Transcriptome analysis of resistant and susceptible genotypes of Glycine tomentella during Phakopsora pachyrhizi infection reveals novel rust resistance genes

Theoretical and Applied Genetics

Volumn 120, Issue 7, 2010, Pages 1315-1333

  Soria Guerra, Ruth Elena ^a   Rosales Mendoza, Sergio ^a,b   Chang, Sungyul ^a   Haudenshield, James S ^a   Padmanaban, Annamalai ^c   Rodriguez Zas, Sandra ^a   Hartman, Glen L ^a,d   Ghabrial, Said A ^c   Korban, Schuyler S ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^c UNIVERSITY OF KENTUCKY   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS PATHWAYS; CELL CYCLE; CELLULAR COMMUNICATION; CELLULAR TRANSPORT; DEFENSE RESPONSE; DIFFERENTIAL EXPRESSIONS; DIFFERENTIALLY EXPRESSED GENE; FALSE DISCOVERY RATE; FLAVONOIDS; FOLIAR DISEASE; GENES CODING; GLUTATHIONES; HEAT SHOCK PROTEIN; LIPOXYGENASES; PHENYLPROPANOID PATHWAYS; PLANT DEFENSE; PLANT METABOLISM; Q-RT-PCR; REVERSE TRANSCRIPTION-POLYMERASE CHAIN REACTION; RUST INFECTIONS; RUST RESISTANCE; RUST RESISTANCE GENES; SOY BEAN RUSTS; TIME POINTS; TRANSCRIPTOME ANALYSIS; TRANSCRIPTOME PROFILING;

BIOCHEMISTRY; PLANTS (BOTANY); POLYMERASE CHAIN REACTION; PROTEINS; TRANSCRIPTION;

GENES;

ARTICLE; BASIDIOMYCETES; CYTOLOGY; DISEASE PREDISPOSITION; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; IMMUNOLOGY; INNATE IMMUNITY; METHODOLOGY; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOYBEAN; UPREGULATION;

BASIDIOMYCOTA; DISEASE SUSCEPTIBILITY; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOTYPE; IMMUNITY, INNATE; PLANT DISEASES; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOYBEANS; UP-REGULATION;

GLYCINE MAX; GLYCINE TOMENTELLA; PHAKOPSORA PACHYRHIZI;

EID: 77953130301     PISSN: 00405752     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00122-009-1258-0     Document Type: Article

References (72)

