Genetic and Genomic Analysis of Rhizoctonia solani Interactions with Arabidopsis; Evidence of Resistance Mediated through NADPH Oxidases

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Foley, Rhonda C ^a   Gleason, Cynthia A ^a   Anderson, Jonathan P ^a,b   Hamann, Thorsten ^c   Singh, Karam B ^a,b  

^a CSIRO   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; AUXIN; CAMALEXIN; ETHYLENE; HEAT SHOCK PROTEIN; JASMONIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SALICYLIC ACID; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; DISEASE RESISTANCE; ECOTYPE; ENZYME ACTIVITY; ENZYME ANALYSIS; FUNGAL STRAIN; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ANALYSIS; HSP GENE; MULTIGENE FAMILY; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PLANT DISEASE; PLANT FUNGUS INTERACTION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; THANATEPHORUS CUCUMERIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DISEASE RESISTANCE; GENOMICS; NADPH OXIDASE; RHIZOCTONIA;

EID: 84874509475     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056814     Document Type: Article

References (84)

1. Glazebrook J, (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205-227.
2. Lazniewska J, Macioszek VK, Lawrence CB, Kononowicz AK, (2010) Fight to the death: Arabidopsis thaliana defense response to fungal necrotrophic pathogens. Acta Physiologiae Plantarum 32: 1-10.
3. Friesen TL, Faris JD, Solomon PS, Oliver RP, (2008) Host-specific toxins: effectors of necrotrophic pathogenicity. Cellular Microbiology 10: 1421-1428.
4. Berrocal-Lobo M, Molina A, (2008) Arabidopsis defense response against Fusarium oxysporum. Trends in Plant Science 13: 145-150.
5. Dhawan R, Luo HL, Foerster AM, AbuQamar S, Du HN, et al. (2009) HISTONE MONOUBIQUITINATION1 Interacts with a Subunit of the Mediator Complex and Regulates Defense against Necrotrophic Fungal Pathogens in Arabidopsis. Plant Cell 21: 1000-1019.
6. Flors V, Ton J, van Doorn R, Jakab G, Garcia-Agustin P, et al. (2008) Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant Journal 54: 81-92.
7. Mengiste T, Chen X, Salmeron J, Dietrich R, (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15: 2551-2565.
8. Okubara PA, Paulitz TC, (2005) Root defense responses to fungal pathogens: a molecular perspective. Root physiology: from gene to function pp. 215-226.
9. Tyler BM, (2007) Phytophthora sojae: root rot pathogen of soybean and model oomycete. Molecular Plant Pathology 8: 1-8.
10. Sneh B (1996) Rhizoctonia species: Taxonomy, molecular biology, ecology, pathology and disease control; Second International Symposium on Rhizoctonia, Noordwijkerhout, Netherlands, June 27-30, 1995. Rhizoctonia species: Taxonomy, molecular biology, ecology, pathology and disease control: xvi+578p.
11. Vilgalys R, Cubeta MA, (1994) Molecular systematics and populations biology of Rhizoctonia. Annual Review of Phytopathology 32: 135-155.
12. Carling DE, Kuninaga S, Brainard KA, (2002) Hyphal anastomosis reactions, rDNA-internal transcribed spacer sequences, and virulence levels among subsets of Rhizoctonia solani anastomosis group-2 (AG-2) and AG-BI. Phytopathology 92: 43-50.
13. Gonzalez D, Cubeta MA, Vilgalys R, (2006) Phylogenetic utility of indels within ribosomal DNA and beta-tubulin sequences from fungi in the Rhizoctonia solani species complex. Molecular Phylogenetics and Evolution 40: 459-470.
14. Willocquet L, Savary S, (2011) Resistance to rice sheath blight (Rhizoctonia solani Kuhn) [(teleomorph: Thanatephorus cucumeris (A.B. Frank) Donk.] disease: current status and perspectives. Euphytica 178: 1-22.
