Timecourse microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode)

Planta

Volumn 224, Issue 4, 2006, Pages 838-852

  Alkharouf, Nadim W ^a,b,c,d   Klink, Vincent P ^a   Chouikha, Imed B ^a,b   Beard, Hunter S ^a   MacDonald, Margaret H ^a   Meyer, Susan ^e   Knap, Halina T ^f   Khan, Rana ^g   Matthews, Benjamin F ^a  

^a Bldg006   (United States)

^b GEORGE MASON UNIVERSITY   (United States)

^c Bldg 142   (United States)

^d BRITISH COLUMBIA CANCER AGENCY   (Canada)

^e AGRICULTURAL RESEARCH SERVICE   (United States)

^f CLEMSON UNIVERSITY   (United States)

^g UNIVERSITY OF MARYLAND UNIVERSITY COLLEGE   (United States)

Author keywords

Gene expression; Glycine max; Heterodera glycines; Laser capture microdissection (LCM); Microarray; OLAP; Soybean cyst nematode

Indexed keywords

ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; HOST PARASITE INTERACTION; METABOLISM; MICROARRAY ANALYSIS; NEMATODE; PARASITOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOYBEAN; TIME;

ANIMALS; GENE EXPRESSION REGULATION, PLANT; HOST-PARASITE RELATIONS; MICROARRAY ANALYSIS; PLANT DISEASES; PLANT ROOTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOYBEANS; TIME FACTORS; TYLENCHOIDEA;

GLYCINE MAX; HETERODERA GLYCINES;

EID: 33747857598     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-006-0270-8     Document Type: Article

References (64)

