The transcriptome of compatible and incompatible interactions of potato (Solanum tuberosum) with Phytophthora infestans revealed by DeepSAGE analysis

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Gyetvai, Gabor ^a   Sønderkær, Mads ^b   Göbel, Ulrike ^a   Basekow, Rico ^c   Ballvora, Agim ^a   Imhoff, Maren ^c   Kersten, Birgit ^c   Nielsen, Kåre Lehman ^b   Gebhardt, Christiane ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b AALBORG UNIVERSITY   (Denmark)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

ARTICLE; BASE PAIRING; CARBON DIOXIDE FIXATION; COMPARATIVE STUDY; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE IDENTIFICATION; GENETIC DIFFERENCE; GENETIC TRANSCRIPTION; GENOTYPE; HOST PATHOGEN INTERACTION; INFECTION; MULTIGENE FAMILY; NEAR ISOGENIC LINE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; PHYTOPHTHORA INFESTANS; PLANT DEFENSE; PLANT DISEASE; POTATO; R1 RESISTANCE GENE; SEQUENCE TAGGED SITE; SERIAL ANALYSIS OF GENE EXPRESSION; TRANSGENE; UNINDEXED SEQUENCE; GENETICS; MICROBIOLOGY; PARASITOLOGY; PATHOGENICITY;

PHYTOPHTHORA INFESTANS; SOLANUM TUBEROSUM;

PHYTOPHTHORA INFESTANS; PLANT DISEASES; SOLANUM TUBEROSUM; TRANSCRIPTOME;

EID: 84856650192     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031526     Document Type: Article

References (72)

