Simultaneous Transcriptome Analysis of Sorghum and Bipolaris sorghicola by Using RNA-seq in Combination with De Novo Transcriptome Assembly

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Yazawa, Takayuki ^a,b   Kawahigashi, Hiroyuki ^a   Matsumoto, Takashi ^a   Mizuno, Hiroshi ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b HITACHI LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; LYSINE MOTIF KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PROTEIN CPCA; PROTEIN HACA; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; BIPOLARIS SORGHICOLA; CAMS GENE; CDPK GENE; CIPK GENE; CONTROLLED STUDY; CULTIVAR; FUNGUS; FUNGUS GROWTH; FUNGUS IDENTIFICATION; GENE EXPRESSION; GENE IDENTIFICATION; LEUCINE RICH REPEAT GENE; MITOGEN ACTIVATED PROTEIN KINASE GENE; MITOGEN ACTIVATED PROTEIN KINASE KINASE GENE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE GENE; NONHUMAN; PHYLOGENETIC TREE; PLANT DEFENSE; PLANT FUNGUS INTERACTION; PLANT GENE; PLANT GENOME; PLANT LEAF; PLANT PATHOGEN INTERACTION; PROTEIN DOMAIN; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SORGHUM; TRANSCRIPTOMICS; WRKY28 GENE; WRKY45 GENE; ASCOMYCETES; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PHYSIOLOGY;

BIPOLARIS SORGHICOLA; FUNGI; POACEAE; SORGHUM BICOLOR;

ASCOMYCOTA; GENE EXPRESSION REGULATION, FUNGAL; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; PLANT PROTEINS; SEQUENCE ANALYSIS, RNA; SORGHUM; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84876974302     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062460     Document Type: Article

References (85)

1. Dodds PN, Rathjen JP, (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nature reviews Genetics 11: 539-548.
2. Tör M, Lotze MT, Holton N, (2009) Receptor-mediated signalling in plants: molecular patterns and programmes. Journal of experimental botany 60: 3645-3654.
3. Tena G, Boudsocq M, Sheen J, (2011) Protein kinase signaling networks in plant innate immunity. Current opinion in plant biology 14: 519-529.
4. Naoumkina M a, He X, Dixon R a, (2008) Elicitor-induced transcription factors for metabolic reprogramming of secondary metabolism in Medicago truncatula. BMC plant biology 8: 132.
5. Van Loon LC, Rep M, Pieterse CMJ, (2006) Significance of inducible defense-related proteins in infected plants. Annual review of phytopathology 44: 135-162.
6. Hok S, Attard A, Keller H, (2010) Getting the most from the host: how pathogens force plants to cooperate in disease. Molecular plant-microbe interactions: MPMI 23: 1253-1259.
7. Westermann AJ, Gorski S a, Vogel J, (2012) Dual RNA-seq of pathogen and host. Nature Reviews Microbiology 10: 618-630.
8. Kawahara Y, Oono Y, Kanamori H, Matsumoto T, Itoh T, et al. (2012) Simultaneous RNA-Seq Analysis of a Mixed Transcriptome of Rice and Blast Fungus Interaction. PLoS ONE 7: e49423.
9. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson D a, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature biotechnology 29: 644-652.
10. Zhao Q-Y, Wang Y, Kong Y-M, Luo D, Li X, et al. (2011) Optimizing de novo transcriptome assembly from short-read RNA-Seq data: a comparative study. BMC Bioinformatics 12: S2.
11. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, et al. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551-556.
12. Kawahigashi H, Kasuga S, Ando T, Kanamori H, Wu J, et al. (2011) Positional cloning of ds1, the target leaf spot resistance gene against Bipolaris sorghicola in sorghum. TAG Theoretical and applied genetics Theoretische und angewandte Genetik 123: 131-142.
13. Mizuno H, Kawahigashi H, Kawahara Y, Kanamori H, Ogata J, et al. (2012) Global transcriptome analysis reveals distinct expression among duplicated genes during sorghum-Bipolarissorghicola interaction. BMC Plant Biology 12: 121.
