Dissection of two soybean QTL conferring partial resistance to Phytophthora sojae through sequence and gene expression analysis

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Wang, Hehe ^a   Wijeratne, Asela ^b   Wijeratne, Saranga ^b   Lee, Sungwoo ^a   Taylor, Christopher G ^a   St Martin, Steven K ^a   McHale, Leah ^a   Dorrance, Anne E ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Gene expression; P. sojae; qRT PCR; QTL; Sequencing; SNP; Soybean

Indexed keywords

ALCOHOL DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE 3;

ARTICLE; CELL DEATH; CELL STRUCTURE; CHROMOSOME 19; CONTROLLED STUDY; CULTIVAR IDENTIFICATION; EXON; GENE EXPRESSION; GENE FUNCTION; GENE MAPPING; HAPLOTYPE; INTRON; MICROARRAY ANALYSIS; NONHUMAN; PHYTOPHTHORA; PHYTOPHTHORA SOJAE; PLANT GENETICS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; QUANTITATIVE TRAIT LOCUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SOYBEAN; UBIQUITINATION; UNTRANSLATED REGION; UPREGULATION;

CHROMOSOMES, PLANT; GENE EXPRESSION REGULATION, PLANT; HAPLOTYPES; HOST-PARASITE INTERACTIONS; PHYTOPHTHORA; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SEQUENCE ANALYSIS, DNA; SOYBEANS; TRANSCRIPTION FACTORS; UBIQUITINATION;

GLYCINE MAX; PHYTOPHTHORA SOJAE;

EID: 84865312945     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-428     Document Type: Article

References (87)

