Current Genetics

, Volume 60, Issue 4, pp 327–341 | Cite as

Identification and functional analysis of AG1-IA specific genes of Rhizoctonia solani

Research Article

Abstract

Rhizoctonia solani is an important necrotrophic fungal pathogen which causes disease on diverse plant species. It has been classified into 14 genetically distinct anastomosis groups (AGs), however, very little is known about their genomic diversity. AG1-IA causes sheath blight disease in rice and controlling this disease remains a challenge for sustainable rice cultivation. Recently the draft genome sequences of AG1-IA (rice isolate) and AG1-IB (lettuce isolate) had become publicly available. In this study, using comparative genomics, we report identification of 3,942 R. solani genes that are uniquely present in AG1-IA. Many of these genes encode important biological, molecular functions and exhibit dynamic expression during in-planta growth of the pathogen in rice. Based upon sequence similarity with genes that are required for plant and human/zoonotic diseases, we identified several putative virulence/pathogenicity determinants amongst AG1-IA specific genes. While studying the expression of 19 randomly selected genes, we identified three genes highly up-regulated during in-planta growth. The detailed in silico characterization of these genes and extent of their up-regulation in different rice genotypes, having variable degree of disease susceptibility, suggests their importance in rice–Rhizoctonia interactions. In summary, the present study reports identification, functional characterization of AG1-IA specific genes and predicts important virulence determinants that might enable the pathogen to grow inside hostile plant environment. Further characterization of these genes would shed useful insights about the pathogenicity mechanism of AG1-IA on rice.

Keywords

Sheath blight disease Fungal pathogenesis Anastomosis group Disease resistance Host specificity Necrotrophs Secondary metabolism Toxins 