1. Fry W, (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9: 385-402.
2. Ross H, (1986) Potato breeding- problems and perspectives; In: Horn WaR G, editors. Berlin and Hamburg Paul Parey.
3. Van der Vossen E, Sikkema A, Hekkert BtL, Gros J, Stevens P, et al. (2003) An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J 36: 867-882.
4. Song J, Bradeen JM, Naess SK, Raasch JA, Wielgus SM, 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.
5. Huang S, van der Vossen EAG, Kuang H, Vleeshouwers VGAA, Zhang N, et al. (2005) Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J 42: 251-261.
6. Ballvora A, Ercolano MR, Weiss J, Meksem K, Bormann CA, et al. (2002) The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J 30: 361-371.
7. Foster SJ, Park T-H, Pel M, Brigneti G, Åšliwka J, et al. (2009) Rpi-vnt1.1, a Tm-22 homolog from Solanum venturii, confers resistance to potato late blight. Mol Plant-Microbe Interact 22: 589-600.
8. Vleeshouwers VGAA, Rietman H, Krenek P, Champouret N, Young C, et al. (2008) Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes. PLoS ONE 3: e2875.
9. van der Vossen EAG, Gros J, Sikkema A, Muskens M, Wouters D, et al. (2005) The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J 44: 208-222.
10. van Poppel PMJA, Guo J, van de Vondervoort PJI, Jung MWM, Birch PRJ, et al. (2008) The Phytophthora infestans avirulence gene Avr4 encodes an RXLR-dEER effector. Mol Plant-Microbe Interact 21: 1460-1470.
11. Armstrong MR, Whisson SC, Pritchard L, Bos JIB, 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.
12. Lokossou AA, Park T-h, van Arkel G, Arens M, Ruyter-Spira C, et al. (2009) Exploiting knowledge of R/Avr genes to rapidly clone a new LZ-NBS-LRR family of late blight resistance genes from potato linkage group IV. Mol Plant-Microbe Interact 22: 630-641.
13. Pan Q, Wendel J, Fluhr R, (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evolution 50: 203-213.
14. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ, (2009) Shades of gray: the world of quantitative disease resistance. Trends in Plant Science 14: 21-29.
15. Stewart HE, Bradshaw JE, Pande B, (2003) The effect of the presence of R-genes for resistance to late blight (Phytophthora infestans) of potato (Solanum tuberosum) on the underlying level of field resistance. Plant Pathol 52: 193-198.
16. Leonards-Schippers C, Gieffers W, Schafer-Pregl R, Ritter E, Knapp SJ, et al. (1994) Quantitative resistance to Phytophthora infestans in potato: a case study for QTL mapping in an allogamous plant species. Genetics 137: 67-77.
17. Gebhardt C, Valkonen JP, (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39: 79-102.
18. Pajerowska-Mukhtar K, Stich B, Achenbach U, Ballvora A, Lübeck J, et al. (2009) Single nucleotide polymorphisms in the Allene Oxide Synthase 2 gene are associated with field resistance to late blight in populations of tetraploid potato cultivars. Genetics 181: 1115-1127.
19. Pajerowska-Mukhtar KM, Mukhtar MS, Guex N, Halim VA, Rosahl S, et al. (2008) Natural variation of potato allene oxide synthase 2 causes differential levels of jasmonates and pathogen resistance in Arabidopsis. Planta 228: 293-306.
20. Trognitz F, Manosalva P, Gysin R, Nino-Liu D, Simon R, et al. (2002) Plant defense genes associated with quantitative resistance to potato late blight in Solanum phureja x dihaploid S. tuberosum hybrids. Mol Plant Microbe Interact 15: 587-597.
21. Hoegen E, Stromberg A, Pihlgren U, Kombrink E, (2002) Primary structure and tissue-specific expression of the pathogenesis-related protein PR-1b in potato. Mol Plant Pathol 3: 329-345.
22. Taylor J, Fritzemeier K-H, Häuser I, Kombrink E, Rohwer F, et al. (1990) Structural analysis and activation by fungal infection of a gene encoding a pathogenesis-related protein in potato. Mol Plant-Microbe Interact 3: 72-77.
23. Constabel CP, Brisson N, (1992) The defense-related STH-2 gene product of potato shows race-specific accumulation after inoculation with low concentrations of Phytophthora infestans zoospores. Planta 188: 289-295.
24. Fritzemeier K-H, Cretin C, Kombrink E, Rohwer F, Taylor J, et al. (1987) Transient induction of phenylalanine ammonia-lyase and 4-coumarate: CoA ligase mRNAs in potato leaves infected with virulent or avirulent races of Phytophthora infestans. Plant Physiol 85: 34-41.
25. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, 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.
26. Beyer K, Binder A, Boller T, Collinge M, (2001) Identification of potato genes induced during colonization by Phytophthora infestans. Mol Plant Pathol 2: 125-134.
27. Birch PRJ, Avrova AO, Duncan JM, Lyon GD, Toth RL, (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.
28. Henriquez MA, Daayf F, (2010) Identification and cloning of differentially expressed genes involved in the interaction between potato and Phytophthora infestans using a subtractive hybridization and cDNA-AFLP combinational approach. J Integrative Plant Biol 52: 453-467.
29. Ros B, Thümmler F, Wenzel G, (2004) Analysis of differentially expressed genes in a susceptible and moderately resistant potato cultivar upon Phytophthora infestans infection. Mol Plant Pathol 5: 191-201.
30. Wan J, Dunning M, Bent A, (2002) Probing plant-pathogen interactions and downstream defense signaling using DNA microarrays. Functional & Integrative Genomics 2: 259-273.
31. Lindqvist-Kreuze H, Carbajulca D, Gonzalez-Escobedo G, Perez W, Bonierbale M, (2010) Comparison of transcript profiles in late blight-challenged Solanum cajamarquense and B3C1 potato clones. Mol Plant Pathol 11: 513-530.
32. Restrepo S, Myers KL, del Pozo O, Martin GB, Hart AL, et al. (2005) Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase. Mol Plant-Microbe Interact 18: 913-922.