1. Agrawal GK, Tamogami S, Han O, Iwahashi H, Rakwal R (2004) Rice octadecanoid pathway. Biochem Biophys Res Commun 317:1-15
2. Alkharouf N, Matthews BF (2004) SGMD: the soybean genomics and microarray database. Nucleic Acids Res 32:D398-D400
3. Alkharouf N, Khan R, Matthews BF (2004) Analysis of expressed sequence tags from roots of resistant soybean infected by the soybean cyst nematode. Genome 47:380-388
4. Alkharouf N, Jamison C, Matthews BF (2005) Online analytical processing (OLAP): a fast and effective data mining tool for gene expression databases. J Biomed Biotechnol 2:181-188
5. de Almeida Engler J, De Vleesschauwer V, Burssens S, Celenza JL Jr, Inze D, Van Montagu M, Engler G, Gheysen G (1999) Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell 11:793-808
6. Altschul SF, Madden TL, Schaffer 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
7. Arz MC, Grambow HJ (1994) Polyphosphoinositide phospholipase C and evidence for inositol-phosphate-hydrolysing activities in the plasma-membrane fraction from light-grown wheat (Triticum aestivum L.) leaves. Planta 195:57-62
8. Bilban M, Buehler LK, Head S, Desoye G, Quaranta V (2002) Normalizing DNA microarray data. Curr Issues Mol Biol 4:57-64
9. Cebolla A, Vinardell JM, Kiss E, Olah B, Roudier F, Kondorosi A, Kondorosi E (1999) The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J 18:4476-4484
10. Clark GB, Roux SJ (1995) Annexins of plant cells. Plant Physiol 109:1133-1139
11. Codd EF, Codd SB, Salley CT (1993) Providing OLAP (on-line analytical processing) to user-analysts: an IT mandate. Technical Report, EF Codd & Associates
12. Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21-37
13. Droge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon RA, Lamb C (1997) Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J 16:726-738
14. Durrant WE, Rowland O, Piedras P, Hammond-Kosack KE, Jones JD (2000) cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12:963-977
15. Duyvesteijn RG, van Wijk R, Boer Y, Rep M, Cornelissen BJ, Haring MA (2003) Frp1 is a Fusarium oxysporum F-box protein required for pathogenicity on tomato. Mol Microbiol 57:1051-1063
16. Endo BY (1964) Penetration and development of Heterodera glycines in soybean roots and related anatomical changes. Phytopathology 54:79-88
17. Endo BY (1965) Histological responses of resistant and susceptible soybean varieties, and backcross progeny to entry development of Heterodera glycines. Phytopathology 55:375-381
18. Endo B (1971) Synthesis of nucleic acids at infection sites of soybean roots parasitized by Heterodera glycines. Phytopathology 61:395-399
19. Endo BY (1991) Ultrastructure of initial responses of resistant and susceptible soybean roots to infection by Heterodera glycines. Rev Nematol 14:73-94
20. Foster AJ, Jenkinson JM, Talbot NJ (2003) Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea. EMBO J 22:225-235
21. Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Annu Rev Phytopathol 40:191-219
22. Grundler FMW, Bockenhoff A (1997) Physiology of nematode feeding and feeding sites. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant-nematode interactions. Kluwer, Dordrecht, pp 107-119
23. Hermsmeier D, Mazarei M, Baum TJ (1998) Differential display analysis of the early compatible interaction between soybean and the soybean cyst nematode. Mol Plant Microbe Interact 11(12):1258-1263
24. Heo WD, Lee SH, Kim MC, Kim JC, Chung WS, Chun HJ, Lee KJ, Park CY, Park HC, Choi JY, Cho MJ (1999) Involvement of specific calmodulin isoforms in salicylic acid-independent activation of plant disease resistance responses. Proc Natl Acad Sci USA 96:766-771
25. Hegde P, Qi R, Abernathy K, Gay C, Dharap S, Gaspard R, Hughes JE, Snesrud E, Lee N, Quackenbush J (2000) A concise guide to cDNA microarray analysis. Biotechniques 29:548-556
26. Jammes F, Lecomte P, de Almeida-Engler J, Bitton F, Martin-Magniette ML, Renou JP, Abad P, Favery B (2005) Genomewide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J 44:447-458
27. Jung C, Wyss U (1999) New approaches to control plant parasitic nematodes. Appl Microbiol Biotechnol 51:439-446
28. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889-905
29. Khan R, Alkharouf N, Beard HS, MacDonald M, Chouikha I, Meyer S, Grefenstette J, Knap H, Matthews BF (2004) Resistance mechanisms in soybean: gene expression profile at an early stage of soybean cyst nematode invasion. J Nematol 36:241-248
30. Kiegle E, Moore CA, Haseloff J, Tester MA, Knight MR (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23:267-278
31. 2+-dependent lipid-binding domain. Plant Mol Biol 35:969-972
32. Klink VP, MacDonald M, Alkharouf N, Matthews BF (2005) Laser capture microdissection (LCM) and expression analyses of Glycine max (soybean) syncytium containing root regions formed by the plant pathogen Heterodera glycines (soybean cyst nematode). Plant Mol Biol 59:969-983
33. Lange BM, Wildung MR, McCaskill D, Croteau R (1998) A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc Natl Acad Sci USA 95:2100-2104
34. Laxalt AM, Cassia RO, Sanllorenti PM, Madrid EA, Andreu AB, Daleo GR, Conde RD, Lamattina L (1996) Accumulation of cytosolic glyceraldehydes-3- phosphate dehydrogenase RNA under biological stress conditions and elicitor treatments in potato. Plant Mol Biol 30:961-972
35. Lee SH, Kim JC, Lee MS, Heo WD, Seo HY, Yoon HW, Hong JC, Lee SY, Bahk JD, Hwang I, Cho MJ (1995) Identification of a novel divergent calmodulin isoform from soybean which has differential ability to activate calmodulin-dependent enzymes. J Biol Chem 270:21806-21812
