Population-specific gene expression in the plant pathogenic nematode Heterodera glycines exists prior to infection and during the onset of a resistant or susceptible reaction in the roots of the Glycine max genotype Peking

BMC Genomics

Volumn 10, Issue , 2009, Pages

  Klink, Vincent P ^a,b   Hosseini, Parsa ^c   MacDonald, Margaret H ^b   Alkharouf, Nadim W ^c   Matthews, Benjamin F ^b  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c TOWSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE KINASE; CELLULASE; GENE PRODUCT; PROTEIN HGG 20; PROTEIN TN8; PROTIN G20E03; PROTIN G30C02; SERINE PROTEINASE; STEROID REDUCTASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; HELMINTH RNA;

ARTICLE; GENE EXPRESSION; GENE IDENTIFICATION; GENE REPRESSION; GENE TARGETING; GENETIC RESISTANCE; GENETIC SUSCEPTIBILITY; HETERODERA GLYCINES; LARVAL STAGE; MICROARRAY ANALYSIS; NEMATODAL PLANT DISEASE; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT PATHOGEN INTERACTION; PLANT ROOT; SOYBEAN; UNINDEXED SEQUENCE; ANIMAL; CLUSTER ANALYSIS; COMPARATIVE STUDY; DNA MICROARRAY; DNA SEQUENCE; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HOST PARASITE INTERACTION; PARASITOLOGY; PLANT DISEASE; SPECIES DIFFERENCE; TIME;

GLYCINE MAX; HETERODERA GLYCINES;

ANIMALS; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, HELMINTH; HOST-PARASITE INTERACTIONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT DISEASES; PLANT ROOTS; RNA, HELMINTH; SEQUENCE ANALYSIS, DNA; SOYBEANS; SPECIES SPECIFICITY; TIME FACTORS; TYLENCHOIDEA;

EID: 63449090337     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-111     Document Type: Article

References (64)