Supplementary material

294_2014_438_MOESM1_ESM.pdf (71 kb)
Online Resource 1: List of primers (PDF 70 kb)
294_2014_438_MOESM2_ESM.xlsx (23 kb)
Online Resource 2: Blast analysis against AG1-IB genomic contigs and Inparanoid database based ortholog prediction (XLSX 22 kb)
294_2014_438_MOESM3_ESM.xlsx (227 kb)
Online Resource 3: List of AG1-IA specificR. solanigenes (XLSX 227 kb)
294_2014_438_MOESM4_ESM.xlsx (356 kb)
Online Resource 4: Distribution of AG1-IA specificR. solanigenes across different genomic contigs (XLSX 355 kb)
294_2014_438_MOESM5_ESM.xlsx (13 kb)
Online Resource 5: GO annotation of AG1-IA specific genes clustered in each genomic contig (XLSX 12 kb)
294_2014_438_MOESM6_ESM.pdf (1.5 mb)
Online Resource 6: The orthologs of AG1-IA specific genes in FungiDB database. (PDF 1576 kb)
294_2014_438_MOESM7_ESM.pdf (667 kb)
Online Resource 7: The relative proportion of AG1-IA specific GO terms compared to that present in entire AG1-IA genome. The relative fraction of GO terms was computed using custom script and top 20 terms in Biological Process (A) and Molecular Function (B) are displayed. (PDF 667 kb)
294_2014_438_MOESM8_ESM.pdf (727 kb)
Online Resource 8: KOG and KEGG classification of AG1-IA specific genes. KOG and KEGG classification of AG1-IA specific genes were performed using eggNOG application and KAAS annotation server, respectively. The analysis classified 613 AG1-IA specific proteins into 23 KOG groups (A) and 187 genes across KEGG pathways. (PDF 727 kb)
294_2014_438_MOESM9_ESM.xlsx (23 kb)
Online Resource 9: AG1-IA specific genes having homology in PHIDIAS database. (XLSX 23 kb)
294_2014_438_MOESM10_ESM.pdf (589 kb)
Online Resource 10: KEGG annotation of AG1-IA specific proteins that demonstrate homology in PHIDIAS database. (PDF 589 kb)
294_2014_438_MOESM11_ESM.tif (847 kb)
Online Resource 11: Microscopic analysis oftrypan blue stained mycelia of differentRhizoctoniastrains. The analysis was performed using Nikon Eclipse E100 microscope at 400X magnification. (TIFF 846 kb)
294_2014_438_MOESM12_ESM.docx (109 kb)
Online Resource 12: Phylogenetic relationship and ITS sequences of differentRhizoctoniastrains (DOCX 108 kb)
294_2014_438_MOESM13_ESM.pdf (1.3 mb)
Online Resource 13: PCR analysis of selected AG1-IA specific genes across geographically diverse strains ofR. solani. The 19 selected genes were PCR amplified from different R. solani strains (A. BRS-1, B. BRS-2, C. BRS-6, D. BRS-7, E. BRS-4) analysed on 1.5 % agarose gel. The presence of these genes across different strains is summarized in F. Dark dot reflects confirmative presence of these genes, while cases having ambiguity are reflected as empty dots. The lane L2 and M2 represent the same gene, however the primer binding sites are different. M represents molecular weight marker. (PDF 1310 kb)
294_2014_438_MOESM14_ESM.pdf (421 kb)
Online Resource 14: PCR analysis to confirm the presence of some ambiguous AG1-IA specific genes. The genes RS_L1, RS_L5, RS_L6, and RS_M5 which showed ambiguous results in PCR (Online Resource 11) were individually PCR amplified in different AG1-1A isolates. M represents molecular weight marker. (PDF 420 kb)
294_2014_438_MOESM15_ESM.xlsx (296 kb)
Online Resource 15: FPKM based expression analysis of AG1-IA specific genes (XLSX 296 kb)
294_2014_438_MOESM16_ESM.xlsx (1.1 mb)
Online Resource 16: Differential expression profile of AG1-IA specific genes across different time intervals (XLSX 1131 kb)
294_2014_438_MOESM17_ESM.pdf (2.5 mb)
Online Resource 17: Expression dynamics of selected AG1-IA specific genes. Semi-quantitative PCR based expressions of 19 selected candidate AG1-IA specific genes were analysed. The expression at 3 and 6 DPI of BRS-1 growth in susceptible rice IR64 is depicted in A and D, respectively. The expression at 3 and 6 DPI of BRS-1 growth in partially resistant rice cultivar Tetep is depicted in B and E, respectively while the expression during its growth in potato dextrose broth (PDB) at 3 and 6 DPI is reflected in C and F, respectively. The expression pattern of these genes at different stages is summarized in G. Dark dot reflects confirmative expression of these genes, while ambiguous cases are reflected as empty dots. R. solani specific 18S rDNA primers were used as a normalization control. The data is a representative of at least two biological and three technical replicates. The lane L2 and M2 represent the same gene, however the primer binding sites were different. M represents molecular weight marker. (PDF 2540 kb)
294_2014_438_MOESM18_ESM.pdf (416 kb)
Online Resource 18: Domain architecture of in-planta induced AG1-IA specific genes. The domain architecture of RS_P1 (A), RS_P3 (B), RS_P4 (C) proteins as revealed by Prosite and Pfam analysis. a: represents AG1-IA specific sequence while b: represents AG3 sequence, the nearest ortholog as per BLASTP analysis. Red flag in A.a represents PkC phosphorylation site and CAMP phosphorylation site is denoted by grey flag. In B.a Violet flag represents a PkC phosphorylation site while red and grey flag denotes N myristylation and Asn Glycosylation sites, respectively. Red flags in C.a represent N- Myristylation sites at N-terminal. (PDF 416 kb)