14. Schulz MH, Zerbino DR, Vingron M, Birney E, (2012) Oases: Robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics (Oxford, England) 28: 1-7.
15. Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5: 1-8 doi:10.1038/NMETH.1226.
16. Pruitt KD, Tatusova T, Maglott DR, (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic acids research 35: D61-5.
17. Boeckmann B, (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Research 31: 365-370.
18. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic acids research 40: D1178-86.
19. Trapnell C, Williams B a, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28: 511-515.
20. Hipskind JD, Nicholson RL, Goldsbrough PB, (1997) Isolation of a cDNA encoding a novel leucine-rich repeat motif from Sorghum bicolor inoculated with fungi. Molecular plantmicrobe interactions MPMI 10: 819-825.
21. Schwessinger B, Ronald PC, (2012) Plant innate immunity: perception of conserved microbial signatures. Annual review of plant biology 63: 451-482.
22. Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LGG, Rensing S a, Kersten B, et al. (2010) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic acids research 38: D822-7.
23. Pandey SP, Somssich IE, (2009) The role of WRKY transcription factors in plant immunity. Plant physiology 150: 1648-1655.
24. Cosio C, Dunand C, (2009) Specific functions of individual class III peroxidase genes. Journal of experimental botany 60: 391-408.
25. Liu G, Sheng X, Greenshields DL, Ogieglo A, Kaminskyj S, et al. (2005) Profiling of wheat class III peroxidase genes derived from powdery mildew-attacked epidermis reveals distinct sequence-associated expression patterns. Molecular plant-microbe interactions: MPMI 18: 730-741.
26. Koua D, Cerutti L, Falquet L, Sigrist CJ a, Theiler G, et al. (2009) PeroxiBase: a database with new tools for peroxidase family classification. Nucleic acids research 37: D261-6.
27. Chua NH, Soundararajan S, Jedd G, Li X, Ramos-pamplon M, et al. (2004) Woronin Body Function in Magnaporthe grisea Is Essential for Efficient Pathogenesis and for Survival during Nitrogen Starvation Stress. The Plant Cell 16: 1564-1574 doi:10.1105/tpc.020677.2001.
28. De Jonge R, Thomma BPHJ, (2009) Fungal LysM effectors: extinguishers of host immunity? Trends in microbiology 17: 151-157.
29. Carsiotis M, Jones RF, Wesseling a C, (1974) Cross-pathway regulation: histidine-mediated control of histidine, tryptophan, and arginine biosynthetic enzymes in Neurospora crassa. Journal of bacteriology 119: 893-898.
30. Krappmann S, Bignell EM, Reichard U, Rogers T, Haynes K, et al. (2004) The Aspergillus fumigatus transcriptional activator CpcA contributes significantly to the virulence of this fungal pathogen. Molecular microbiology 52: 785-799.
31. Elliott CE, Fox EM, Jarvis RS, Howlett BJ, (2011) The cross-pathway control system regulates production of the secondary metabolite toxin, sirodesmin PL, in the ascomycete, Leptosphaeria maculans. BMC microbiology 11: 169.
32. Cox JS, Walter P, (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87: 391-404.
33. Moore K a, Hollien J, (2012) The unfolded protein response in secretory cell function. Annual review of genetics 46: 165-183.
34. Richie DL, Hartl L, Aimanianda V, Winters MS, Fuller KK, et al. (2009) A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLoS pathogens 5: e1000258.
35. Van den Brink J, De Vries RP, (2011) Fungal enzyme sets for plant polysaccharide degradation. Applied microbiology and biotechnology 91: 1477-1492.
36. Vogel J, (2008) Unique aspects of the grass cell wall. Current opinion in plant biology 11: 301-307.
37. Lalaoui F, Halama P, Dumortier V, Paul B, (2000) Cell wall-degrading enzymes produced in vitro by isolates of Phaeosphaeria nodorum differing in aggressiveness. Plant Pathology 49: 727-733.
38. Pandelova I, Betts MF, Manning V a, Wilhelm LJ, Mockler TC, et al. (2009) Analysis of transcriptome changes induced by Ptr ToxA in wheat provides insights into the mechanisms of plant susceptibility. Molecular plant 2: 1067-1083.
39. Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, et al. (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. The Plant journal: for cell and molecular biology 56: 181-195.
40. Zhou L, Cheung M-Y, Zhang Q, Lei C-L, Zhang S-H, et al. (2009) A novel simple extracellular leucine-rich repeat (eLRR) domain protein from rice (OsLRR1) enters the endosomal pathway and interacts with the hypersensitive-induced reaction protein 1 (OsHIR1). Plant, cell & environment 32: 1804-1820.
41. Xu Z-S, Xiong T-F, Ni Z-Y, Chen X-P, Chen M, et al. (2009) Isolation and identification of two genes encoding leucine-rich repeat (LRR) proteins differentially responsive to pathogen attack and salt stress in tobacco. Plant Science 176: 38-45.
42. Jacques A, Ghannam A, Erhardt M, De Ruffray P, Baillieul F, et al. (2006) NtLRP1, a tobacco leucine-rich repeat gene with a possible role as a modulator of the hypersensitive response. Molecular plant-microbe interactions: MPMI 19: 747-757.
43. Park YH, Choi C, Park EM, Kim HS, Park HJ, et al. (2012) Over-expression of rice leucine-rich repeat protein results in activation of defense response, thereby enhancing resistance to bacterial soft rot in Chinese cabbage. Plant cell reports 31: 1845-1850.
44. Chen F, Yuan Y, Li Q, He Z, (2007) Proteomic analysis of rice plasma membrane reveals proteins involved in early defense response to bacterial blight. Proteomics 7: 1529-1539.
45. Zhou L, Cheung M-Y, Li M-W, Fu Y, Sun Z, et al. (2010) Rice hypersensitive induced reaction protein 1 (OsHIR1) associates with plasma membrane and triggers hypersensitive cell death. BMC plant biology 10: 290.
46. Choi HW, Kim YJ, Hwang BK, (2011) The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity. Molecular plant-microbe interactions: MPMI 24: 68-78.
47. Delteil A, Blein M, Faivre-rampant O, Guellim A, Estevan J, et al. (2012) Building a mutant resource for the study of disease resistance in rice reveals the pivotal role of several genes involved in defence. Molecular Plant Pathology 13: 72-82 doi:10.1111/J.1364-3703.2011.00731.X.
48. Shen Q-H, Saijo Y, Mauch S, Biskup C, Bieri S, et al. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science (New York, NY) 315: 1098-1103.
49. Alfano JR, (2009) Roadmap for future research on plant pathogen effectors. Molecular Plant Pathology 10: 805-813 doi:10.1111/J.1364-3703.2009.00588.X.
50. Shimono M, Sugano S, Nakayama A, Jiang C-J, Ono K, et al. (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. The Plant cell 19: 2064-2076.
51. Shimono M, Koga H, Akagi AYA, Hayashi N, Goto S, et al. (2012) Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Molecular Plant Pathology 13: 83-94 doi:10.1111/J.1364-3703.2011.00732.X.
52. Passardi F, Longet D, Penel C, Dunand C, (2004) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65: 1879-1893.
53. Allison SD, Schultz JC, (2004) Differential activity of peroxidase isozymes in response to wounding, gypsy moth, and plant hormones in northern red oak (Quercus rubra L.). Journal of chemical ecology 30: 1363-1379.
54. Loukili A, Limam F, Ayadi A, Boyer N, Ouelhazi L, (1999) Purification and characterization of a neutral peroxidase induced by rubbing tomato internodes. Physiologia Plantarum 105: 24-31.
55. Reimers PJ, Guo a, Leach JE, (1992) Increased Activity of a Cationic Peroxidase Associated with an Incompatible Interaction Between Xanthomonas oryzae pv oryzae and Rice (Oryza sativa). Plant physiology 99: 1044-1050.
56. Young S a, Guo a, Guikema J a, White FF, Leach JE, (1995) Rice cationic peroxidase accumulates in xylem vessels during incompatible interactions with Xanthomonas oryzae pv oryzae. Plant physiology 107: 1333-1341.