1. Grau CR, Dorrance AE, Bond J, Russin JS: Fungal Diseases. In Soybeans: Improvement, Production and Uses. Edited by Boerma HR, Specht JE. Madison, WI: American Society of Agronomy; Crop Science Society of America; Soil Science Society of America; 2004.
2. Schmitthenner AF: Problems and progress in control of Phytophthora root rot of soybean. Plant Dis 1985, 69:362-368.
3. Enkerli K, Hahn MG, Mims CW: Ultrastructure of compatible and incompatible interactions of soybean roots infected with the plant pathogenic oomycete Phytophthora sojae. Can J Bot 1997, 75:1493-1508.
4. Mideros S: Study of incomplete resistance to Phytophthora sojae in soybean, MSc Thesis.: The Ohio State University, Plant Pathology; 2006.
5. Ranathunge K, Thomas RH, Fang X, Peterson CA, Gijzen M, Bernards MA: Soybean root suberin and partial resistance to root rot caused by Phytophthora sojae. Phytopathology 2008, 98:1179-1189.
6. Burnham KD, Dorrance AE, Van Toai TT, St Martin SK: Quantitative trait loci for partial resistance to Phytophthora sojae in soybean. Crop Sci 2003, 43:1610-1617.
7. Han Y, Teng W, Yu K, Poysa V, Anderson T, Qiu L, Lightfoot DA, Li W: Mapping QTL tolerance to Phytophthora root rot in soybean using microsatellite and RAPD/SCAR derived markers. Euphytica 2008, 162:231-239.
8. Li X, Han Y, Teng W, Zhang S, Yu K, Poysa V, Anderson T, Ding J, Li W: Pyramided QTL underlying tolerance to Phytophthora root rot in megaenvironments from soybean cultivars Conrad and Hefeng 25. Theor Appl Genet 2010, 121:651-658.
9. Tucker DM, Saghai Maroof MA, Mideros S, Skoneczka JA, Nabati DA, Buss GR, Hoeschele I, Tyler BM, St Martin SK, Dorrance AE: Mapping quantitative trait loci for partial resistance to Phytophthora sojae in a soybean interspecific cross. Crop Sci 2010, 50:628-635.
10. Wang H, Waller L, Tripathy S, St Martin SK, Zhou L, Krampis K, Tucker DM, Mao Y, Hoeschele I, Saghai Maroof MA, Tyler BM, Dorrance AE: Analysis of genes underlying soybean quantitative trait loci conferring partial resistance to Phytophthora sojae. The Plant Genome 2010, 3:23-40.
11. Wang H, St Martin SK, Dorrance AE: Comparison of phenotypic methods and yield contributions of QTL for partial resistance to Phytophthora sojae in soybean. Crop Sci 2012, 52:609-622.
12. Weng C, Yu K, Anderson TR, Poysa V: A quantitative trait locus influencing tolerance to Phytophthora root rot in the soybean cultivar Conrad. Euphytica 2007, 158:81-86.
13. Wu X, Zhou B, Zhao J, Guo N, Zhang B, Yang F, Chen S, Gai J, Xing H: Identification of quantitative trait loci for partial resistance to Phytophthora sojae in soybean. Plant Breeding 2011, 130:144-149.
14. Kou Y, Wang S: Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 2010, 13:181-185.
15. St Clair DA: Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopathol 2010, 48:247-268.
16. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ: Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 2009, 14:1360-1385.
17. Young ND: QTL mapping and quantitative disease resistance in plants. Annu Rev Phytopathol 1996, 34:479-501.
18. Vega-Sáncheza ME, Redinbaugh MG, Costanzo S, Dorrance AE: Spatial and temporal expression analysis of defense-related genes in soybean cultivars with different levels of partial resistance to Phytophthora sojae. Physiol Mol Plant Pathol 2005, 66:175-182.
19. Thomas R, Fang X, Ranathunge K, Anderson TR, Peterson CA, Bernards MA: Soybean root suberin: anatomical distribution, chemical composition, and relationship to partial resistance to Phytophthora sojae. Plant Physiol 2007, 144:299-311.
20. Tyler BM, Jiang RHY, Zhou L, Tripathy S, Dou D, Torto-Alalibo T, Li H, Mao Y, Liu B, Vega-Sanchez M, Mideros SX, Hanlon R, Smith BM, Krampis K, Ye K, St Martin S, Dorrance AE, Hoeschele I, Saghai Maroof MA: Functional genomics and bioinformatics of the Phytophthora sojae-soybean interaction. In Genomics of Disease. Edited by Gustafson JP, Taylor J, Stacey G. New York: Springer; 2007.