References

  1. Ahvenniemi P, Wolf M, Lehtonen MJ, Wilson P, German-Kinnari M, Valkonen JPT (2009) Evolutionary diversification indicated by compensatory base changes in ITS2 secondary structures in a complex fungal species, Rhizoctonia solani. J Mol Evol 69:150–163. doi:10.1007/s00239-009-9260-3 PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefPubMedCentralGoogle Scholar
  3. Anderson NA (1982) The genetics and pathology of Rhizoctonia solani. Annu Rev Phytopathol 20:329–347CrossRefGoogle Scholar
  4. Brooks SA (2007) Sensitivity to a phytotoxin from Rhizoctonia solani correlates with sheath blight susceptibility in rice. Phytopathology 97:1207–1212. doi:10.1094/PHYTO-97-10-1207 PubMedCrossRefGoogle Scholar
  5. Channamallikarjuna V, Sonah H, Prasad M, Rao GJN, Chand S, Upreti HC, Singh NK, Sharma TR (2009) Identification of major quantitative trait loci qSBR11-1 for sheath blight resistance in rice. Mol Breed 25:155–166. doi:10.1007/s11032-009-9316-5 CrossRefGoogle Scholar
  6. Ciuffetti LM, Manning VA, Pandelova I, Betts MF, Martinez JP (2010) Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis–wheat interaction. New Phytol 187:911–919. doi:10.1111/j.1469-8137.2010.03362.x PubMedCrossRefGoogle Scholar
  7. Crack JC, Green J, Thomson AJ, Le Brun NE (2012) Iron–sulfur cluster sensor-regulators. Curr Opin Chem Biol 16:35–44. doi:10.1016/j.cbpa.2012.02.009 PubMedCrossRefGoogle Scholar
  8. De Castro E, Sigrist CJA, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Bairoch A, Hulo N (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34:W362–W365. doi:10.1093/nar/gkl124 PubMedCrossRefPubMedCentralGoogle Scholar
  9. De Hoon MJL, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453–1454. doi:10.1093/bioinformatics/bth078 PubMedCrossRefGoogle Scholar
  10. Devasahayam G, Chaturvedi V, Hanes SD (2002) The Ess1 prolyl isomerase is required for growth and morphogenetic switching in Candida albicans. Genetics 160:37–48PubMedPubMedCentralGoogle Scholar
  11. Doyle JJ, Doyle JL (1990) A rapid total DNA preparation procedure for fresh plant tissue. Focus (Madison) 12:13–15Google Scholar
  12. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868. doi:10.1073/pnas.95.25.14863 PubMedCrossRefPubMedCentralGoogle Scholar
  13. Fenille RC, de Souza NL, Kuramae EE (2002) Characterization of Rhizoctonia solani associated with soybean in Brazil. Eur J Plant Pathol 108:783–792CrossRefGoogle Scholar
  14. Frei dit Frey N, Robatzek S (2009) Trafficking vesicles: pro or contra pathogens? Curr Opin Plant Biol 12:437–443. doi:10.1016/j.pbi.2009.06.002 PubMedCrossRefGoogle Scholar
  15. Gemmill TR, Wu X, Hanes SD (2005) Vanishingly low levels of Ess1 prolyl-isomerase activity are sufficient for growth in Saccharomyces cerevisiae. J Biol Chem 280:15510–15517. doi:10.1074/jbc.M412172200 PubMedCrossRefGoogle Scholar
  16. Giraldo MC, Dagdas YF, Gupta YK, Mentlak Ta, Yi M, Martinez-Rocha AL, Saitoh H, Terauchi R, Talbot NJ, Valent B (2013) Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat Commun 4:1996. doi:10.1038/ncomms2996 PubMedCrossRefPubMedCentralGoogle Scholar
  17. Gonzalez Garcia V, Portal Onco MA, Rubio Susan V (2006) Review. Biology and systematics of the form genus Rhizoctonia. Span J Agric Res 4:55–79CrossRefGoogle Scholar
