A correlation between host-mediated expression of parasite genes as tandem inverted repeats and abrogation of development of female Heterodera glycines cyst formation during infection of Glycine max

Planta

Volumn 230, Issue 1, 2009, Pages 53-71

  Klink, Vincent P ^a   Kim, Kyung Hwan ^b,c   Martins, Veronica ^b   MacDonald, Margaret H ^b   Beard, Hunter S ^b   Alkharouf, Nadim W ^d   Lee, Seong Kon ^b,c   Park, Soo Chul ^b,c   Matthews, Benjamin F ^b  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c National Institute of Animal Science   (South Korea)

^d TOWSON UNIVERSITY   (United States)

Author keywords

EGFP; RNAi

Indexed keywords

ANIMAL; ARTICLE; BIOLOGICAL MODEL; DNA MICROARRAY; FEMALE; GENE; GENE EXPRESSION PROFILING; GENE VECTOR; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; INVERTED REPEAT; LIFE CYCLE; MALE; NEMATODE; PARASITOLOGY; PHYSIOLOGY; SOYBEAN; TRANSGENIC PLANT;

ANIMALS; FEMALE; GENE EXPRESSION PROFILING; GENES, HELMINTH; GENETIC VECTORS; HOST-PARASITE INTERACTIONS; INVERTED REPEAT SEQUENCES; LIFE CYCLE STAGES; MALE; MODELS, BIOLOGICAL; NEMATODA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANTS, GENETICALLY MODIFIED; SOYBEANS;

CAENORHABDITIS ELEGANS; GLYCINE MAX; HETERODERA GLYCINES;

EID: 67349229122     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-009-0926-2     Document Type: Article

References (65)