21. Waller L, Zhou L, Mideros SX, Tripathy S, Mao Y, Hanlon R, Torto Alalibo T, St Martin SK, Saghai Maroof MA, Hoeschele I, Dorrance AE, Tyler BM: Transcriptionl profiling of potential regulatory factors modulating defense mechanisms in soybean under P. sojae infection. In The 8th International Conference on Systems Biology: 1-6 Oct. 2007. Long Beach, California; 2007:H45.
22. Zhou L, Mideros S, Bao L, Hanlon R, Arredondo FD, Tripathy S, Krampis K, Jerauld A, Evans C, St Martin SK, Saghai Maroof MA, Hoeschele I, Dorrance AE, Tyler BM: Infection and genotype remodel the entire soybean transcriptome. BMC Genomics 2009, 10:49.
23. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, et al: Genome sequence of the paleopolyploid soybean. Nature 2010, 463:178-183.
24. Fukuoka S, Okuno K: QTL analysis and mapping of pi21, a recessive gene for field resistance to rice blast in Japanese upland rice. Theor Appl Genet 2001, 103:185-190.
25. Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi A, Hirochika H, Okuno K, Yano M: Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 2009, 325:998-1001.
26. Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J: A kinase START gene confers temperature dependent resistance to wheat stripe rust. Science 2009, 323:1357-1360.
27. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B: A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 2009, 323:1360-1363.
28. Spielmeyer W, Singh RP, McFadden H, Wellings CR, Huerta-Espino J, Kong X, Appels R, Lagudah ES: Fine scale genetic and physical mapping using interstitial deletion mutants of Lr34/Yr18: a disease resistance locus effective against multiple pathogens in wheat. Theor Appl Genet 2008, 116:481-490.
29. Stroup WW: Why mixed models in applications of mixed models in agriculture and related disciplines. Baton Rouge, LA: Southern Coop Ser Bull. Louisiana Agricultural Experiment Station; 1989.
30. Demirbas A, Rector BG, Lohnes DG, Fioritto RJ, Graef GL, Cregan PB, Shoemaker RC, Specht JE: Simple sequence repeat markers linked to the soybean Rps genes for Phytophthora resistance. Crop Sci 2001, 41:1220-1222.
31. Sandhu D, Gao H, Cianzio S, Bhattacharyya MK: Deletion of a disease resistance nucleotide-binding-site leucine-rich-repeat-like sequence is associated with the loss of the Phytophthora resistance gene Rps4 in soybean. Genetics 2004, 168:2157-2167.
32. Grant D, Nelson RT, Cannon SB, Shoemaker RC: SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 2010, 38: D843-D846.
33. Hyten DL, Choi IY, Song Q, Specht JE, Carter TE, Shoemaker RC, Hwang EY, Matukumalli LK, Cregan PB: A high density integrated genetic linkage map of soybean and the development of a 1536 universal soy linkage panel for quantitative trait locus mapping. Crop Sci 2010, 50:960-968.
34. Deschamps S, la Rota M, Ratashak JP, Biddle P, Thureen D, Farmer A, Luck S, Beatty M, Nagasawa N, Michael L, Llaca V, Sakai H, May G, Lightner J, Campbell MA: Rapid genome-wide single nucleotide polymorphism discovery in soybean and rice via deep resequencing of reduced representation libraries with the Illumina genome analyzer. The Plant Genome 2009, 3:53-68.
35. Choi IY, Hyten DL, Matukumalli LK, Song Q, Chaky JM, Quigley CV, Chase K, Lark KG, Reiter RS, Yoon MS, Hwang EY, Yi SI, Young ND, Shoemaker RC, Van Tassel CP, Specht JE, Cregan PB: A soybean transcript map: Gene distribution, haplotype and single-nucleotide polymorphism analysis. Genetics 2007, 176:685-696.
36. Zhu YL, Song QJ, Hyten DL, Van Tassell CP, Matukumalli LK, Grimm DR, Hyatt SM, Fickus EW, Young ND, Cregan PB: Single-nucleotide polymorphisms in soybean. Genetics 2003, 163:1123-1134.
37. Gaudet M, Fara AG, Sabatti M, Kuzminsky E, Mugnozza GS: Single-reaction for SNP genotyping on agarose gel by allele-specific PCR in black poplar (Populus nigra L.). Plant Mol Biol Rep 2007, 25:1-9.
38. Dodd AN, Kudla J, Sanders D: The language of calcium signaling. Annu Rev Plant Biol 2010, 61:593-620.
39. Guo Y, Xiong L, Song CP, Gong D, Halfter U, Zhu JK: A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. Dev Cell 2002, 3:233-244.
