phytophthora sojae includes rapidly evolving groups that lack necrosis-inducing activity. Mol Plant-Microbe Interact 25: 896-909.
68. Kunjeti SG, Evans TA, Marsh AG, Gregory NF, Kunjeti S, et al. (2012) RNA-Seq reveals infection-related global gene changes in Phytophthora phaseoli, the causal agent of lima bean downy mildew. Mol Plant Pathol 13: 454-466.
69. Abramovitch RB, Kim YJ, Chen S, Dickman MB, Martin GB, (2003) Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J 22: 60-69.
70. Lamour KH, Mudge J, Gobena D, Hurtado-Gonzales OP, Schmutz J, et al. (2012) Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Mol Plant-Microbe Interact 25: 1350-1360.
71. Ye W, Wang X, Tao K, Lu Y, Dai T, et al. (2011) Digital gene expression profiling of the Phytophthora sojae transcriptome. Mol Plant-Microbe Interact 24: 1530-1539.
72. Shan 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 gene Rps1b. Mol Plant-Microbe Interact 17: 394-403.
73. Qutob D, Tedman-Jones J, Dong S, Kuflu K, Pham H, et al. (2009) Copy number variation and transcriptional polymorphisms of Phytophthora sojae RXLR effector genes Avr1a and Avr3a. PLoS ONE 4: e5066.
74. Grabbe C, Dikic I, (2009) Functional roles of ubiquitin-like domain (ULD) and ubiquitin-binding domain (UBD) containing proteins. Chem Rev 109: 1481-1494.
75. Clem RJ, (2007) Baculoviruses and apoptosis: a diversity of genes and responses. Curr Drug Targets 8: 1069-1074.
76. Tyler BM, (2009) Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell Microbiol 11: 13-20.
77. Feng BZ, Li PQ, Fu L, Sun BB, Zhang XG, (2011) Methodology identification of 18 genes encoding necrosis-inducing proteins from the plant pathogen Phytophthora capsici (Pythiaceae: Oomycetes). Genet Mol Res 10: 910-922.
78. Yousef LF, Yousef AF, Mymryk JS, Dick WA, Dick RP, (2009) Stigmasterol and cholesterol regulate the expression of elicitin genes in Phytophthora sojae. J Chem Ecol 35: 824-832.
79. Forbes BA, Sahm DF, Weissfeld AS (2002) Bailey & Scott's diagnostic microbiology. St LouisMO: Mosby. 789 p.