A novel non-protein-coding infection-specific gene family is clustered throughout the genome of Phytophthora infestans

Microbiology

Volumn 153, Issue 3, 2007, Pages 747-759

  Avrova, Anna O ^a   Whisson, Stephen C ^a   Pritchard, Leighton ^a   Venter, Eduard ^a,b   De Luca, Sergio ^a   Hein, Ingo ^a   Birch, Paul R J ^a  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF JOHANNESBURG   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA; FUNGAL PROTEIN; PROTEIN PINCI 1; UNCLASSIFIED DRUG;

ARTICLE; BIOLOGY; FUNGUS IDENTIFICATION; GENE EXPRESSION; GENE SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYTOPHTHORA INFESTANS; PLANT DISEASE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; UPREGULATION;

BASE SEQUENCE; DNA, ALGAL; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENOME; MOLECULAR SEQUENCE DATA; PHYTOPHTHORA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, ALGAL; RNA, UNTRANSLATED; SOLANUM TUBEROSUM;

BACTERIA (MICROORGANISMS); PHYTOPHTHORA INFESTANS; SOLANUM TUBEROSUM;

EID: 33947387973     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2006/002220-0     Document Type: Article

References (60)

1. Ah Fong, A. M. V. & Judelson, H. S. (2004). The hAT-like DNA transposon DodoPi resides in a cluster of retro- and DNA transposons in the stramenopile Phytophthora infestans. Mol Genet Genom 271, 577-585.
2. Andersen, A. A. & Panning, B. (2003). Epigenetic gene regulation by noncoding RNAs. Curr Opin Cell Biol 15, 281-289.
3. Armstrong, M. R., Whisson, S. C., Pritchard, L., Bos, J. I. B, Venter, E., Avrova, A. O., Rehmany, A. P., Böhme, U., Brooks, K. & other authors (2005). An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognised in the host cytoplasm. Proc Natl Acad Sci U S A 102, 7766-7771.
4. Avrova, A. O., Stewart, H. E., De Jong, W., Heilbronn, J., Lyon, G. D. & Birch, P. R. J. (1999). A cysteine protease gene is expressed early in resistant potato interactions with Phytophthora infestans. Mol Plant Microbe Interact 12, 1114-1119.
5. Avrova, A. O., Venter, E., Birch, P. R. J. & Whisson, S. C. (2003). Profiling and quantifying differential gene transcription in Phytophthora infestans prior to and during the early stages of potato infection. Fungal Genet Biol 40, 4-14.
6. Avrova, A. O., Taleb, N., Rokka, V. M., Heilbronn, J., Hein, I., Gilroy, E. M., Cardle, L., Stewart H. S., Loake, G. & other authors (2004). Potato oxysterol binding protein and cathepsin B are rapidly upregulated in independent defence pathways that distinguish R gene-mediated and field resistances to Phytophthora infestans. Mol Plant Pathol 5, 45-56.
7. Baldauf, S. L. (2003). The deep roots of eukaryotes. Science 300, 1703-1706.
8. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
9. Bell, K. S., Avrova, A. O., Holeva, M. C., Cardle, L., Morris, W., De Jong, W., Toth, I. K., Waugh, R., Bryan, G. J. & Birch, P. R. J. (2002). Sample sequencing of a selected region of the genome of Erwinia carotovora subsp. atroseptica reveals candidate phytopathogenicity genes and allows comparison with Escherichia coli. Microbiology 148, 1367-1378.
10. Bendtsen, J. D., Nielsen, H., von Heijne, G. & Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340, 783-795.
11. Beyer, K., Binder, A., Boller, T. & Collinge, M. (2001). Identification of potato genes induced during colonization by Phytophthora infestans. Mol Plant Pathol 2, 125-135.
12. Beyer, K., Jimenez Jimenez, S., Randall, T. A., Lam, S., Binder, A., Boller, T. & Collinge, M. (2002). Characterisation of Phytophthora infestans genes regulated during the interaction with potato. Mol Plant Pathol 3, 473-485.
13. Bhattacharjee, S., Hiller, N. L., Liolios, K., Win, J., Kanneganti, T.-D., Young, C., Kamoun, S. & Haldar, K. (2006). The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog 2, e50. doi:10.1371/journal.ppat.0020050.
14. Birch, P. R. J. & Whisson, S. C. (2001). Phytophthora infestans enters the genomics era. Mol Plant Pathol 2, 257-263.