40. Pandey GK, Cheong YH, Kim KN, Grant JJ, Li L, Hung W, D'Angelo C, Weinl S, Kudla J, Luan S: The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 2004, 16:1912-1924.
41. McDonald KL, Cahill DM: Influence of abscisic acid and the abscisic acid biosynthesis inhibitor, norflurazon, on interactions between Phytophthora sojae and soybean (Glycine max). Eur J Plant Pathol 1999, 105:651-658.
42. Ward EW, Cahill DM, Bhattacharyya MK: Abscisic acid suppression of phenylalanine ammonialyase activity and mRNA, and resistance of soybeans to Phytophthora megasperma f.sp. glycinea. Plant Physiol 1989, 91:23-27.
43. Kovtun Y, Chiu W, Tena G, Sheen J: Functional analysis of oxidative stressactivated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 2000, 97:2940-2945.
44. Suarez Rodriguez MS, Petersen M, Mundy J: Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 2010, 61:621-649.
45. Diaz M, Achkor H, Titarenko E, Martinez MC: The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS (Fed Eur Bio-chem Soc) Lett 2003, 543:136-139.
46. Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ: A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA 2005, 102:8054-8059.
47. Moreau M, Lindermayr C, Durner J, Klessig DF: NO synthesis and signaling in plants-where do we stand? Physiol Plant 2010, 138:372-383.
48. Rusterucci C, Espunya MC, Diaz M, Chabannes M, Martinez MC: Snitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 2007, 143:1282-1292.
49. Pearce G, Moura DS, Stratmann J, Ryan CA: RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci USA 2001, 98:12843-12847.
50. Gupta S, Chakraborti D, Sengupta A, Basu D, Das S: Primary metabolism of chickpea is the initial target of wound inducing early sensed Fusarium oxysporum f. sp. ciceri Race I. PLoS One 2010, 5:e9030.
51. Haruta M, Constabel CP: Rapid Alkalinization Factors in Poplar Cell Cultures. Peptide Isolation, cDNA Cloning, and Differential Expression in Leaves and Methyl Jasmonate-Treated Cells. Plant Physiol 2003, 131:814-823.
52. Tian ZD, Liu J, Wang BL, Xie CH: Screening and expression analysis of Phytophthora infestans induced genes in potato leaves with horzontal resistance. Plant Cell Rep 2006, 25:1094-1103.
53. Narusaka Y, Narusaka M, Park P, Kubo Y, Hirayama T, Seki M, Shiraishi T, Ishida J, Nakashima M, Enju A, Sakurai T, Satou M, Kobayashi M, Shinozaki K: RCH1, a locus in Arabidopsis that confers resistance to the hemibiotrophic fungal pathogen Colletotrichum higginsianum. Mol Plant Microbe Interact 2004, 17:749-762.
54. Domingo C, Andrés F, Tharreau D, Iglesias DJ, Talón M: Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Mol Plant Microbe Interact 2009, 22:201-210.
55. Kidd BN, Kadoo NY, Dombrecht B, Tekeoglu M, Gardiner DM, Thatcher LF, Aitken EA, Schenk PM, Manners JM, Kazan K: Auxin signaling and transport promote susceptibility to the root-infecting fungal pathogen Fusarium oxysporum in Arabidopsis. Mol Plant Microbe Interact 2011, 24:733-748.
56. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X: Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 2007, 17:1784-1790.
57. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O,Jones JDG: Plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006, 312:436-439.
58. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sweelam N, Schenk PM, Manners JM, Kazan K: MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 2007, 19:2225-2245.
59. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM: Networking by small-molecules hormones in plant immunity. Nat Chem Biol 2009, 5:308-316.
60. Robert-Seilaniantz A, Grant M, Jones JDG: Hormone crosstalk in plant disease and defense: More than just jasmonate salicylate antagonism. Annu Rev Phytopathol 2011, 49:317-343.
61. Minic Z: Physiological roles of plant glycoside hydrolases. Planta 2008, 227:723-740.
62. Smith CJ, Watson CF, Morris PC, Bird CR, Seymour GB, Gray JE, Arnold C, Tucker GA, Schuch W, Harding S, Grierson D: Inheritance and effect on ripening of antisense polygalacturonase genes in transgenic tomatoes. Plant Mol Biol 1990, 14:369-379.