1. Williamson VM Kumar A Nematode resistance in plants: The battle underground TRENDS in Genetics 2006, 22:396-403. 10.1016/ j.tig.2006.05.003 16723170
2. Klink VP Overall CC Matthews BF Developing a systems biology approach to study disease progression caused by Heterodera glycines in Glycine max Gene Regulation and Systems Biology 2007, 2:17-33.
3. Abad P Gouzy J Aury JM Castagnone-Sereno P Danchin EG Deleury E Perfus-Barbeoch L Anthouard V Artiguenave F Blok VC Caillaud MC Coutinho PM Dasilva C De Luca F Deau F Esquibet M Flutre T Goldstone JV Hamamouch N Hewezi T Jaillon O Jubin C Leonetti P Magliano M Maier TR Markov GV McVeigh P Pesole G Poulain J Robinson-Rechavi M Sallet E Ségurens B Steinbach D Tytgat T Ugarte E van Ghelder C Veronico P Baum TJ Blaxter M Bleve-Zacheo T Davis EL Ewbank JJ Favery B Grenier E Henrissat B Jones JT Laudet V Maule AG Quesneville H Rosso MN Schiex T Smant G Weissenbach J Wincker P Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita Nat Biotechnol 2008, 26:909-15. 10.1038/nbt.1482 18660804
4. Wrather JA Koenning SR Estimates of disease effects on soybean yields in the United States 2003-2005 J Nematology 2006, 38:173-180.
5. Cregan PB Mudge J Fickus EW Marek LF Danesh D Denny R Shoemaker RC Matthews BF Jarvik T Young ND Targeted isolation of simple sequence repeat markers through the use of bacterial artificial chromosomes Theor Appl Genet 1999, 98:919-928. 10.1007/s001220051151
6. Matthews BF Devine TE Weisemann JM Beard HS Lewers KS MacDonald MH Park Y-B Maiti R Lin J-J Kuo J Pedroni MJ Cregan PB Saunders JA Incorporation of sequenced cDNA and genomic markers into the soybean genetic map Crop Sci 2001, 41:516-521.
7. Riggs RD Schmitt DP Optimization of the Heterodera glycines race test procedure J Nematol 1991, 23:149-154. 2619141 19283105
8. Niblack TL Arelli PR Noel GR Opperman CH Orf JH Schmitt DP Shannon JG Tylka GL A revised classification scheme for genetically diverse populations of Heterodera glycines J Nematol 2002, 34:279-288. 2620582 19265945
9. Jenkins WR Taylor DP Plant Nematology Reinhold, New York; 1967.
10. Jung C Wyss U New approaches to control plant parasitic nematodes Applied Microbiology and Biotechnology 1999, 51:439-446. 10.1007/ s002530051414
11. Endo BY Penetration and development of Heterodera glycines in soybean roots and related and related anatomical changes Phytopathology 1964, 54:79-88.
12. Endo BY Histological responses of resistant and susceptible soybean varieties, and backcross progeny to entry development of Heterodera glycines Phytopathology 1965, 55:375-381.
13. Endo B Synthesis of nucleic acids at infection sites of soybean roots parasitized by Heterodera glycines Phytopathology 1971, 61:395-399.
14. Endo BY Ultrastructure of initial responses of resistant and susceptible soybean roots to infection by Heterodera glycines Rev Nematol 1991, 14:73-94.
15. Endo BY Veech JA Morphology and histochemistry of soybean roots infected with Heterodera glycines Phytopathology 1970, 60:1493-1498.
16. Gipson I Kim KS Riggs RD An ultrastructural study of syncytium development in soybean roots infected with Heterodera glycines Phytopathol 1971, 61:347-353.
17. Jones MGK Northcote DH Nematode-induced syncytium-a multinucleate transfer cell J Cell Sci 1972, 10:789-809. 5038416
18. Riggs RD Kim KS Gipson I Ultrastructural changes in Peking soybeans infected with Heterodera glycines Phytopathology 1973, 63:76-84.
19. Klink VP Overall CC Alkharouf N MacDonald MH Matthews BF A comparative microarray analysis of an incompatible and compatible disease response by soybean (Glycine max) to soybean cyst nematode (Heterodera glycines) infection Planta 2007, 226:1423-1447. 10.1007/s00425-007-0581-4 17653570
20. Klink VP Overall CC Alkharouf N MacDonald MH Matthews BF Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean roots infected by soybean cyst nematode (Heterodera glycines) Planta 2007, 226:1389-409. 10.1007/s00425-007-0578-z 17668236
21. Jones MGK Dropkin VH Cellular alterations induced in soybean roots by three endoparasitic nematodes Physiol Plant Path 1975, 5:119-124. 10.1016/0048-4059(75)90015-6
22. Jones MGK Dropkin VH Scanning electron microscopy of syncytial transfer cells induced in roots by cyst-nematodes Physiol Plant Path 1975, 7:259-263. 10.1016/0048-4059(75)90030-2
23. Kim YH Riggs RD Kim KS Structural changes associated with resistance of soybean to Heterodera glycines J Nematol 1987, 19(2):177-187. 19290127
24. Atibalentja N Bekal S Domier LL Niblack TL Noel GR Lambert KN A genetic linkage map of the soybean cyst nematode Heterodera glycines Mol Gen Genomics 2005, 273:273-281. 10.1007/s00438-005-1125-x