36. Mahalingam R, Wang G, Knap HT (1999) Polygalacturonase and polygalacturonase inhibitor protein: gene isolation and transcription in Glycine max-Heterodera glycines interactions. Mol Plant Microbe Interact. 12:490-498
37. Mujer CV, Andrews DL, Manhart JR, Pierce SK, Rumpho ME (1996) Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proc Natl Acad Sci USA 93:12333-12338
38. Niebel A, Heungens K, Barthels N, Inze C, Van Montagu M, Gheysen G (1995) Characterization of a pathogen-induced potato catalase and its systemic expression upon nematode and bacterial infection. Mol Plant Microbe Interact 8:371-378
39. Niebel A, de Almeida Engler J, Hemerly A, Ferreira P, Inze D, Van Montagu M, Gheysen G (1996) Induction of cdc2a and cyc1At expression in Arabidopsis thaliana during early phases of nematode-induced feeding cell formation. Plant J 10:1037-1043
40. Ongena M, Duby F, Rossignol F, Fauconnier ML, Dommes J, Thonart P (2004) Stimulation of the lipoxygenase pathway is associated with systemic resistance induced in bean by a non-pathogenic Pseudomonas strain. Mole Plant Path Interact 17:1009-1018
41. Oztur ZN, Talame V, Deyholos M, Michalowski CB, Gozukirmizi DW, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551-573
42. Park CY, Heo WD, Yoo JH, Lee JH, Kim MC, Chun HJ, Moon BC, Kim IH, Park HC, Choi MS, Ok HM, Cheong MS, Lee SM, Kim HS, Lee KH, Lim CO, Chung WS, Cho MJ (2004a) Pathogenesis-related gene expression by specific calmodulin isoforms is dependent on NIM1, a key regulator of systemic acquired resistance. Mol Cells 18:207-213
43. Park HC, Kim ML, Kang YH, Jeon JM, Yoo JH, Kim MC, Park CY, Jeong JC, Moon BC, Lee JH, Yoon HW, Lee SH, Chung WS, Lim CO, Lee SY, Hong JC, Cho MJ (2004b) Pathogen- and NaCl-induced expression of the SCaM-4 promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiol 135:2150-2161
44. Potenza C, Thomas SH, Sengupta-Gopalan C (2001) Genes induced during early response to Meloidogyne incognita in roots of resistant and susceptible alfalfa cultivars. Plant Sci 161:289-299
45. Puthoff DP, Nettleton D, Rodermel SR, Baum TJ (2003) Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. Plant J 33:911-921
46. Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707-719
47. Robatzek S, Somssich IE (2001) A new member of the Arabidposis WRKY transcription factor family, AtWRKY6 is associated with both senescence- and defence-related processes. Plant J 28:123-133
48. Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16:1139-1149
49. Ryu SB, Wang X (1996) Activation of phospholipase D and the possible mechanism of activation in wound-induced lipid hydrolysis in castor bean leaves. Biochim Biophys Acta 1303:243-250
50. Seal SN, Schmidt A, Marcus A (1983) Eukaryotic initiation factor 4A is the component that interacts with ATP in protein chain initiation. Proc Natl Acad Sci USA 80:6562-6565
51. Schaffer R, Landgraf J, Acerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13:113-123
52. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinate plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97(21):11655-11660
53. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carcini P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses using a full-length cDNA microarray. Plant Cell 13:61-72
54. Takahashi N, Kuroda H, Kuromori T, Hirayama T, Seki M, Shinozaki K, Shimada H, Matsui M (2004) Expression and interaction analysis of Arabidopsis Skp1-related genes. Plant Cell Physiol 45:83-91
55. The Gene Ontology Consortium (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258-D261
56. Tomkins JP, Mahalingam R, Smith H, Goicoechea JL, Knap HT, Wing RA (1999) A bacterial artificial chromosome library for soybean PI 437654 and identification of clones associated with cyst nematode resistance. Plant Mol Biol 41:25-32
57. Tusher V, Tibshirani R, Chu C (2001) Significance analysis of microarrays applied to ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121
58. Vaghchhipawala Z, Bassuner R, Clayton K, Lewers K, Shoemaker R, Mackenzie S (2001) Modulations in gene expression and mapping of genes associated with cyst nematode infection of soybean. Mol Plant Microbe Interact 14:42-54
59. Vaghchhipawala ZE, Schlueter JA, Shoemaker RC, Mackenzie SA (2004) Soybean FGAM synthase promoters direct ectopic nematode feeding site activity. Genome 47:404-413
60. Van der Eycken W, de Almeida Engler J, Inze D, Montagu M, Gheysen G (1996) A molecular study of root-knot nematode-induced feeding sites. Plant J 9:45-54
61. Vodkin LO, Khanna A, Shealy R, Clough SJ, Gonzalez DO, Philip R, Zabala G, Thibaud-Nissen F, Sidarous M, Stromvik MV, Shoop E, Schmidt C, Retzel E, Erpelding J, Shoemaker RC, Rodriguez-Huete AM, Polacco JC, Coryell V, Keim P, Gong G, Liu L, Pardinas J, Schweitzer P (2004) Microarrays for global expression constructed with a low redundancy set of 27,500 sequenced cDNAs representing an array of developmental stages and physiological conditions of the soybean plant. BMC Genomics 5:73-91
62. Wuarin J, Buck V, Nurse P, Millar JB (2002) Stable association of mitotic cyclin B/Cdc2 to replication origins prevents endoreduplication. Cell 111:419-431
63. Wrather JA, Stienstra WC, Koenning SR (2001) Soybean disease loss estimates for the United States from 1996 to 1998. Can J Plant Pathol 23:122-131
64. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization of cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acid Res 30(4):e15