  18. Guillemaut C, Edel-Hermann V, Camporota P, Alabouvette C, Richard-Molard M, Steinberg C (2003) Typing of anastomosis groups of Rhizoctonia solani by restriction analysis of ribosomal DNA. Can J Microbiol 49:556–568. doi:10.1139/w03-066 PubMedCrossRefGoogle Scholar
  19. Heller J, Tudzynski P (2011) Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu Rev Phytopathol 49:369–390. doi:10.1146/annurev-phyto-072910-095355 PubMedCrossRefGoogle Scholar
  20. Howlett BJ (2006) Secondary metabolite toxins and nutrition of plant pathogenic fungi. Curr Opin Plant Biol 9:371–375. doi:10.1016/j.pbi.2006.05.004 PubMedCrossRefGoogle Scholar
  21. Ito K, Tanaka T, Hatta R, Yamamoto M, Akimitsu K, Tsuge T (2004) Dissection of the host range of the fungal plant pathogen Alternaria alternata by modification of secondary metabolism. Mol Microbiol 52:399–411. doi:10.1111/j.1365-2958.2004.04004.x PubMedCrossRefGoogle Scholar
  22. Jia Y, Liu G, Park DS, Yang Y (2013) Inoculation and scoring methods for rice sheath blight disease. Methods Mol Biol 956:257–268PubMedCrossRefGoogle Scholar
  23. Keijer J, Houterman PM, Dullemans AM, Korsman MG (1996) Heterogeneity in electrophoretic karyotype within and between anastomosis groups of Rhizoctonia solani. Mycol Res 100:789–797. doi:10.1016/S0953-7562(96)80023-2 CrossRefGoogle Scholar
  24. Khush GS (2005) What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol 59:1–6. doi:10.1007/s11103-005-2159-5 PubMedCrossRefGoogle Scholar
  25. Kuninaga S, Natsuaki T, Takeuchi T, Yokosawa R (1997) Sequence variation of the rDNA ITS regions within and between anastomosis groups in Rhizoctonia solani. Curr Genet 32:237–243. doi:10.1007/s002940050272 PubMedCrossRefGoogle Scholar
  26. Lee FN, Rush MC (1983) Rice sheath blight: a major rice disease. Plant Dis 67:829–832CrossRefGoogle Scholar
  27. Lill R (2009) Function and biogenesis of iron–sulphur proteins. Nature 460:831–838. doi:10.1038/nature08301 PubMedCrossRefGoogle Scholar
  28. Liu Z, Zhang Z, Faris JD, Oliver RP, Syme R, McDonald MC, McDonald BA, Solomon PS, Lu S, Shelver WL, Xu S, Friesen TL (2012) The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS Pathog 8:e1002467. doi:10.1371/journal.ppat.1002467 PubMedCrossRefPubMedCentralGoogle Scholar
  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408. doi:10.1006/meth.2001.1262 PubMedCrossRefGoogle Scholar
  30. O’Brien KP, Remm M, Sonnhammer ELL (2005) Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res. doi:10.1093/nar/gki107 PubMedGoogle Scholar
  31. Ogoshi A (1987) Ecology and pathogenicity of anastomosis and intraspecific groups of Rhizoctonia solani Kuhn. Annu Rev Phytopathol 25:125–143CrossRefGoogle Scholar
  32. Oliver RP, Friesen TL, Faris JD, Solomon PS (2012) From pathology to genomics and host resistance. Annu Rev Phytopathol 50:23–43. doi:10.1146/annurev-phyto-081211-173019 PubMedCrossRefGoogle Scholar
  33. Ortoneda M, Guarro J, Madrid MP, Caracuel Z, Roncero MIG, Mayayo E, Di Pietro A (2004) Fusarium oxysporum as a multihost model for the genetic dissection of fungal virulence in plants and mammals. Infect Immun 72:1760–1766. doi:10.1128/IAI.72.3.1760-1766.2004 PubMedCrossRefPubMedCentralGoogle Scholar
  34. Pan XB, Rush MC, Sha XY, Xie QJ, Liscombe SD, Stenina SR, Orad JH (1999) Major gene non-allelic sheath blight resistance from the rice cultivars Jasmine 85 and Teqing. Crop Sci 39:338–346Google Scholar