15. MacNish GC, Neate SM, (1996) Rhizoctonia bare patch of cereals- An Australian perspective. Plant Disease 80: 965-971.
16. Khangura RK, Barbetti MJ, Sweetingham MW, (1999) Characterization and pathogenicity of Rhizoctonia species on canola. Plant Disease 83: 714-721.
17. Cook RJ, Schillinger WF, Christensen NW, (2002) Rhizoctonia root rot and take-all of wheat in diverse direct-seed spring cropping systems. Canadian Journal of Plant Pathology-Revue Canadienne De Phytopathologie 24: 349-358.
18. Murray GM, Brennan JP, (2009) Estimating disease losses to the Australian wheat industry. Australasian Plant Pathology 38: 558-570.
19. Banville GJ, (1989) Yield losses and damage to potato plants caused by Rhizoctonia solani. Kuhn American Potato Journal 66: 821-834.
20. Hide GA, Read PJ, Hall SM, (1992) Stem canker (Rhizoctoniu solani) on three early and three maincrop potato cultivars: effects of seed tuber size on growth and yield. Annals of Applied Biology 120: 391-403.
21. Verma PR, (1996) Biology and control of Rhizoctonia solani on rapeseed: A review. Phytoprotection 77: 99-111.
22. Kluth C, Varrelmann M, (2010) Maize genotype susceptibility to Rhizoctonia solani and its effect on sugar beet crop rotations. Crop Protection 29: 230-238.
23. Kiewnick S, Jacobsen BJ, Braun-Kiewnick A, Eckhoff JLA, Bergman JW, (2001) Integrated control of Rhizoctonia crown and root rot of sugar beet with fungicides and antagonistic bacteria. Plant Disease 85: 718-722.
24. Kühn J, Rippel R, Schmidhalter U, (2009) Abiotic soil properties and the occurrence of Rhizoctonia crown and root rot in sugar beet. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 172: 661-668.
25. Okubara P, Steber C, DeMacon V, Walter N, Paulitz T, et al. (2009) Scarlet-Rz1, an EMS-generated hexaploid wheat with tolerance to the soilborne necrotrophic pathogens Rhizoctonia solani AG-8 and R. oryzae. TAG Theoretical and Applied Genetics.
26. Knecht K, Seyffarth M, Desel C, Thurau T, Sherameti I, et al. (2010) Expression of BvGLP-1 Encoding a Germin-Like Protein from Sugar Beet in Arabidopsis thaliana Leads to Resistance Against Phytopathogenic Fungi. Molecular Plant-Microbe Interactions 23: 446-457.
27. Sharon M, Freeman S, Sneh B, (2011) Assessment of Resistance Pathways Induced in Arabidopsis thaliana by Hypovirulent Rhizoctonia spp. Isolates. Phytopathology 101: 828-838.
28. Perl-Treves R, Foley RC, Chen WQ, Singh KB, (2004) Early induction of the Arabidopsis GSTF8 promoter by specific strains of the fungal pathogen Rhizoctonia solani. Molecular Plant-Microbe Interactions 17: 70-80.
29. Stodart BJ, Harvey PR, Neate SM, Melanson DL, Scott ES, (2007) Genetic variation and pathogenicity of anastomosis group 2 isolates of Rhizoctonia solani in Australia. Mycological Research 111: 891-900.
30. Kliebenstein DJ, Kroymann J, Brown P, Figuth A, Pedersen D, et al. (2001) Genetic Control of Natural Variation in Arabidopsis Glucosinolate Accumulation. Plant Physiol 126: 811-825.
31. Bari R, Jones J, (2009) Role of plant hormones in plant defence responses. Plant Molecular Biology 69: 473-488.
32. Thatcher LF, Anderson JP, Singh KB, (2005) Plant defence responses: what have we learnt from Arabidopsis? Functional Plant Biology 32: 1-19.
