Biphasic gene expression changes elicited by Phakopsora pachyrhizi in soybean correlate with fungal penetration and haustoria formation

Plant Physiology

Volumn 157, Issue 1, 2011, Pages 355-371

  Schneider, Katherine T ^a   van de Mortel, Martijn ^b   Bancroft, Timothy J ^c   Braun, Edward ^b   Nettleton, Dan ^c   Nelson, Rex T ^d   Frederick, Reid D ^a   Baum, Thomas J ^b   Graham, Michelle A ^b,d   Whitham, Steven A ^b  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c Department of Statistics Center for Statistics and Applications in Forensic Evidence Iowa State University 2438 Osborn Dr Ames   (United States)

^d U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE MAX; PHAKOPSORA PACHYRHIZI;

EID: 80052396086     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.181149     Document Type: Article

References (84)

1. 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: 3389-3402
2. Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, et al (2004) UniProt: the Universal Protein knowledgebase. Nucleic Acids Res 32: D115-D119
3. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al (2000) Gene Ontology: tool for the unification of biology. Nat Genet 25: 25-29
4. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1994) Current Protocols in Molecular Biology. John Wiley & Sons, Hoboken, NJ
5. Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69: 473-488
6. Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45: 399-436
7. Berardini TZ, Mundodi S, Reiser L, Huala E, Garcia-Hernandez M, Zhang P, Mueller LA, Yoon J, Doyle A, Lander G, et al (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 135: 745-755
8. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33: 1597-1613
9. Boerjan W, Ralph J, Baucher M(2003) Lignin biosynthesis. Annu Rev Plant Biol 54: 519-546
10. Bolton MD (2009) Primary metabolism and plant defense: fuel for the fire. Mol Plant Microbe Interact 22: 487-497
11. Bonde MR, Melching JS, Bromfield KR (1976) Histology of susceptpathogen relationship between Glycine max and Phakopsora pachyrhizi, cause of soybean rust. Phytopathology 66: 1290-1294
12. Bonde MR, Nester SE, Austin CN, Stone CL, Frederick RD, Hartman GL, Miles MR (2006) Evaluation of virulence of Phakopsora pachyrhizi and P. meibomiae isolates. Plant Dis 90: 708-716
13. Bonferroni CE (1935) Il calcolo delle assicurazioni su gruppi di teste. In Studi in Onore del Professore Salvatore Ortu Carboni. Rome, pp 13-60
14. Bromfield KR (1984) Soybean Rust. Monograph No. 11. American Phytopathological Society, St. Paul, MN
15. Bromfield KR, Hartwig EE (1980) Resistance to soybean rust and mode of inheritance. Crop Sci 20: 254-255
16. Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG (2006)Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18: 243-256
17. Cheng YW, Chan KL (1968) The breeding of 'Tainung 3' soybean. J Taiwan Agric Res 17: 30-35
18. Choi JJ, Alkharouf NW, Schneider KT, Matthews BF, Frederick RD (2008) Expression patterns in soybean resistant to Phakopsora pachyrhizi reveal the importance of peroxidases and lipoxygenases. Funct Integr Genomics 8: 341-359
19. Coram TE, Settles ML, Chen X (2008) Transcriptome analysis of hightemperature adult-plant resistance conditioned by Yr39 during the wheat-Puccinia striiformis f. sp. tritici interaction. Mol Plant Pathol 9: 479-493
20. Davies PJ (2010) The plant hormones: their nature, occurrence, and functions. In PJ Davies, ed, Plant Hormones. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 1-15
21. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20: 1453-1454
22. Deverall BJ, Keogh RC, McLeod S (1977) Responses of soybean to infection by, and to germination fluids from urediniospores of Phakopsora pachyrhizi. T rans Br Mycol Soc 69: 411-415
23. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-forgene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103: 8888-8893
24. Dra ̌ghici S, Khatri P, Martins RP, Ostermeier GC, Krawetz SA (2003) Global functional profiling of gene expression. Genomics 81: 98-104
25. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210
26. Ellis JG, Dodds PN, Lawrence GJ (2007a) Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu Rev Phytopathol 45: 289-306
27. Ellis JG, Dodds PN, Lawrence GJ (2007b) The role of secreted proteins in diseases of plants caused by rust, powdery mildew and smut fungi. Curr Opin Microbiol 10: 326-331
28. Fehr WR, Caviness CE (1977) Stages of Soybean Development. Special Report 80. Iowa State University of Science and Technology, Iowa Agriculture and Home Economics Experiment Station, Ames, IA
29. Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265-276
30. Fisher RA (1966) The Design of Experiments, Ed 8. Oliver and Boyd, Edinburgh
31. Garcia A, Calvo ES, de Souza Kiihl RA, Harada A, Hiromoto DM, Vieira LG (2008) Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor Appl Genet 117: 545-553
32. Goellner K, Loehrer M, Langenbach C, Conrath U, Koch E, Schaffrath U (2010) Phakopsora pachyrhizi, the causal agent of Asian soybean rust. Mol Plant Pathol 11: 169-177
33. Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277-284
34. Hartwig EE (1986) Identification of a fourth major gene conferring resistance to soybean rust. Crop Sci 26: 1135-1136
35. Hartwig EE, Bromfield KR (1983) Relationships among three genes conferring specific resistance to rust in soybeans. Crop Sci 23: 237-239
36. He K, Guo AY, Gao G, Zhu QH, Liu XC, Zhang H, Chen X, Gu X, Luo J (2010) Computational identification of plant transcription factors and the construction of the PlantT FDB database. Methods Mol Biol 674: 351-368
37. Heath MC (1984) Relationship between heat-induced fungal death and plant necrosis in compatible and incompatible interactions involving the bean and cowpea rust fungi. Phytopathology 74: 1370-1376
38. Hidayat OO, Somaatmadja S (1977) Screening of soybean breeding lines for resistance to soybean rust (Phakopsora pachyrhizi Sydow). Soybean Rust Newsl. 1: 9-22
39. Hoefle C, Loehrer M, Schaffrath U, Frank M, Schultheiss H, Hückelhoven R (2009) Transgenic suppression of cell death limits penetration success of the soybean rust fungus Phakopsora pachyrhizi into epidermal cells of barley. Phytopathology 99: 220-226
40. Hyten DL, Smith JR, Frederick RD, Tucker ML, Song Q, Cregan PB (2009) Bulked segregant analysis using the GoldenGate assay to locate the Rpp3 locus that confers resistance to soybean rust in soybean. Crop Sci 49: 265-271
41. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444: 323-329
42. Keane PJ, Limongiello N, Warren MA (1988) A modified method for clearing and staining leaf-infecting fungi in whole leaves. Australas Plant Pathol 17: 37-38
43. Keogh RC, Deverall BJ, McLeod S (1980) Comparison of histological and physiological-responses to Phakopsora pachyrhizi in resistant and susceptible soybean. Trans Br Mycol Soc 74: 329-333
44. Koch E, Ebrahim-Nesbat F, Hoppe HH (1983) Light and electron-microscopic studies on the development of soybean rust (Phakopsora pachyrhizi Syd) in susceptible soybean leaves. Phytopathol Z 106: 302-320
45. Kumudini S, Godoy CV, Board JE, Omielan J, Tollenaar M (2008a) Mechanisms involved in soybean rust-induced yield reduction. Crop Sci 48: 2334-2342
46. Kumudini S, Prior E, Omielan J, Tollenaar M(2008b) Impact of Phakopsora pachyrhizi infection on soybean leaf photosynthesis and radiation absorption. Crop Sci 48: 2343-2350
47. La Camera S, Gouzerh G, Dhondt S, Hoffmann L, Fritig B, Legrand M, Heitz T (2004) Metabolic reprogramming in plant innate immunity: the contributions of phenylpropanoid and oxylipin pathways. Immunol Rev 198: 267-284
48. Loehrer M, Langenbach C, Goellner K, Conrath U, Schaffrath U (2008) Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. Mol Plant Microbe Interact 21: 1421-1430
49. Mackey D, McFall AJ (2006) MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol Microbiol 61: 1365-1371
50. Marchetti MA, Uecker FA, Bromfield KR (1975) Uredial development of Phakopsora pachyrhizi in soybeans. Phytopathology 65: 822-823
51. McLean RJ (1979) Histological studies of resistance to soybean rust, Phakopsora pachyrhizi Syd. Aust J Agric Res 30: 77-84
52. McLean RJ, Byth DE (1980) Inheritance of resistance to rust (Phakopsora pachyrhizi) in soybeans. Aust J Agric Res 31: 951-956
53. Meindl T, Boller T, Felix G (2000) The bacterial elicitor flagellin activates its receptor in tomato cells according to the address-message concept. Plant Cell 12: 1783-1794
54. Melching JS, Bromfield KR, Kingsolver CH (1983) The plant pathogen containment facility at Frederick, Maryland. Plant Dis 67: 717-722
55. Monteros MJ, Missaoui AM, Phillips DV, Walker DR, Boerma HR (2007) Mapping and confirmation of the 'Hyuuga' red-brown lesion resistance gene for Asian soybean rust. Crop Sci 47: 829-834
56. Nettleton D (2006) A discussion of statistical methods for design and analysis of microarray experiments for plant scientists. Plant Cell 18: 2112-2121
57. Ogle HJ, Byth DE, McLean R (1979) Effect of rust (Phakopsora pachyrhizi) on soybean yield and quality in south-eastern Queensland. Aust J Agric Res 30: 883-893