  35. Panstruga R (2010) Introduction to a virtual special issue on pathogenic plant–fungus interactions. New Phytol 188:907–910. doi:10.1111/j.1469-8137.2010.03530.x PubMedCrossRefGoogle Scholar
  36. Park D-S, Sayler RJ, Hong Y-G, Nam M-H, Yang Y (2008) A method for inoculation and evaluation of rice sheath blight disease. Plant Dis 92:25–29. doi:10.1094/PDIS-92-1-0025 CrossRefGoogle Scholar
  37. Prasad B, Eizenga GC (2008) Rice sheath blight disease resistance identified in Oryza spp. accessions. Plant Dis 92:1503–1509. doi:10.1094/PDIS-92-11-1503 CrossRefGoogle Scholar
  38. Remm M, Storm CE, Sonnhammer EL (2001) Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol 314:1041–1052. doi:10.1006/jmbi.2000.5197 PubMedCrossRefGoogle Scholar
  39. Ren P, Rossettini A, Chaturvedi V, Hanes SD (2005) The Ess1 prolyl isomerase is dispensable for growth but required for virulence in Cryptococcus neoformans. Microbiology 151:1593–1605. doi:10.1099/mic.0.27786-0 PubMedCrossRefGoogle Scholar
  40. Rioux R, Manmathan H, Singh P, los Reyes B, Jia Y, Tavantzis S (2011) Comparative analysis of putative pathogenesis-related gene expression in two Rhizoctonia solani pathosystems. Curr Genet 57:391–408. doi:10.1007/s00294-011-0353-3 PubMedCrossRefGoogle Scholar
  41. Rouault TA, Tong W-H (2005) Iron–sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat Rev Mol Cell Biol 6:345–351PubMedCrossRefGoogle Scholar
  42. Rush MC, Lee F (1992) Sheath blight. In: Webster F, Gunnell P (eds) Compendium of Rice Diseases. APS Press, St. Paul, pp 22–23Google Scholar
  43. Sato H, Ideta IO, Ando I, Kunihiro Y, Hirabayashi H, Iwano M, Miyasaka A, Nemoto H, Imbe T (2004) Mapping QTLs for sheath blight resistance in the rice line WSS2. Breed Sci 54:265–271CrossRefGoogle Scholar
  44. Sexton AC, Howlett BJ (2006) Parallels in fungal pathogenesis on plant and animal hosts. Eukaryot Cell 5:1941–1949. doi:10.1128/EC.00277-06 PubMedCrossRefPubMedCentralGoogle Scholar
  45. Sharon A, Shlezinger N (2013) Fungi infecting plants and animals: killers, non-killers, and cell death. PLoS Pathog 9:e1003517PubMedCrossRefPubMedCentralGoogle Scholar
  46. Sinclair JB (1970) Rhizoctonia solani: special methods of study. In: Parmeter J (ed) Rhizoctonia solani biology and pathology. University of California Press, Berkeley, Los Angeles and London, pp 199–217Google Scholar
  47. Singh HK, Singh U (2012) Virulence diversity of Rhizoctonia solani causing sheath blight disease in rice and its host pathogen interaction. Int J Agric Environ Biotechnol 5:367–372Google Scholar
  48. Sneh B, Ichielevich-Auster M (1998) Induced resistance of cucumber seedlings caused by some non-pathogenicRhizoctonia (np-R) isolates. Phytoparasitica 26:27–38. doi:10.1007/BF02981263 CrossRefGoogle Scholar
  49. Soanes DM, Chakrabarti A, Paszkiewicz KH, Dawe AL, Talbot NJ (2012) Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae. PLoS Pathog. doi:10.1371/journal.ppat.1002514 PubMedPubMedCentralGoogle Scholar
  50. Taheri P, Gnanamanickam S, Höfte M (2007) Characterization, genetic structure, and pathogenicity of Rhizoctonia spp. associated with rice sheath diseases in India. Phytopathology 97:373–383. doi:10.1094/PHYTO-97-3-0373 PubMedCrossRefGoogle Scholar
  51. Tan K-C, Oliver RP, Solomon PS, Moffat CS (2010) Proteinaceous necrotrophic effectors in fungal virulence. Funct Plant Biol 37:907. doi:10.1071/FP10067 CrossRefGoogle Scholar