1. Abbasi PA, Graham MY, Graham TL (2001) Effects of soybean genotype on the glyceollin elicitation competency of cotyledon tissues to Phytophthora sojae glucan elicitors. Physiol Mol Plant Pathol 59: 95-105.
2. Abe M, Hayashi T, Hada K, Kimura M (2008) Identification of cDNAs encoding the WD repeat protein and auxin-regulated protein in Nicotiana glutinosa leaves induced in response to Tobacco Mosaic Virus infection at 25°C. J Fac Agric Kyushu Univ 53: 459-465.
3. Baldridge GD, O'Neill NR, Samac DA (1998) Alfalfa (Medicago sativa L.) resistance to the root-lesion nematode, Pratylenchus penetrans: defense-response gene mRNA and isoflavonoid phytoalexin levels in roots. Plant Mol Biol 38: 999-1010.
4. 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.
5. Bhuiyan NH, Selvaraj G, Wei Y, King J (2009) Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defence in wheat against powdery mildew invasion. J Exp Bot 60: 509-521.
6. Blee E (2002) Impact of phyto-oxylipins in plant defense. Trends Plant Sci 7: 315-322.
7. Bonde MR, Nester SE, Hartman GL, Miles MR, Austin CN, Stone CL, Frederick RD (2006) Evaluation of virulence of Phakopsora pachyrhizi and P. meibomiae isolates. Plant Dis 90: 708-716.
8. Burdon JJ (1988) Major gene resistance to Phakopsora pachyrhizi in Glycine canescens, a wild relative of soybean. Theor Appl Genet 75: 923-928.
9. Chang YC, Nair MG, Nitiss JL (1995) Metabolites of diadzein and genistein and their biological activities. J Nat Prod 58: 1901-1905.
10. Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, Budworth PR, Tao Y, Xie Z, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl JL, Wang X, Zhu T (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14: 559-574.
11. Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129: 661-677.
12. 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.
13. Croft K, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol 101: 13-24.
14. Cui X, Kerr MK, Churchill GA (2003) Transformations for cDNA microarray data. Stat Appl Genet Mol Biol 2: Article 4.
15. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, Beynon J, Marco Y (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. PNAS 99: 2404-2409.
16. Dhawale S, Souciet G, Kuhn DN (1989) Increase of chalcone synthase mRNA in pathogen-inoculated soybeans with race-specific resistance is different in leaves and roots. Plant Physiol 91: 911-916.
17. Dixon RA (1986) The phytoalexin response: elicitation, signaling and control of host gene expression. Biol Rev 61: 239-291.
18. Dixon RA (1999) Isoflavonoids: biochemistry, molecular biology and biological functions. In: Sankawa U (ed) Comprehensive natural products chemistry. Elsevier, Amsterdam, pp 773-823.
19. Dixon RA, Dey PM, Lawton MA, Lamb CJ (1983) Phytoalexin induction in French bean. Intercellular transmission of elicitation in cell suspension cultures and hypocotyl sections of Phaseolus vulgaris. Plant Physiol 71: 251-256.
20. Ebel J, Grisebach H (1988) Defense strategies of soybean against the fungus Phytophthora megasperma f. sp. glycinea: a molecular analysis. Trends Biochem Sci 13: 23-27.
21. Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10: 71-78.
22. Fritig B, Heitz T, Legrand M (1998) Antimicrobial proteins in induced plant defense. Curr Opin Immunol 10: 16-22.
23. Fritzemeier KH, Cretin C, Kombrink E, Rohwer F, Taylor J, Scheel D, Hahlbrock K (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.
24. Garcia A, Calvo ES, Kiihl RAD, Harada A, Hiromoto DM, Vieira LGE (2008) Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor Appl Genet 117: 545-553.
25. Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Interact 19: 711-724.
26. Gasic K, Hernandez A, Korban SS (2004) RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction. Plant Mol Biol Rep 22: 437a-437g.
27. Gonzalez DO, Vodkin LO (2007) Specific elements of the glyoxylate pathway play a significant role in the functional transition of the soybean cotyledon during seedling development. BMC Genomics 8: 468.