25. Bekal S Craig JP Hudson ME Niblack TL Domier LL Lambert KN Genomic DNA sequence comparison between two inbred soybean cyst nematode biotypes facilitated by massively parallel 454 micro-bead sequencing Mol Genet Genomics 2008, 279:535-43. 10.1007/s00438-008-0331-8 18324416
26. Niblack TL Heinz RD Smith GS Donald PA Distribution, density, and diversity of Heterodera glycines in Missouri J Nematol 1993, 25:880-886. 2619456 19279857
27. Puthoff DP Nettleton D Rodermel SR Baum TJ Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles The Plant Journal 2003, 33:911-921. 10.1046/j.1365-313X.2003.01677.x 12609032
28. Khan R Alkharouf N Beard HS MacDonald M Chouikha I Meyer S Grefenstette J Knap H Matthews BF Resistance mechanisms in soybean: Gene expression profile at an early stage of soybean cyst nematode invasion J Nematology 2004, 36:241-248.
29. Jammes F Lecomte P de Almeida-Engler J Bitton F Martin-Magniette ML Renou JP Abad P Favery B Genome-wide expression profiling of the host response to root knot nematode infection in Arabidopsis Plant J 2005, 44:447-458. 10.1111/j.1365-313X.2005.02532.x 16236154
30. Alkharouf NW Klink VP Chouikha IB Beard HS MacDonald MH Meyer S Knap HT Khan R Matthews BF Timecourse microarray analyses reveals global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode) Planta 2006, 224:838-852. 10.1007/s00425-006-0270-8 16575592
31. Ithal N Recknor J Nettleston D Hearne L Maier T Baum TJ Mitchum MG Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean Molecular Plant-Microbe Interactions 2007, 20:293-305. 10.1094/MPMI-20-3-0293 17378432
32. Bhattarai KK Li Q Liu Y Dinesh-Kumar SP Kaloshian I The MI-1 mediated pest resistance requires Hsp90 and Sgt1 Plant Physiol 2007, 144:312-23. 1913790 17351050 10.1104/pp.107.097246
33. Hill AA Hunter CP Tsung BT Tucker-Kellogg G Brown EL Genomic analysis of gene expression in C. elegans Science 2000, 290:809-812. 10.1126/ science.290.5492.809 11052945
34. Kim SK Lund J Kiraly M Duke K Jiang M Stuart JM Eizinger A Wylie BN Davidson GS A gene expression map for Caenorhabditis elegans Science 2001, 293:2087-2092. 10.1126/science.1061603 11557892
35. Gao B Allen R Maier T Davis EL Baum TJ Hussey RS Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode Heterodera glycines Mol Plant Microbe Interact 2001, 14:1247-1254. 10.1094/MPMI.2001.14.10.1247 11605964
36. Gao B Allen R Maier T Davis EL Baum TJ Hussey RS The parasitome of the phytonematode Heterodera glycines Mol Plant Microbe Interact 2003, 16:720-726. 10.1094/MPMI.2003.16.8.720 12906116
37. Sardanelli S Kenworthy WJ Soil Moisture Control and Direct Seeding for Bioassay of Heterodera glycines on Soybean J Nematol 1997, 29(4S):625-634. 19274262 2619819
38. Klink VP Alkharouf N MacDonald M Matthews BF Laser capture microdissection (LCM) and analysis of Glycine max (soybean) syncytial cells formed by the soybean cyst nematode Heterodera glycines Plant Mol Biol 2005, 59:969-983. 10.1007/s11103-005-2416-7
39. Alkharouf N Khan R Matthews BF Analysis of expressed sequence tags from roots of resistant soybean infected by the soybean cyst nematode Genome 2004, 47:380-388. 15060591
40. Matthews B MacDonald MH Thai VK Tucker ML Molecular characterization of argenine kinase in the soybean cyst nematode (Heterodera glycines) Journal of Nematology 2003, 35:252-258. 2620652 19262758
41. Mujer CV Andrews DL Manhart JR Pierce SK Rumpho ME Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica Proc Natl Acad Sci USA 1996, 93:12333-12338. 37991 8901581 10.1073/pnas.93.22.12333
42. Altschul SF Madden TL Schaffer AA Zhang J Zhang Z Miller W Lipman DJ Gapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res 1997, 25:3389-3402. 146917 9254694 10.1093/ nar/25.17.3389
43. Tusher VG Tibshirani R Chu G Significance analysis of microarrays applied to the ionizing radiation response PNAS 2001, 98:5116-5121. 33173 11309499 10.1073/pnas.091062498
44. The Gene Ontology Consortium The Gene Ontology (GO) database and informatics resource Nucleic Acids Res 2004, 32:D258-D261. 308770 14681407 10.1093/nar/gkh036
45. MacQueen JB "Some Methods for classification and Analysis of Multivariate Observations Proceedings of 5-th Berkeley Symposium on Mathematical Statistics and Probability" Berkeley, University of California Press 1967, 1:281-297.
46. Klink VP Martins VE Overall CC Alkharouf N MacDonald MH Matthews BF A decline in transcript abundance for Heterodera glycines homologs of Caenorhabditis elegans uncoordinated genes accompanies its sedentary parasitic phase BMC Developmental Biology 2007, 7:35. 1867819 17445261 10.1186/1471-213X-7-35