33. Wang B, Liu J, Tian Z, Song B, Xie C, (2005) Monitoring the expression patterns of potato genes associated with quantitative resistance to late blight during Phytophthora infestans infection using cDNA microarrays. Plant Science 169: 1155-1167.
34. Mardis ER, (2008) The impact of next-generation sequencing technology on genetics. Trends in Genetics 24: 133-141.
35. Velculescu VE, Zhang L, Vogelstein B, Kinzler K, (1995) Serial analysis of gene expression. Science 270: 484-487.
36. Nielsen KL, Hogh AL, Emmersen J, (2006) DeepSAGE-digital transcriptomics with high sensitivity, simple experimental protocol and multiplexing of samples. Nucl Acids Res 34: e133.
37. 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.
38. van Loon LC, Rep M, Pieterse CMJ, (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44: 135-162.
39. Liu F, Lu J, Hu W, Wang S-Y, Cui S-J, et al. (2006) New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathog 2: e29.
40. Heibges A, Glaczinski H, Ballvora A, Salamini F, Gebhardt C, (2003) Structural diversity and organization of three gene families for Kunitz-type enzyme inhibitors from potato tubers (Solanum tuberosum L.). Mol Genet Genomics 269: 526-534.
41. Schaaf GJ, van Ruissen F, va Kampen A, Kool M, Ruijter JM, (2008) Statistical comparison of two or more SAGE libraries: one tag at a time. Methods Mol Biol 387: 151-168.
42. Beissbarth T, Hyde L, Smyth GK, Job C, Boon W-M, et al. (2004) Statistical modeling of sequencing errors in SAGE libraries. Bioinformatics 20: i31-i39.
43. Hardcastle T, Kelly K, (2010) baySeq: Empirical Bayesian methods for identifying differential expression in sequence count data. BMC Bioinformatics 11: 422.
44. Wang L, Feng Z, Wang X, Wang X, Zhang X, (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136-138.
45. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biology 11: R106.
46. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
47. PGSC (2011) Genome sequence and analysis of the tuber crop potato. Nature 475: 189-195.
48. Mangeon A, Junqueira RM, Sachetto-Martins G, (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav 5: 99-104.
49. Vlot AC, Klessig DF, Park S-W, (2008) Systemic acquired resistance: the elusive signal(s). Current Op Plant Biol 11: 436-442.
50. Goellner K, Conrath U, (2008) Priming: it's all the world to induced disease resistance. Eur J Plant Pathol 121: 233-242.
51. Kanehisaa M, Goto S, (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28: 27-30.
52. Caillau M, Paul Quick W, (2005) New insights into plant transaldolase. Plant J 43: 1-16.
53. Moehs CP, Allen PV, Friedman M, Belknap WR, (1996) Cloning and expression of transaldolase from potato. Plant Mol Biol 32: 447-452.
54. Singh DK, McNellis TW, (2011) Fibrillin protein function: the tip of the iceberg? Trends in Plant Science In Press, Corrected Proof.
55. Youssef A, Laizet Yh, Block MA, Maréchal E, Alcaraz J-P, et al. (2010) Plant lipid-associated fibrillin proteins condition jasmonate production under photosynthetic stress. Plant J 61: 436-445.
56. Eschen-Lippold L, Altmann S, Gebhardt C, Göbel C, Feussner I, et al. (2010) Oxylipins are not required for R gene-mediated resistance in potato. Eur J Plant Pathol 127: 437-442.
57. Wasternack C, (2007) Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany 100: 681-697.
58. Odeny DA, Stich B, Gebhardt C, (2010) Physical organization of mixed protease inhibitor gene clusters, coordinated expression and association with resistance to late blight at the StKI locus on potato chromosome III. Plant, Cell & Environment 33: 2149-2161.
59. Mayrose M, Ekengren SK, Melech-Bonfil S, Martin GB, Sessa G, (2006) A novel link between tomato GRAS genes, plant disease resistance and mechanical stress response. Mol Plant Pathol 7: 593-604.
60. Ballvora A, Jöcker A, Viehover P, Ishihara H, Paal J, et al. (2007) Comparative sequence analysis of Solanum and Arabidopsis in a hot spot for pathogen resistance on potato chromosome V reveals a patchwork of conserved and rapidly evolving genome segments. BMC Genomics 8: 112.
61. Bormann CA, (2003) Genetic and molecular analysis of quantitative and qualitative late blight resistance in tetraploid potato. Hohenheim University of Hohenheim.
62. Jones JD, Shlumukov L, Carland F, English J, Scofield SR, et al. (1992) Effective vectors for transformation, expression of heterologous genes, and assaying transposon excision in transgenic plants. Transgenic Res 1: 285-297.
63. Si-Ammour A, Mauch-Mani B, Mauch F, (2003) Quantification of induced resistance against Phytophthora species expressing GFP as a vital marker: â-aminobutyric acid but not BTH protects potato and Arabidopsis from infection. Mol Plant Pathol 4: 237-248.
64. Caten CE, Junks JL, (1968) Spontaneous variability of single isolates of Phytophthora infestans l. Cultural variation. Can J Botany 46: 329-348.
65. Leonards-Schippers C, Gieffers W, Salamini F, Gebhardt C, (1992) The R1 gene conferring race-specific resistance to Phytophthora infestans in potato is located on potato chromosome V. Mol Gen Genet 233: 278-283.
66. Judelson HS, Tooley PW, (2000) Enhanced polymerase chain reaction methods for detecting and quantifying Phytophthora infestans in plants. Phytopathology 90: 1112-1119.
67. Nielsen KL, Petersen AH, Emmersen J, eds. (2008) (2008) DeepSAGE - tag based transcriptome analysis beyond microarrays Berlin, Germany Wiley-Blackwell pp. 229-239.
68. Meyer S, Nagel A, Gebhardt C, (2005) PoMaMo-a comprehensive database for potato genome data. Nucl Acids Res 33: D666-670.
69. Rickert AM, Kim JH, Meyer S, Nagel A, Ballvora A, et al. (2003) First-generation SNP/InDel markers tagging loci for pathogen resistance in the potato genome. Plant Biotechnol J 1: 399-410.
70. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological) 57: 289-300.
71. Maere S, Heymans K, Kuiper M, (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449.
72. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.