63. Smith CJS, Watson CF, Ray J, Bird CR, Morris PC, Schuch W, Grierson D: Antisense RNA inhibition of polygalacturonase gene expression in transgenic tomatoes. Nature 1998, 334:724-726.
64. Walton JD: Deconstructing the cell wall. Plant Physiol 1994, 104:1113-1118.
65. Herron SR, Benen JAE, Scavetta RD, Visser J, Jurnak F: Structure and function of pectic enzymes: Virulence factors of plant pathogens. Proc Natl Acad Sci USA 2000, 97:8762-8769.
66. Reignault P, Valette-Collet O, Boccara M: The importance of fungal pectinolytic enzymes in plant invasion, host adaptability and symptom type. Eur J Plant Pathol 2008, 120:1-11.
67. Lee YJ, Liu B: Cytoskeletal motors in Arabidopsis: Sixty-one kinesins and seventeen myosins. Plant Physiol 2004, 136:3877-3883.
68. Schmidt SM, Panstruga R: Cytoskeleton functions in plant-microbe interactions. Physiol Mol Plant Pathol 2007, 71:135-148.
69. Chrispeels MJ, Raikhel NV: Lectins, lectin genes and their role in plant defense. Plant Cell 1991, 3:1-9.
70. van Damme EJM, Peumans WJ, Barre A, Rougé P: Plant lectins: A composite of several distinct families of structurally and evolutionary related proteins with diverse biological roles. Crit Rev Plant Sci 1998, 17:575-692.
71. Peumans WJ, van Damme EJM: Lectins as plant defense proteins. Plant Physiol 1995, 109:347-353.
72. Gibson DM, Stack S, Krell K, House J: A comparison of soybean agglutinin in cultivars resistant and susceptible to Phytophthora megasperma var. sojae (race 1). Plant Physiol 1982, 70:560-566.
73. Dannenhoffer JM, Schulz A, Skaggs MI, Bostwick DE, Thompson GA: Expression of the phloem lectin is developmentally linked to vascular differentiation in cucurbits. Planta 1997, 201:405-414.
74. Balachandran S, Xiang Y, Schobert C, Thompson GA, Lucas WJ: Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proc Natl Acad Sci USA 1997, 94:14150-14155.
75. Trujillo M, Shirasu K: Ubiquitination in plant immunity. Curr Opinion in Plant Biol 2010, 13:402-408.
76. Craig A, Ewan R, Mesmar J, Gudipati V, Sadanandom A: E3 ubiquitin ligases and plant innate immunity. J Exp Bot 2009, 60:1123-1132.
77. Lee SJ, Rose JKC: Mediation of the transition from biotrophy to necrotrophy in hemibiotrophic plant pathogens by secreted effector proteins. Plant Signal Behav 2010, 5:769-772.
78. Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH, Leung H, Leach JE: A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice. Plant Physiol 2009, 149:286-296.
79. Dorrance AE, Berry SA, Anderson TR, Meharg C: Isolation, storage, pathotype characterization, and evaluation of resistance for Phytophthora sojae in soybean. Plant Health Progress 2008, 10.1094/PHP-2008-0118-01-DG.
80. Song Q, Jia G, Zhu Y, Grant D, Nelson RT, Hwang EY, Hyten DL, Cregan P: Abundance of SSR motifs and development of candidate polymorphic SSR markers (BARCSOYSSR_1.0) in soybean. Crop Sci 2010, 50:1950-1960.
81. Van Ooijen JW: JoinMapW 4.0, Software for the calculation of genetic linkage maps in experimental populations. The Netherlands: Kyazma B.V, Wageningen; 2006.
82. Van Ooijen JW: MapQTL 5, Software for the mapping of quantitative trait loci in experimental populations. The Netherlands: Kyazma BV, Wageningen; 2004.
83. Churchill GA, Doerge RW: Empirical threshold values for quantitative trait mapping. Genetics 1994, 138:963-971.
84. Calla B, Vuong T, Radwan O, Hartman GL, Clough SJ: Gene expression profiling soybean stem tissue early response to Sclerotinia sclerotiorum and in silico mapping in relation to resistance markers. Plant Genome 2009, 2:149-166.
85. You FM, Huo N, Gu YQ, Luo M, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD: BatchPrimer3: A high throughput web application for PCR and sequencing primer design. BMC Bioinforma 2008, 9:253.
86. Harismendy O, Frazer K: Method for improving sequence coverage uniformity of targeted genomic intervals amplified by LR-PCR using Illumina GA sequencing-by-synthesis technology. Biotechniques 2009, 46:229-231.
87. Pfaffl MW: A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res 2001, 29:e45.