57. Hilaire E, Young S a, Willard LH, McGee JD, Sweat T, et al. (2001) Vascular defense responses in rice: peroxidase accumulation in xylem parenchyma cells and xylem wall thickening. Molecular plant-microbe interactions: MPMI 14: 1411-1419.
58. Wally O, Punja ZK, (2010) Enhanced disease resistance in transgenic carrot (Daucus carota L.) plants over-expressing a rice cationic peroxidase. Planta 232: 1229-1239.
59. Altpeter F, Varshney A, Abderhalden O, Douchkov D, Sautter C, et al. (2005) Stable expression of a defense-related gene in wheat epidermis under transcriptional control of a novel promoter confers pathogen resistance. Plant molecular biology 57: 271-283.
60. Schweizer P, (2008) Tissue-specific expression of a defence-related peroxidase in transgenic wheat potentiates cell death in pathogen-attacked leaf epidermis. Molecular Plant Pathology 9: 45-57.
61. Johrde A, Schweizer P, (2008) A class III peroxidase specifically expressed in pathogen-attacked barley epidermis contributes to basal resistance. Molecular Plant Pathology 9: 687-696.
62. Campos-Soriano L, Gómez-Ariza J, Bonfante P, San Segundo B, (2011) A rice calcium-dependent protein kinase is expressed in cortical root cells during the presymbiotic phase of the arbuscular mycorrhizal symbiosis. BMC plant biology 11: 90.
63. Mall TK, Dweikat I, Sato SJ, Neresian N, Xu K, et al. (2011) Expression of the rice CDPK-7 in sorghum: molecular and phenotypic analyses. Plant molecular biology 75: 467-479.
64. Boudsocq M, Sheen J, (2012) CDPKs in immune and stress signaling. Trends in plant science 18: 30-40.
65. Xiang Y, Huang Y, Xiong L, (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant physiology 144: 1416-1428.
66. Martin M, (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal 17: 10-12.
67. Langmead B, Salzberg SL, (2012) Fast gapped-read alignment with Bowtie 2. Nature methods 9: 357-359.
68. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics (Oxford, England) 25: 2078-2079.
69. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics (Oxford, England) 25: 1105-1111.
70. Zerbino DR, Birney E, (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome research 18: 821-829.
71. Li W, Godzik A, (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics (Oxford, England) 22: 1658-1659.
72. Kent WJ, (2002) BLAT-the BLAST-like alignment tool. Genome Research 12: 656-664.
73. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, et al. (2009) BLAST+: architecture and applications. BMC bioinformatics 10: 421.
74. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic acids research 38: D211-22.
75. Higo K, Ugawa Y, Iwamoto M, Higo H, (1998) PLACE: a database of plant cis-acting regulatory DNA elements. Nucleic acids research 26: 358-359.
76. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, et al. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic acids research 39: D225-9.
77. Mi H, Dong Q, Muruganujan A, Gaudet P, Lewis S, et al. (2010) PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic acids research 38: D204-10.
78. Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, et al. (2012) InterPro in 2011: new developments in the family and domain prediction database. Nucleic acids research 40: D306-12.
79. Sonnhammer EL, Von Heijne G, Krogh A, (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proceedings International Conference on Intelligent Systems for Molecular Biology ISMB International Conference on Intelligent Systems for Molecular Biology 6: 175-182.
80. Shen H-B, Chou K-C, (2007) Signal-3L: A 3-layer approach for predicting signal peptides. Biochemical and biophysical research communications 363: 297-303.
81. Hiller K, Grote A, Scheer M, Münch R, Jahn D, (2004) PrediSi: prediction of signal peptides and their cleavage positions. Nucleic acids research 32: W375-9.
82. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic acids research 22: 4673-4680.
83. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular biology and evolution 28: 2731-2739.
84. Felsenstein J, (1985) Confidence-Limits on Phylogenies- an Approach Using the Bootstrap. Evolution 39: 783-791.
85. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, et al. (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic acids research 40: D1202-10.