Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach

Genome Biology

Volumn 4, Issue 6, 2003, Pages

  Scholl, Elizabeth H ^a   Thorne, Jeffrey L ^a   McCarter, James P ^b,c   Bird, David Mck ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Divergence Inc   (United States)

Author keywords

Chorismate Mutase; Codon Adaptation Index; Codon Usage; Glutamine Synthetase; Nematode Gene

Indexed keywords

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BACTERIAL GENE; CAENORHABDITIS ELEGANS; COMPARATIVE STUDY; DROSOPHILA MELANOGASTER; GENE; GENETICS; GENOME; GENOMICS; HORIZONTAL GENE TRANSFER; METHODOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NEMATODE; NEMATODIASIS; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PLANT; PLANT ROOT; RHIZOBIACEAE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; GENES, HELMINTH; GENES, INSECT; GENOME; GENOMICS; MOLECULAR SEQUENCE DATA; NEMATODA; NEMATODE INFECTIONS; PLANT ROOTS; PLANTS; RHIZOBIACEAE; TYLENCHOIDEA;

EID: 0038576862     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2003-4-6-r39     Document Type: Article

References (59)

1. Boucher G, Lambshead PJD: Ecological biodiversity of marine nematodes in samples from temperate, tropical, and deep-sea regions. Conserv Biol. 1994, 9: 1594-1604. 10.1046/j.1523-1739.1995.09061594.x. DOI: 10.1046/j.1523-1739.1995.09061594.x
2. Koenning SR, Overstreet C, Noling JW, Donald PA, Becker JO, Fortnum BA: Survey of crop losses in response to phytoparasitic nematodes in the United States for 1994. J Nematol. 1999, 31: 587-618.
3. Bird DMcK, Koltai H: Plant parasitic nematodes: habitats, hormones, and horizontally-acquired genes. J Plant Growth Regul. 2000, 19: 183-194.
4. Blaxter ML, DeLey P, Garey J, Liu LX, Scheldeman P, Vierstraete A, Vanfletern J, Mackey LY, Dorris M, Frisse LM, et al: A molecular evolutionary framework for the phylum Nematoda. Nature. 1998, 392: 71-75. 10.1038/32160. DOI: 10.1038/32160
5. Jain R, Rivera MC, Lake JA: Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA. 1999, 96: 3801-3806. 10.1073/pnas.96.7.3801. DOI: 10.1073/pnas.96.7.3801
6. Lawrence JG: Gene transfer, speciation, and the evolution of bacterial genomes. Curr Opin Microbiol. 1999, 2: 519-523. 10.1016/S1369-5274(99)00010-7. DOI: 10.1016/S1369-5274(99)00010-7
7. Ochman H, Lawrence JG, Groisman EA: Lateral gene transfer and the nature of bacterial innovation. Nature. 2000, 405: 299-304. 10.1038/35012500. DOI: 10.1038/35012500
8. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, et al: The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science. 2002, 298: 2157-2167. 10.1126/science.1080049. DOI: 10.1126/science.1080049
9. Andersson JO, Sjögren ÅM, Davis LAM, Embley TM, Roger AJ: Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol. 2003, 13: 94-104. 10.1016/S0960-9822(03)00003-4. DOI: 10.1016/S0960-9822(03)00003-4
10. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Aravind L, Mitchell W, Olinger L, Tatusov RL, Zhao Q: Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science. 1998, 282: 754-759. 10.1126/science.282.5389.754. DOI: 10.1126/science.282.5389.754
11. Wolf YI, Aravind L, Koonin EV: Rickettsiae and Chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends Genet. 1999, 15: 173-175. 10.1016/S0168-9525(99)01704-7. DOI: 10.1016/S0168-9525(99)01704-7
12. Royo J, Gimez E, Hueros G: CMP-KDO synthetase: A plant gene borrowed from Gram-negative eubacteria. Trends Genet. 2000, 16: 432-433. 10.1016/S0168-9525(00)02102-8. DOI: 10.1016/S0168-9525(00)02102-8
13. Lange BM, Rujan T, Martin W, Croteau R: Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci USA. 2000, 97: 13172-13177. 10.1073/pnas.240454797. DOI: 10.1073/pnas.240454797