28. Hahlbrock K, Scheel D (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40: 347-349.
29. Hartman GL, Wang TC, Hymowitz T (1992) Sources of resistance to soybean rust in perennial Glycine species. Plant Dis 76: 396-399.
30. Hartman GL, Bonde MR, Miles MR, Frederick RD (2004) Variation of Phakopsora pachyrhizi isolates on soybean, pp 440-446 In: Moscardi F, Hoffman-Campo CB, Ferreira Saraiva O, Galerani PR, Kryzanowski FC, Carrao-Panizza MC (eds) Proceedings of VII World Soybean Research Conference, IV International Soybean Processing and Utilization Conference, III Congresso Mundial de Soja (Brazilian Soybean Conference). Emprapa Soybean, Londrina.
31. Hartman GL, Miles MR, Frederick RD (2005) Breeding for resistance to soybean rust. Plant Dis 89: 664-666.
32. Hartwig EE (1995) Resistance to soybean rust. In: Sinclair JB, Hartman GL (eds) Proceedings of the Soybean Rust Workshop, 9-11 August 1995. College of Agricultural, Consumer and Environmental Sciences. National Soybean Research Laboratory, Urbana.
33. Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23: 223-237.
34. Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, Baum TJ, Mitchum MG (2007) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant Microbe Interact 20: 293-305.
35. Jahnen W, Hahlbrock K (1988) Cellular localization of nonhost resistance reactions of parsley (Petroselinum crispum) to fungal infection. Planta 173: 197-204.
36. Jarosz AM, Burdon JJ (1990) Predominance of a single major gene for resistance to Phakopsora pachyrhizi in a population of Glycine argyrea. Heredity 64: 347-353.
37. Killgore E, Heu R (1994) First report of soybean rust in Hawaii. Plant Dis 78: 1216.
38. Koch E, Ebrahim-Nesbat F, Hoppe HH (1983) Light and electronmicroscopic studies on the development of soybean rust (Phakopsora pachyrhizi Syd) in susceptible soybean leaves. Phytopathol Z 106: 302-320.
39. 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.
40. Liu CJ, Deavours BE, Richard SB, Ferrer JL, Blount JW, Huhman D, Dixon RA, Noel JP (2006) Structural basis for dual functionality of isoflavonoid O-methyltransferases in the evolution of plant defense responses. Plant Cell 18: 3656-3669.
41. Lo SC, Hipskind JD, Nicholson RL (1999) cDNA cloning of a sorghum pathogenesis-related protein (PR-10) and differential expression of defense-related genes following inoculation with Cochliobolus heterostrophus or Colletotrichum sublineolum. Mol Plant Microbe Interact 12: 479-489.
42. Lozovaya VV, Lygin AV, Zernova OV, Li S, Hartman GL, Widholm JM (2004) Isoflavonoid accumulation in soybean hairy roots upon treatment with Fusarium solani. Plant Physiol Biochem 42: 671-679.
43. Luo M, Liang XQ, Dang P, Holbrook CC, Bausher MG, Lee RD, Guo BZ (2005) Microarray-based screening of differentially expressed genes in peanut in response to Aspergillus parasiticus infection and drought stress. Plant Sci 169: 695-703.
44. Mentewab A, Cardoza V, Stewart CNJ (2005) Genomic analysis of the response of Arabidopsis thaliana to trinitrotoluene as revealed by cDNA microarrays. Plant Sci 168: 1409-1424.
45. Meyer JD, Silva DC, Yang C, Pedley KF, Zhang C, van de Mortel M, Hill JH, Shoemaker RC, Abdelnoor RV, Whitham SA, Graham MA (2009) Identification and analyses of candidate genes for Rpp4-mediated resistance to asian soybean rust in soybean (Glycine max (L.) Merr.). doi:10.1104/pp.108.134551.
46. 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.
47. Panthee DR, Marois JJ, Wright DL, Narváez 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.
48. Patzoldt ME, Tyagi RK, Hymowitz T, Miles MR, Hartman GL, Frederick RD (2007) Soybean rust resistance derived from Glycine tomentella in amphiploid hybrid lines. Crop Sci 47: 158-161.
49. Rancé I, Fournier J, Esquerré-Tugayé MT (1998) The incompatible interaction between Phytophtora parasitica var. nicotianae race 0 and tobacco is suppressed in transgenic plants expressing antisense lipoxygenase sequences. PNAS 95: 6554-6559.
50. Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59: 143-166.