1. P Abad J Gouzy JM Aury P Castagnone-Sereno EG Danchin E Deleury L Perfus-Barbeoch V Anthouard F Artiguenave VC Blok MC Caillaud PM Coutinho C Dasilva F De Luca F Deau M Esquibet T Flutre JV Goldstone N Hamamouch T Hewezi O Jaillon C Jubin P Leonetti M Magliano TR Maier GV Markov P McVeigh G Pesole J Poulain M Robinson-Rechavi E Sallet B Ségurens D Steinbach T Tytgat E Ugarte C van Ghelder P Veronico TJ Baum M Blaxter T Bleve-Zacheo EL Davis JJ Ewbank B Favery E Grenier B Henrissat JT Jones V Laudet AG Maule H Quesneville MN Rosso T Schiex G Smant J Weissenbach P Wincker 2008 Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita Nat Biotechnol 26 909 915
2. N Alkharouf BF Matthews 2004 SGMD: the soybean genomics and microarray database Nucleic Acids Res 32 D398 D400
3. NW Alkharouf VP Klink IB Chouikha HS Beard MH MacDonald S Meyer HT Knap R Khan BF Matthews 2006 Timecourse microarray analyses reveals global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode) Planta 224 838 852 (Pubitemid 44286375)
4. N Alkharouf VP Klink BF Matthews 2007 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 115 247 258 (Pubitemid 44828062)
5. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389 3402 (Pubitemid 27359211)
6. M Bakhetia PE Urwin HJ Atkinson 2007 QPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host Mol Plant Microbe Interact 20 306 312 (Pubitemid 46281157)
7. Bakhetia M, Urwin PE, Atkinson HJ (2008) 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 (in press)
8. P Bernard M Couturier 1991 The 41 carboxy-terminal residues of the Mini-F plasmid ccdA protein are sufficient to antagonize the killer activity of the CcdB protein Mol Gen Genet 226 297 304
9. DJ Bertioli M Smoker PR Burrows 1999 Nematode-responsive activity of the cauliflower mosaic virus 35S promoter and its subdomains Mol Plant Microbe Interact 12 189 196 (Pubitemid 29103116)
10. S Bhattacharyya N Dey IB Maiti 2002 Analysis of cis-sequence of subgenomic transcript promoter from the Figwort mosaic virus and comparison of promoter activity with the cauliflower mosaic virus promoters in monocot and dicot cells Virus Res 90 47 62 (Pubitemid 35375823)
11. DW Byrd Jr T Kirkpatrick KR Barker 1983 An improved technique for clearing and staining plant tissue for detection of nematodes J Nematol 15 142 143
12. R Collier B Fuchs N Walter W Kevin Lutke CG Taylor 2005 Ex vitro composite plants: an inexpensive, rapid method for root biology Plant J 43 449 457 (Pubitemid 41577011)
13. P Corish C Tyler-Smith 1999 Attenuation of green fluorescent protein half-life in mammalian cells Protein Eng 12 1035 1040 (Pubitemid 30011478)
14. NCA de Ruijter J Verhees W van Leeuwen AR van der Krol 2003 Evaluation and comparison of the GUS, LUC and GFP reporter system for gene expression studies in plants Plant Biol 5 103 115 (Pubitemid 36725786)
15. T Elmayan M Tepfer 1995 Evaluation in tobacco of the organ specificity and strength of the rolD promoter, domain A of the 35S promoter and the 35S2 promoter Transgenic Res 4 388 396
16. BY Endo 1964 Penetration and development of Heterodera glycines in soybean roots and related and related anatomical changes Phytopathology 54 79 88
17. BY Endo 1965 Histological responses of resistant and susceptible soybean varieties, and backcross progeny to entry development of Heterodera glycines Phytopathology 55 375 381
18. BY Endo 1971 Synthesis of nucleic acids at infection sites of soybean roots parasitized by Heterodera glycines Phytopathology 61 395 399
19. BY Endo 1991 Ultrastructure of initial responses of resistant and susceptible soybean roots to infection by Heterodera glycines Rev Nematol 14 73 94
20. BY Endo JA Veech 1970 Morphology and histochemistry of soybean roots infected with Heterodera glycines Phytopathology 60 1493 1498
21. MA Escobar EL Civerolo KR Summerfelt AM Dandekar 2001 RNAi-mediated oncogene silencing confers resistance to crown gall tumorigenesis Proc Natl Acad Sci USA 98 13437 13442 (Pubitemid 33051381)
22. A Fire S Xu MK Montgomery SA Kostas SE Driver CC Mello 1998 Potent and specific genetic interference by double-stranded RNA in Caenohrabditis elegans Nature 391 806 811 (Pubitemid 28099681)
23. I Gipson KS Kim RD Riggs 1971 An ultrastructural study of syncytium development in soybean roots infected with Heterodera glycines Phytopathology 61 347 353
24. AM Golden JM Epps RD Riggs LA Duclos JA Fox RL Bernard 1970 Terminology and identity of infraspecific forms of the soybean cyst nematode (Heterodera glycines) Plant Dis Rep 54 544 546
25. JH Haas LW Moore W Ream S Manulis 1995 Universal PCR primers for detection of phytopathogenic Agrobacterium strains Appl Environ Microbiol 61 2879 2884
26. J Haseloff KR Siemering DC Prasher S Hodge 1997 Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly Proc Natl Acad Sci USA 94 2122 2127 (Pubitemid 27136838)
27. C Helliwell P Waterhouse 2003 Constructs and methods for high-throughput gene silencing in plants Methods 30 289 295 (Pubitemid 36793965)
28. R Hofgen L Willmitzer 1988 Storage of competent cells for Agrobacterium transformation Nucleic Acids Res 16 9877
29. X Huang PS Springer I Kaloshian 2003 Expression of the Arabidopsis MCM gene PROLIFERA during root-knot and cyst nematode infection Phytopathology 93 35 41 (Pubitemid 36029205)
30. G Huang R Allen EL Davis TJ Baum RS Hussey 2006 Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene Proc Natl Acad Sci USA 103 14302 14306 (Pubitemid 44484745)
31. RA Jefferson TA Kavanagh MW Bevan 1987 GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants EMBO J 6 3901 3907