58. Panthee DR, Marois JJ, Wright DL, Narvaéz D, Yuan JS, Stewart CN Jr (2009) Differential expression of genes in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) is soybean growth stage-specific. Theor Appl Genet 118: 359-370
59. Panthee DR, Yuan JS, Wright DL, Marois JJ, Mailhot D, Stewart CN Jr (2007) Gene expression analysis in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) in an early growth stage. Funct Integr Genomics 7: 291-301
60. Patil VS, Wuike RV, Thakare CS, Chirame BB (1997) Viability of uredospores of Phakopsora pachyrhizi Syd. at different storage conditions. J Maharashtra Agric Univ 22: 260-261
61. Pua AR, Ilag LL (1980) Ingress and pathogenic development of Phakopsora pachyrhizi Syd. in soybean. Philipp Agric 63: 9-14
62. Rafiqi M, Gan PH, Ravensdale M, Lawrence GJ, Ellis JG, Jones DA, Hardham AR, Dodds PN (2010) Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of thepathogen. Plant Cell 22: 2017-2032
63. Ravensdale M, Nemri A, Thrall PH, Ellis JG, Dodds PN (2011) Coevolutionary interactions between host resistance and pathogen effector genes in flax rust disease. Mol Plant Pathol 12: 93-102
64. Rinaldi C, Kohler A, Frey P, Duchaussoy F, Ningre N, Couloux A, Wincker P, Le Thiec D, Fluch S, Martin F, et al (2007) Transcript profiling of poplar leaves upon infection with compatible and incompatible strains of the foliar rust Melampsora larici-populina. Plant Physiol 144: 347-366
65. Saldanha AJ (2004) Java TreeView: extensible visualization of microarray data. Bioinformatics 20: 3246-3248
66. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183
67. Schulze-Lefert P, Vogel J (2000) Closing the ranks to attack by powdery mildew. Trends Plant Sci 5: 343-348
68. Singh BB, Thapliyal PN (1977) Breeding for resistance to soybean rust in India. In RE Ford, JB Sinclair, eds, Rust of Soybean: The Problem and Research Needs. INTSOY Series No. 12. College of Agriculture, University of Illinois at Urbana-Champaign, Urbana, IL, pp 62-65
69. Soria-Guerra RE, Rosales-Mendoza S, Chang S, Haudenshield JS, Padmanaban A, Rodriguez-Zas S, Hartman GL, Ghabrial SA, Korban SS (2010a) Transcriptome analysis of resistant and susceptible genotypes of Glycine tomentella during Phakopsora pachyrhizi infection reveals novel rust resistance genes. Theor Appl Genet 120: 1315-1333
70. Soria-Guerra RE, Rosales-Mendoza S, Chang S, Haudenshield JS, Zheng D, Rao SS, Hartman GL, Ghabrial SA, Korban SS (2010b) Identifying differentially expressed genes in leaves of Glycine tomentella in the presence of the fungal pathogen Phakopsora pachyrhizi. Planta 232: 1181-1189
71. Staples RC (2000) Research on the rust fungi during the twentieth century. Annu Rev Phytopathol 38: 49-69
72. Staples RC (2001) Nutrients for a rust fungus: the role of haustoria. Trends Plant Sci 6: 496-498
73. Stergiopoulos I, de Wit PJ (2009) Fungal effector proteins. Annu Rev Phytopathol 47: 233-263
74. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440-9445
75. Tremblay A, Hosseini P, Alkharouf N, Li S, Matthews BF (2010) Transcriptome analysis of a compatible response by Glycine tomentella to Phakopsora pachyrhizi infection. Plant Sci 179: 183-193
76. Trevaskis B, Wandrey M, Colebatch G, Udvardi MK (2002) The soybean GmN6L gene encodes a late nodulin expressed in the infected zone of nitrogen-fixing nodules. Mol Plant Microbe Interact 15: 630-636
77. van de Mortel M, Recknor JC, Graham MA, Nettleton D, Dittman JD, Nelson RT, Godoy CV, Abdelnoor RV, Almeida Á MR, Baum TJ, et al (2007) Distinct biphasic mRNA changes in response to Asian soybean rust infection. Mol Plant Microbe Interact 20: 887-899
78. Van Verk MC, Gatz C, Linthorst HJM (2009) Transcriptional regulation of plant defense responses. Adv Bot Res 51: 397-437
79. Voegele RT, Mendgen K (2003) Rust haustoria: nutrient uptake and beyond. New Phytol 159: 93-100
80. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008a) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20: 471-481
81. Wan J, Zhang XC, Stacey G (2008b) Chitin signaling and plant disease resistance. Plant Signal Behav 3: 831-833
82. Wang Z, Libault M, Joshi T, Valliyodan B, Nguyen HT, Xu D, Stacey G, Cheng J (2010) Soy DB: a knowledge database of soybean transcription factors. BMC Plant Biol 10: 14
83. Wise RP, Caldo RA, Hong L, Shen L, Cannon EK, Dickerson JA (2007) BarleyBase/PLEXdb: a unified expression profiling database for plants and plant pathogens. Methods Mol Biol 406: 347-363
84. Zhang LY, Bai MY, Wu J, Zhu JY, Wang H, Zhang Z, Wang W, Sun Y, Zhao J, Sun X, et al (2009) Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21: 3767-3780