33. Sels J, Mathys J, De Coninck BMA, Cammue BPA, De Bolle MFC, (2008) Plant pathogenesis-related (PR) proteins: A focus on PR peptides. Plant Physiology et Biochemistry 46: 941-950.
34. van Loon LC, Rep M, Pieterse CMJ, (2006) Significance of Inducible Defense-related Proteins in Infected Plants. Annual Review of Phytopathology 44: 135-162.
35. Torres MA, Dangl JL, (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 8: 397-403.
36. Marino D, Dunand C, Puppo A, Pauly N, (2012) A burst of plant NADPH oxidases. Trends in Plant Science 17: 9-15.
37. Torres MA, Dangl JL, Jones JDG, (2002) Arabidopsis gp91(phox) homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences of the United States of America 99: 517-522.
38. Almagro L, Ros LVG, Belchi-Navarro S, Bru R, Barcelo AR, et al. (2009) Class III peroxidases in plant defence reactions. Journal of Experimental Botany 60: 377-390.
39. Bibikov SI, Barnes LA, Gitin Y, Parkinson JS, (2000) Domain organization and flavin adenine dinucleotide-binding determinants in the aerotaxis signal transducer Aer of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 97: 5830-5835.
40. Mushegian AR, Koonin EV, (1995) A putative FAD-binding domain in a distinct group of oxidases including a protein involved in plant development. Protein Science 4: 1243-1244.
41. Edwards R, Dixon DP, (2005) Plant glutathione transferases. Gluthione Transferases and Gamma-Glutamyl Transpeptidases 401: 169-186.
42. Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, et al. (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant Journal 58: 53-68.
43. Gurr SJ, Rushton PJ, (2005) Engineering plants with increased disease resistance: how are we going to express it? Trends in Biotechnology 23: 283-290.
44. Singh KB, Foley RC, Onate-Sanchez L, (2002) Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology 5: 430-436.
45. Eulgem T, Somssich IE, (2007) Networks of WRKY transcription factors in defense signaling. Current Opinion in Plant Biology 10: 366-371.
46. Wang H, Zhao Q, Chen F, Wang M, Dixon RA, (2011) NAC domain function and transcriptional control of a secondary cell wall master switch. The Plant Journal 68: 1104-1114.
47. Gutterson N, Reuber TL, (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Current Opinion in Plant Biology 7: 465-471.
48. Imamura A, Hanaki N, Umeda H, Nakamura A, Suzuki T, et al. (1998) Response regulators implicated in His-to-Asp phosphotransfer signaling in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 95: 2691-2696.
49. Grefen C, Harter K, (2004) Plant two-component systems: principles, functions, complexity and cross talk. Planta 219: 733-742.
50. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, et al. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant Journal 37: 914-939.
51. Wang WX, Vinocur B, Shoseyov O, Altman A, (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science 9: 244-252.
52. van Leeuwen H, Kliebenstein DJ, West MAL, Kim K, van Poecke R, et al. (2007) Natural variation among Arabidopsis thaliana accessions for transcriptome response to exogenous salicylic acid. Plant Cell 19: 2099-2110.
53. Berrocal-Lobo M, Molina A, (2004) Ethylene response factor 1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum. Molecular Plant-Microbe Interactions 17: 763-770.
54. Hoffman T, Schmidt JS, Zheng XY, Bent AF, (1999) Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiology 119: 935-949.
55. Penmetsa RV, Uribe P, Anderson J, Lichtenzveig J, Gish JC, et al. (2008) The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant Journal 55: 580-595.
56. Anderson JP, Lichtenzveig J, Gleason C, Oliver RP, Singh KB, (2010) The B-3 Ethylene Response Factor MtERF1-1 Mediates Resistance to a Subset of Root Pathogens in Medicago truncatula without Adversely Affecting Symbiosis with Rhizobia. Plant Physiology 154: 861-873.
57. Onate-Sanchez L, Anderson JP, Young J, Singh KB, (2007) AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiology 143: 400-409.