51. Sanz A, Moreno JI, Castresana C (1998) PIOX, a new pathogeninduced oxygenase with homology to animal cyclooxygenase. Plant Cell 10: 1523-1537.
52. Schilmiller AL, Koo AJK, Howe GA (2007) Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action. Plant Physiol 143: 812-824.
53. Schmelzer E, Borner H, Grisebach H, Ebel J, Hahlbrock K (1984) Phytoalexin synthesis in soybean (Glycine max): similar time courses of mRNA induction in hypocotyls infected with a fungal pathogen and in cell cultures treated with fungal elicitor. FEBS Lett 172: 59-63.
54. Schmelzer E, Kruger-Lebus S, Hahlbrock K (1989) Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. Plant Cell 1: 993-1001.
55. Schneider RW, Hollier CA, Whitman HK, Palm ME, McKemy JM, Hernandez JR, Levy L, DeVries-Paterson R (2005) First report of soybean rust caused by Phakopsorapachyrhizi in the continental United States. Plant Dis 89: 774.
56. Shen H, Chen J, Wang Z, Yang C, Sasaki T, Yamamoto Y, Matsumoto H, Yan X (2006) Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot 57: 1353-1362.
57. Smith BJ, Ko Y, Southey BR, Rodriguez-Zas SL (2007) BEEHIVE-a suite of tools to manage, analyze and interpret honey bee microarray experiments. Workshop on honey bee genomics & biology. Cold Spring Harbor Laboratory, Cold Spring Harbor, May 6-8.
58. Staples RC (2001) Nutrients for a rust fungus-the role of haustoria. Trends Plant Sci 6: 496-498.
59. Sugiyama A, Sekiya J (2005) Homoglutathione confers tolerance to acifluorfen in transgenic tobacco plants expressing soybean homoglutathione synthetase. Plant Cell Physiol 46: 1428-1432.
60. Tijet N, Helvig C, Pinot F, Le Bouquin R, Lesot A, Durst F, Salaün JP, Benveniste I (1998) Functional expression in yeast and characterization of a chlofibrateinducible plant cytochrome-P450 (CYP94A1) involved in cutin monomers biosynthesis. Biochem J 332: 583-589.
61. Tripathi BN, Bhatt I, Dietz KJ (2009) Peroxiredoxins: a less studied component of hydrogen peroxide detoxification in photosynthetic organisms. Protoplasma. doi: 10. 1007/s00709-009-0032-0.
62. USDA (2009) Pest Information Platform for Extension and Education. (Online) Available at http://www.sbrusa.net.
63. van de Mortel M, Recknor JC, Graham MA, Nettleton D, Dittman JD, Nelson RT, Godoy CV, Abdelnoor RV, Almeida AM, Baum TJ, Whitham SA (2007) Distinct biphasic mRNA changes in response to Asian soybean rust infection. Mol Plant Microbe Interact 20: 887-899.
64. Voegele RT, Mendgen K (2003) Rust haustoria: nutrient uptake and beyond. New Phytol 159: 93-100.
65. Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126: 485-493.
66. Wolfinger RD, Gibson G, Wolfinger ED, Bennett L, Hamadeh H, Bushel P, Afshari C, Paules RS (2001) Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 8: 625-637.
67. Yang XB (1995) Assessment and management of the risk of soybean rust. In: Sinclair JB, Hartman GL (eds) Proceedings of the soybean rust workshop, 9-11 August 1995. National Soybean Research Laboratory, Urbana.
68. Yang PZ, Chen CH, Wang ZP, Fan BF, Chen ZX (1999) A pathogen- and salicylic acid-induced WRKY DNA-binding activity recognizes the elicitor response element of the tobacco class I chitinase gene promoter. Plant J 18: 141-149.
69. Zabala G, Zou J, Tuteja J, Gonzalez DO, Clough SJ, Vodkin LO (2006) Transcriptome changes in the phenylpropanoid pathway of Glycine max in response to Pseudomonas syringae infection. BMC Plant Biol 6: 26.
70. Zhang Y, Wang L (2005) The WRKY transcription factor superfamily-its origin in eukaryotes and expansion in plants. BMC Evol Biol 5: 1.
71. Zierold U, Scholz U, Schweizer P (2005) Transcriptome analysis of mlo-mediated resistance in the epidermis of barley. Mol Plant Pathol 6: 139-151.
72. Zou J, Rodriguez-Zas S, Aldea M, Li M, Zhu J, Gonzalez DO, Vodkin LO, DeLucia E, Clough SJ (2005) Expression profiling soybean response to Pseudomonas syringae reveals new defense-related genes and rapid HR-specific downregulation of photosynthesis. Mol Plant Microb Interact 18: 1161-1174.