  52. Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, Egusa M, Yamamoto M, Otani H (2013) Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 37:44–66. doi:10.1111/j.1574-6976.2012.00350.x PubMedCrossRefGoogle Scholar
  53. Vidhyasekaran P, Ponmalar TR, Samiyappan R, Velazhahan R, Vimala R, Ramanathan A, Paranidharan V, Muthukrishnan S (1997) Host-specific toxin production by Rhizoctonia solani, the rice sheath blight pathogen. Phytopathology 87:1258–1263. doi:10.1094/PHYTO.1997.87.12.1258 PubMedCrossRefGoogle Scholar
  54. Wang Y, Pinson SRM, Fjellstrom RG, Tabien RE (2011) Phenotypic gain from introgression of two QTL, qSB9-2 and qSB12-1, for rice sheath blight resistance. Mol Breed 30:293–303. doi:10.1007/s11032-011-9619-1 CrossRefGoogle Scholar
  55. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols, a guide to methods and applications. Academic Press Inc, London, pp 315–322Google Scholar
  56. Wibberg D, Jelonek L, Rupp O, Hennig M, Eikmeyer F, Goesmann A, Hartmann A, Borriss R, Grosch R, Pühler A, Schlüter A (2013) Establishment and interpretation of the genome sequence of the phytopathogenic fungus Rhizoctonia solani AG1-IB isolate 7/3/14. J Biotechnol 167:142–155. doi:10.1016/j.jbiotec.2012.12.010 PubMedCrossRefGoogle Scholar
  57. Willocquet L, Lore JS, Srinivasachary S, Savary S (2011) Quantification of the components of resistance to rice sheath blight using a detached tiller test under controlled conditions. Plant Dis 95:1507–1515. doi:10.1094/PDIS-01-11-0051 CrossRefGoogle Scholar
  58. Winnenburg R, Baldwin TK, Urban M, Rawlings C, Köhler J, Hammond-Kosack KE (2006) PHI-base: a new database for pathogen host interactions. Nucleic Acids Res 34:D459–D464. doi:10.1093/nar/gkj047 PubMedCrossRefPubMedCentralGoogle Scholar
  59. Xiang Z, Tian Y, He Y (2007) PHIDIAS: a pathogen–host interaction data integration and analysis system. Genome Biol 8:R150. doi:10.1186/gb-2007-8-7-r150 PubMedCrossRefPubMedCentralGoogle Scholar
  60. Xiaoxing L, Ping L, Aiping Z (2013) In vitro selection of sheath blight resistance germplams in rice. Afr J Microbiol Res 7:4422–4429. doi:10.5897/AJMR2013.5659 Google Scholar
  61. Yang G, Li C (2012) General description of Rhizoctonia species complex. In: Cumagun CJ (ed) Plant Pathology, pp 41–52Google Scholar
  62. Yang X, Ben S, Sun Y, Fan X, Tian C, Wang Y (2013) Genome-wide identification, phylogeny and expression profile of vesicle fusion components in Verticillium dahliae. PLoS One 8:e68681. doi:10.1371/journal.pone.0068681 PubMedCrossRefPubMedCentralGoogle Scholar
  63. Zheng A, Lin R, Zhang D, Qin P, Xu L, Ai P, Ding L, Wang Y, Chen Y, Liu Y, Sun Z, Feng H, Liang X, Fu R, Tang C, Li Q, Zhang J, Xie Z, Deng Q, Li S, Wang S, Zhu J, Wang L, Liu H, Li P (2013) The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nat Commun 4:1424. doi:10.1038/ncomms2427 PubMedCrossRefPubMedCentralGoogle Scholar
  64. Zou JH, Pan XB, Chen ZX, Xu JY, Lu JF, Zhai WX, Zhu LH (2000) Mapping quantitative trait loci controlling sheath blight resistance in two rice cultivars (Oryza sativa L.). Theory Appl Genet 101:569–573CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Srayan Ghosh
    • 1
  • Santosh Kumar Gupta
    • 1
  • Gopaljee Jha
    • 1
  1. 1.Plant Microbe Interactions LaboratoryNational Institute of Plant Genome ResearchNew DelhiIndia

Personalised recommendations