58. Geraats BPJ, Bakker P, Lawrence CB, Achuo EA, Hofte M, et al. (2003) Ethylene-insensitive tobacco shows differentially altered susceptibility to different pathogens. Phytopathology 93: 813-821.
59. Venu RC, Jia Y, Gowda M, Jia MH, Jantasuriyarat C, et al. (2007) RL-SAGE and microarray analysis of the rice transcriptome after Rhizoctonia solani infection. Molecular Genetics and Genomics 278: 421-431.
60. Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, et al. (2008) Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiology 146: 669-681.
61. Lionetti V, Raiola A, Camardella L, Giovane A, Obel N, et al. (2007) Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiology 143: 1871-1880.
62. Vogel JP, Raab TK, Somerville CR, Somerville SC, (2004) Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant Journal 40: 968-978.
63. Weinhold AR, Sinclair JB. Rhizoctonia solani: Penetration, colonization, and host response. In: Sneh B, JabajiHare S, Neate S, Dijst G, editors; 1995 Jun 27-30; Noordwijkerhout, Netherlands. pp. 163-174.
64. Keijer J (1996) The initial steps of the infection process in Rhizoctonia solani. In: Sneh B, JabajiHare S, Neate S, Dijst G, editors. Rhizoctonia Species: Taxonomy, Molecular Biology, Ecology, Pathology and Disease Control. Dordrecht: Kluwer Academic Publ. pp. 149-162.
65. Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, et al. (2007) Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10: 310-316.
66. Maimbo M, Ohnishi K, Hikichi Y, Yoshioka H, Kiba A, (2007) Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defense response against Ralstonia solanacearum(1[W]). Plant Physiology 145: 1588-1599.
67. Takahashi A, Casais C, Ichimura K, Shirasu K, (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 100: 11777-11782.
68. Torres MA, (2010) ROS in biotic interactions. Physiologia Plantarum 138: 414-429.
69. Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, et al. (2003) Nicotiana benthamiana gp91(phox) homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15: 706-718.
70. Pogany M, von Rad U, Grun S, Dongo A, Pintye A, et al. (2009) Dual Roles of Reactive Oxygen Species and NADPH Oxidase RBOHD in an Arabidopsis-Alternaria Pathosystem. Plant Physiology 151: 1459-1475.
71. Kimura S, Kaya H, Kawarazaki T, Hiraoka G, Senzaki E, et al. (2012) Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochimica Et Biophysica Acta-Molecular Cell Research 1823: 398-405.
72. Yun BW, Feechan A, Yin MH, Saidi NBB, Le Bihan T, et al. (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478: 264-U161.
73. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen HM, et al. (2003) Genome-wide Insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
74. Chen WQ, Singh KB, (1999) The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant Journal 19: 667-677.
75. Clough SJ, Bent AF, (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735-743.
76. Gao LL, Anderson JP, Klingler JP, Nair RM, Edwards OR, et al. (2007) Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula. Molecular Plant-Microbe Interactions 20: 82-93.
77. 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.
78. Smyth GK, (2005) Limma: Linear models for microarray data. Bioinformatics and Computational Biology Solution Using R and Bioconductor pp. 397-420.
79. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
80. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
81. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, et al. (2001) Minimum information about a microarray experiment (MIAME)- toward standards for microarray data. Nature Genetics 29: 365-371.
82. Edgar R, Domrachev M, Lash AE, (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research 30: 207-210.
83. Kuninaga S, Natsuaki T, Takeuchi T, Yokosawa R, (1997) Sequence variation of the rDNA ITS regions within and between anastomosis groups in Rhizoctonia solani. Current Genetics 32: 237-243.
84. Kasajima I, Ide Y, Ohkama-Ohtsu N, Hayashi H, Yoneyama T, et al. (2004) A protocol for rapid DNA extraction from Arabidopsis thaliana for PCR analysis. Plant Molecular Biology Reporter 22: 49-52.