47. Dieterich C Clifton SW Schuster LN Chinwalla A Delehaunty K Dinkelacker I Fulton L Fulton R Godfrey J Minx P Mitreva M Roeseler W Tian H Witte H Yang SP Wilson RK Sommer RJ The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism Nat Genet 2008, 40:1193-8. 10.1038/ng.227 18806794
48. Tytgat T De Meutter J Vanholme B Claeys M Verreijdt L Gheysen G Coomans A Development and pharyngeal gland activities of Heterodera schachtii infecting Arabidopsis thaliana roots Nematology 2002, 4:899-908. 10.1163/ 156854102321122511
49. Paschinger K Gutternigg M Rendiæ D Wilson IB Carbohydr Res. 2008 The N-glycosylation pattern of Caenorhabditis elegans 2008, 343:2041-2049.
50. Neveu C Jaubert S Abad P Castagnone-Sereno P A set of genes differentially expressed between avirulent and virulent Meloidogyne incognita near-isogenic lines encode secreted proteins Mol Plant Microbe Interact 2003, 16:1077-84. 10.1094/MPMI.2003.16.12.1077 14651341
51. Dubreuil G Magliano M Deleury E Abad P Rosso MN Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism New Phytol 2007, 176:426-36. 10.1111/j.1469-8137.2007.02181.x 17692078
52. Taroni F Verderio E Dworzak F Willems PJ Cavadini P DiDonato S Identification of a common mutation in the carnitine palmitoyltransferase II gene in familial recurrent myoglobinuria patients Nat Genet 1993, 4:314-320. 10.1038/ng0793-314 8358442
53. Tytgat T Vanholme B De Meutter J Claeys M Couvreur M Vanhoutte I Gheysen G Van Criekinge W Borgonie G Coomans A Gheysen G A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic cyst nematodes Mol Plant Microbe Interact 2004, 17:846-852. 10.1094/MPMI.2004.17.8.846 15305605
54. Chitwood DG Lusby WR Metabolism of plant sterols by nematodes Lipids 1990, 26:619-627. 10.1007/BF02536426
55. Lilley CJ Urwin PE Atkinson HJ McPherson MJ Characterization of cDNAs encoding serine proteinases from the soybean cyst nematode Heterodera glycines Mol Biochem Parasitol 89:195-207. 10.1016/S0166-6851(97)00116-3 9364965
56. Atkinson HJ Opportunities for improved control of plant parasitic nematodes via plant biotechnology Opportunities for Molecular Biology in Crop Production British Crop Protection Council, Nottingham, UK Beadle DJ, Bishop DHL, Copping LG, Dixon GK, Holloman DW 1993:257-266.
57. Fire A Xu S Montgomery MK Kostas SA Driver SE Mello CC Potent and specific genetic interference by double-stranded RNA in Caenohrabditis elegans Nature 1998, 391:806-811. 10.1038/35888 9486653
58. Alkharouf N Klink VP Matthews BF Identification of Heterodera glycines (soybean cyst nematode [SCN]) DNA sequences with high similarity to those of Caenorhabditis elegans having lethal mutant or RNAi phenotypes Exp Parasitol 2007, 115:247-258. 10.1016/j.exppara.2006.09.009 17052709
59. Urwin PE Lilley CJ Atkinson HJ Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference Mol Plant Microbe Interact 2002, 15:747-752. 10.1094/MPMI.2002.15.8.747 12182331
60. Bakhetia M Urwin PE Atkinson HJ QPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host Mol Plant Microbe Interact 2007, 20:306-312. 10.1094/MPMI-20-3-0306 17378433
61. Bakhetia M Urwin PE Atkinson HJ Characterisation by RNAi of pioneer genes expressed in the dorsal pharyngeal gland cell of Heterodera glycines and the effects of combinatorial RNAi Int J Parasitol 2008, 38:1589-1597. 10.1016/j.ijpara.2008.05.003
62. Ghedin E Wang S Spiro D Caler E Zhao Q Crabtree J Allen JE Delcher AL Guiliano DB Miranda-Saavedra D Angiuoli SV Creasy T Amedeo P Haas B El-Sayed NM Wortman JR Feldblyum T Tallon L Schatz M Shumway M Koo H Salzberg SL Schobel S Pertea M Pop M White O Barton GJ Carlow CK Crawford MJ Daub J Dimmic MW Estes CF Foster JM Ganatra M Gregory WF Johnson NM Jin J Komuniecki R Korf I Kumar S Laney S Li BW Li W Lindblom TH Lustigman S Ma D Maina CV Martin DM McCarter JP McReynolds L Mitreva M Nutman TB Parkinson J Peregrín-Alvarez JM Poole C Ren Q Saunders L Sluder AE Smith K Stanke M Unnasch TR Ware J Wei AD Weil G Williams DJ Zhang Y Williams SA Fraser-Liggett C Slatko B Blaxter ML Scott AL Draft genome of the filarial nematode parasite Brugia malayi Science 2007, 317:1756-60. 2613796 17885136 10.1126/science.1145406
63. Klink VP Kim K-H Martins VE MacDonald MH Beard HS Alkharouf NW Park S-C Matthews BF A correlation between host-mediated expression of parasite genes as tandem inverted repeats and abrogation of the formation of female Heterodera glycines cysts during infection of Glycine max. Planta
64. Alkharouf N Matthews BF SGMD: The soybean genomics and microarray database Nucleic Acids Research 2004, 32:D398-D400. 308860 14681442 10.1093/nar/gkh126