32. Jenkins WR, Taylor DP (1967) Plant nematology. Reinhold, New York
33. MGK Jones VH Dropkin 1975 Scanning electron microscopy of syncytial transfer cells induced in roots by cyst-nematode Physiol Plant Pathol 7 259 263
34. MGK Jones DH Northcote 1972 Nematode-induced syncytium-a multinucleate transfer cell J Cell Sci 10 789 809
35. C Jung U Wyss 1999 New approaches to control plant parasitic nematodes Appl Microbiol Biotechnol 51 439 446 (Pubitemid 29210563)
36. YH Kim RD Riggs KS Kim 1987 Structural changes associated with resistance of soybean to Heterodera glycines J Nematol 19 177 187
37. VP Klink SM Wolniak 2000 The efficacy of RNAi in the study of the plant cytoskeleton J Plant Growth Regul 19 371 384 (Pubitemid 32550383)
38. VP Klink SM Wolniak 2001 Centrin is necessary for the formation of the motile apparatus in spermatids of Marsilea Mol Biol Cell 12 761 776 (Pubitemid 33052027)
39. VP Klink CC Overall N Alkharouf MH MacDonald BF Matthews 2007 A comparative microarray analysis of an incompatible and compatible disease response by soybean (Glycine max) to soybean cyst nematode (Heterodera glycines) infection Planta 226 1423 1447 (Pubitemid 47573284)
40. VP Klink CC Overall N Alkharouf M MacDonald BF Matthews 2007 Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean (Glycine max) roots infected by the soybean cyst nematode (Heterodera glycines) Planta 226 1389 1409 (Pubitemid 47573281)
41. VP Klink VE Martins NW Alkharouf CC Overall MH MacDonald BF Matthews 2007 A decline in transcript abundance for Heterodera glycines homologs of Caenorhabditis elegans uncoordinated genes accompanies its sedentary parasitic phase BMC Dev Biol 7 35
42. VP Klink CC Overall BF Matthews 2007 Developing a systems biology approach to study disease progression caused by Heterodera glycines in Glycine max Gene Regul Syst Biol 2 17 33
43. VP Klink MH MacDonald VE Martins S-C Park K-H Kim S-H Baek BF Matthews 2008 MiniMax, a new diminutive Glycine max variety, with a rapid life cycle, embryogenic potential and transformation capabilities Plant Cell Tissue Organ Cult 92 183 195
44. ES Kovaleva SA Subbotin EP Masler DJ Chitwood 2005 Molecular characterization of the actin gene from cyst nematodes in comparison with those from other nematodes Comp Parasitol 2005 72 39 49 (Pubitemid 40225111)
45. B Matthews MH MacDonald VK Thai ML Tucker 2003 Molecular characterization of arginine kinase in the soybean cyst nematode (Heterodera glycines) J Nematol 35 252 258 (Pubitemid 37518963)
46. BF Matthews K Pilitt VP Klink 2004 Molecular characterization of a soybean cyst nematode (Heterodera glycines) homolog of unc-87 J Nematol 36 457 465 (Pubitemid 40697440)
47. pro-1 cDNA Can J Bot 85 437 441 (Pubitemid 47262435)
48. T Murashige F Skoog 1962 A revised medium for rapid growth and bio-assays with tobacco tissue cultures Physiol Plant 15 473 497
49. C Napoli C Lemieux R Jorgensen 1990 Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans Plant Cell 2 279 289 (Pubitemid 120029588)
50. TL Niblack PR Arelli GR Noel CH Opperman JH Orf DP Schmitt JG Shannon GL Tylka 2002 A revised classification scheme for genetically diverse populations of Heterodera glycines J Nematol 34 279 288 (Pubitemid 36413092)
51. RD Riggs DP Schmitt 1991 Optimization of the Heterodera glycines race test procedure J Nematol 23 149 154
52. RD Riggs KS Kim I Gipson 1973 Ultrastructural changes in Peking soybeans infected with Heterodera glycines Phytopathology 63 76 84
53. MA Salmon L Van Melderen P Bernard M Couturier 1994 The antidote and autoregulatory functions of the F plasmid ccdA protein: a genetic and biochemical survey Mol Gen Genet 244 530 538 (Pubitemid 24281467)
54. S Sardanelli WJ Kenworthy 1997 Soil moisture control and direct seeding for bioassay of Heterodera glycines on soybean J Nematol (Suppl) 29 625 634
55. AS Sindhu TR Maier MG Mitchum RS Hussey EL Davis TJ Baum 2009 Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success J Exp Bot 60 1 315 324
56. RM Steeves TC Todd JS Essig HN Trick 2006 Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines reproduction Funct Plant Biol 33 991 999 (Pubitemid 44665361)
57. D Tepfer 1984 Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype Cell 37 959 967 (Pubitemid 15139289)
58. The Gene Ontology Consortium 2004 The Gene Ontology (GO) database and informatics resource Nucleic Acids Res 32 D258 D261
59. L Timmons A Fire 1998 Specific interference by ingested dsRNA Nature 395 854 (Pubitemid 28503418)
60. PE Urwin CJ Lilley HJ Atkinson 2002 Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference Mol Plant Microbe Interact 15 747 752
61. D Weigel JH Ahn MA Blázquez JO Borevitz SK Christensen C Fankhauser C Ferrándiz I Kardailsky EJ Malancharuvil MM Neff JT Nguyen S Sato ZY Wang Y Xia RA Dixon MJ Harrison CJ Lamb MF Yanofsky J Chory 2000 Activation tagging in Arabidopsis Plant Physiol 122 1003 1013 (Pubitemid 30221380)
62. SV Wesley CA Helliwell NA Smith MB Wang DT Rouse Q Liu PS Gooding SP Singh D Abbott PA Stoutjesdijk SP Robinson AP Gleave AG Green PM Waterhouse 2001 Construct design for efficient, effective and high-throughput gene silencing in plants Plant J 27 581 590 (Pubitemid 32961462)
63. FF White BH Taylor GA Huffman MP Gordon EW Nester 1985 Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes J Bacteriol 164 33 44 (Pubitemid 16223486)
64. VM Williamson RS Hussey 1996 Nematode pathogenesis and resistance in plants Plant Cell 8 10 1735 1745 (Pubitemid 27012401)
65. JA Wrather SR Koenning 2006 Estimates of disease effects on soybean yields in the United States 2003-2005 J Nematol 38 173 180 (Pubitemid 44594598)