15. Birch, P. R. J., Avrova, A. O., Duncan, J. M., Lyon, G. D. & Toth, R. L. (1999). Isolation of potato genes that are induced during an early stage of the hypersensitive response to Phytophthora infestans. Mol Plant Microbe Interact 12, 356-361.
16. Birch, P. R. J., Avrova, A. O., Armstrong, M., Venter, E., Taleb, N., Gilroy, E. M., Phillips, M. S. & Whisson, S. C. (2003). The potato-Phytophthora infestans interaction transcriptome. Can J Plant Pathol 25, 226-231.
17. Birch, P. R. J., Rehmany, A. P., Pritchard, L., Kamoun, S., Beynon, J. L. (2006). Trafficking arms: Oomycete effectors enter host plant cells. Trends Microbiol 14, 8-11.
18. Bittner-Eddy, P. D., Allen, R. L., Rehmany, A. P., Birch, P. R. J. & Beynon, J. L. (2003). Use of suppression subtractive hybridization to identify downy mildew genes expressed during infection of Arabidopsis thaliana. Mol Plant Pathol 4, 501-508.
19. Blanco, F. A. & Judelson, H. S. (2005). A bZIP transcription factor from Phytophthora interacts with a protein kinase and is required for zoospore motility and plant infection. Mol Microbiol 56, 638-648.
20. Cawley, S., Bekiranov, S., Ng, S. S., Kapranov, P., Sekinger, E. A., Kampa, D., Piccolboni, A., Sementchenko, V., Cheng, J. & other authors (2004). Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 116, 499-509.
21. Cheng, J., Kapranov, P., Drenkow, J., Dike, S., Brubaker, S., Patel, S., Long, J., Stern, D., Tammana, H. & other authors (2005). Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 308, 1149-1154.
22. Claverie, J. M. (2005). Fewer genes, more noncoding RNA. Science 309, 1529-1530.
23. Cook, P. R. (2003). Nongenic transcription, gene regulation and action at a distance. J Cell Sci 116, 4483-4491.
24. Cvitanich, C. & Judelson, H. S. (2003). Stable transformation of the oomycete, Phytophthora infestans, using microprojectile bombardment. Curr Genet 42, 228-235.
25. Dekker, J., Rippe, K., Dekker, M. & Kleckner, N. (2002). Capturing chromosome conformation. Science 295, 1306-1311.
26. Duncan, J. M. (1999). Phytophthora - an abiding threat to our crops. Microbiol Today 26, 114-116.
27. Fickett, J. W. (1982). Recognition of protein coding regions in DNA sequences. Nucleic Acids Res 10, 5303-5318.
28. Goodrich, J. A. & Kugel, J. F. (2006). Non-coding-RNA regulators of RNA polymerase II transcription. Nat Rev Mol Cell Biol 7, 612-616.
29. Grenville-Briggs, L. J., Avrova, A. O., Bruce, C. R., Williams, A., Whisson, S. C., Birch, P. R. J. & van West, P. (2005). Elevated amino acid biosynthesis in Phytophthora infestans during appressorium formation and potato infection. Fungal Genet Biol 42, 244-256.
30. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 95-98.
31. Hirsch, J., Lefort, V., Vankersschaver, M., Boualem, A., Lucas, A., Thermes, C., d'Aubenton-Carafa, Y. & Crespi, M. (2006). Characterization of 43 non-protein-coding mRNA genes in Arabidopsis, including the MIR162a-derived transcripts. Plant Physiol 140, 1192-1204.
32. Hopp, T. P., Prickett, K. S., Price, V. L., Libby, R. T., March, C. J., Cerretti, D. P., Urdal, D. L. & Conlon, P. J. (1988). A short polypeptide marker sequence useful for recombinant protein identification and purification. Bio/Technology 6, 1204-1210.
33. Huang, X. & Madan, A. (1999). CAP3: a DNA sequence assembly program. Genome Research 9, 868-877.
34. Jiang, R. H., Dawe, A. L., Weide, R., van Staveren, M., Peters, S., Nuss, D. L. & Govers, F. (2005). Elicitin genes in Phytophthora infestans are clustered and interspersed with various transposon-like elements. Mol Genet Genom 273, 20-32.
35. Judelson, H. S. (2002). Sequence variation and genomic amplification of a family of Gypsy-like elements in the oomycete genus Phytophthora. Mol Biol Evol 19, 1313-1322.
36. Judelson, H. S. & Randall, T. A. (1998). Families of repeated DNA in the oomycete Phytophthora infestans and their distribution within the genus. Genome 41, 605-615.
37. Kamoun, S. (2003). Molecular genetics of pathogenic oomycetes. Eukaryot Cell 2, 191-199.
38. Kamoun, S. (2006). A Catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44, 41-60.
39. Latijnhouwers, M., Ligterink, W., Vleeshouwers, V. G. A. A., Van West, P. & Covers, F. (2004). A Gα subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans. Mol Microbiol 51, 925-936.
40. Ling, J., Baibakov, B., Pi, W., Emerson, B. M. & Tuan, D. (2005). The HS2 enhancer of the β-globin locus control region initiates synthesis of non-coding, polyadenylated RNAs independent of a cis-linked globin promoter. J Mol Biol 350, 883-896.
41. Llave, C., Kasschau, K. D., Rector, M. A. & Carrington, J. C. (2002). Endogenous and silencing-associated small RNAs in plants. Plant Cell 14, 1605-1619.
42. Mallory, A. C. & Vaucheret, H. (2006). Functions of microRNAs and related small RNAs in plants. Nat Genet 38, Suppl. S31-S36.
43. Mattick, J. S. (2003). Challenging the dogma: the hidden layers of non-protein-coding RNAs in complex organisms. BioEssays 25, 930-939.
44. Morey, C. & Avner, P. (2004). Employment opportunities for non-coding RNAs. FEBS Lett 567, 27-34.
45. Okazaki, Y., Furuno, M., Kasukawa, T., Adachi, J., Bono, H., Kondo, S., Nikaido, I., Osato, N., Saito, R. & other authors (2002). Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420, 563-573.
46. Ota, T., Suzuki, Y., Nishikawa, T., Otsuki, T., Sugiyama, T., Irie, R., Wakamatsu, A., Hayashi, K., Sato, H. & other authors (2004). Complete sequencing and characterization of 21243 full-length human cDNAs. Nat Genet 36, 40-45.
47. Pollard, K. S., Salama, S. R., Lambert, N., Lambot, M.-A., Coppens, S., Pedersen, J., Katzman, S., King, B., Onodera, C. & other authors (2006). An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443, 167-172.
48. Pritchard, L., White, J. A., Birch, P. R. J. & Toth, I. K. (2006). GenomeDiagram: a Python package for the visualisation of large-scale genomic data. Bioinformatics 22, 616-617.
49. Randall, T. A., Dwyer, R. A., Huitema, E., Beyer, K., Cvitanich, C., Kelkar, H., Ah Fong, A., Gates, K., Roberts, S. & other authors (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.
50. Rehmany, A. P., Gordon, A., Rose, L. E., Allen, R. L., Armstrong, M. R., Whisson, S. C., Kamoun, S., Tyler, B.M., Birch, P. R. J. & Beynon, J. L. (2005). Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17, 1839-1850.
51. Saha, S., Murthy, S. & Rangarajan, P. N. (2006). Identification and characterization of a virus-inducible non-coding RNA in mouse brain. J Gen Virol 87, 1991-1995.
52. Srikantan, V., Zou, Z., Petrovics, G., Zu, L., Augustus, M., Davis, L., Livezey, J. R., Connell, T., Sesterhenn, I. A. & other authors (2000). PCGEM1, a prostate-specific gene, is overexpressed in prostate cancer. Proc Natl Acad Sci U S A 97, 12216-12221.
53. Tooley, P. W. & Garfinkel, D. G. (1996). Presence of Ty1-copia group retrotransposon sequences in the potato late blight pathogen Phytophthora infestans. Mol Plant Microbe Interact 9, 305-309.
54. Torto, T. A., Li, S., Styer, A., Huitema, E., Testa, A., Gow, N. A., van West, P. & Kamoun, S. (2003). EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Res 13, 1675-1685.
55. van West, P., de Jong, A. J., Judelson, H. S., Emons, A. M. C. & Govers, F. (1998). The ipiO gene of Phytophthora infestans is highly expressed in invading hyphae during infection. Fungal Genet Biol 23, 126-138.
56. Vleeshouwers, V. G., van Dooijeweert, W., Govers, F., Kamoun, S. & Colon, L. T. (2000). The hypersensitive response is associated with host and nonhost resistance to Phytophthora infestans. Planta 210, 853-864.
57. Wassenegger, M. (2000). RNA-directed DNA methylation. Plant Mol Biol 43, 203-220.
58. Whisson, S. C., van der Lee, T., Bryan, G., Waugh, R., Govers, F. & Birch, P. R. J. (2001). Physical mapping across an avirulence locus of Phytophthora infestans using a highly representative, large-insert bacterial artificial chromosome library. Mol Genet Genomics 266, 289-295.
59. Whisson, S. C., Avrova, A. O., Lavrova, O. & Pritchard, L. (2005). Families of short interspersed elements in the genome of the oomycete plant pathogen, Phytophthora infestans. Fungal Genet Biol 4, 351-365.
60. Zhang, B., Pan, X., Cobb, G. P. & Anderson, T. A. (2006). Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289, 3-16.