14. International Human Genome Sequencing Consortium: Initial sequencing and analysis of the human genome. Nature. 2001, 409: 860-921. 10.1038/35057062. DOI: 10.1038/35057062
15. Brinkman FSL, Blanchard JL, Cherkasov A, Av-Gay Y, Brunham RC, Fernandez RC, Finlay BB, Otto SP, Ouellette BFF, Keeling PJ, et al: Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the choloroplast. Genome Res. 2002, 12: 1159-1167. 10.1101/gr.341802. DOI: 10.1101/gr.341802
16. Stanhope MJ, Lupas A, Italia MJ, Koretke KK, Volker C, Brown JR: Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature. 2001, 411: 940-944. 10.1038/35082058. DOI: 10.1038/35082058
17. Popeijus H, Overmars H, Jones J, Blok V, Goverse A, Helder J, Schots A, Bakker J, Smant G: Degradation of plant cell walls by a nematode. Nature. 2000, 406: 36-37. 10.1038/35017641. DOI: 10.1038/35017641
18. Smant G, Stokkermans JPWG, Yan Y, De Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, et al: Endogenous cellulases in animals: Isolation of β-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci USA. 1998, 95: 4906-4911. 10.1073/pnas.95.9.4906. DOI: 10.1073/pnas.95.9.4906
19. Yan Y, Smant G, Stokkermans J, Qin L, Helder J, Baum T, Schots A, Davis E: Genomic organization of four β-1,4-endoglucanase genes in plant-parasitic cyst nematodes and its evolutionary implications. Gene. 1998, 220: 61-70. 10.1016/S0378-1119(98)00413-2. DOI: 10.1016/S0378-1119(98)00413-2
20. Lambert KN, Allen KD, Sussex IM: Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol Plant Microbe Interact. 1999, 12: 328-336. DOI: 10.1094/MPMI.1999.12.4.328
21. Jaubert S, Laffaire J-B, Abad P, Rosso M-N: A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Lett. 2002, 522: 109-112. 10.1016/S0014-5793(02)02906-X. DOI: 10.1016/S0014-5793(02)02906-X
22. McCarter JP, Abad P, Jones J, Bird DMcK: Rapid gene discovery in plant parasitic nematodes via expressed sequence tags. Nematology. 2000, 2: 719-731. 10.1163/156854100509574. DOI: 10.1163/156854100509574
23. Veronico P, Jones J, Di Vito M, De Giorgi C: Horizontal transfer of a bacterial gene involved in polyglutamate biosynthesis to the plant-parasitic nematode Meloidogyne artiellia. FEBS Lett. 2001, 508: 470-474. 10.1016/S0014-5793(01)03132-5. DOI: 10.1016/S0014-5793(01)03132-5
24. Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA: Evidence for a clade of nematodes, arthropods and other moulting animals. Nature. 1997, 387: 489-493. 10.1038/387489a0. DOI: 10.1038/387489a0
25. Mallatt J, Winchell CJ: Testing the new animal phylogeny: first use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Mol Biol Evol. 2002, 19: 289-301. DOI: 10.1093/oxfordjournals.molbev.a004082
26. Hedges SB: The origin and evolution of model organisms. Nat Rev Genet. 2002, 3: 838-849. 10.1038/nrg929. DOI: 10.1038/nrg929
27. Blair JE, Ikeo K, Gojobori T, Hedges SB: The evolutionary position of nematodes. BMC Evol Biol. 2002, 2: 7-10.1186/1471-2148-2-7. DOI: 10.1186/1471-2148-2-7
28. McCarter JP, Mitreva MD, Martin J, Dante M, Wylie T, Rao U, Pape D, Bowers Y, Theising B, Murphy C, et al: Analysis and functional classification of transcripts from the root-knot nematode Meloidogyne incognita. Genome Biol. 2003, 4: R26-10.1186/gb-2003-4-4-r26. DOI: 10.1186/gb-2003-4-4-r26
29. McCarter JP, Clifton SW, Bird DMcK, Waterston R: Nematode gene sequences; Update for June 2002. J Nematol. 2002, 34: 71-74.
30. Nematode.net. [http://www.nematode.net]
31. Koltai H, Dhandaydham M, Opperman C, Thomas J, Bird DMcK: Overlapping plant signal transduction pathways induced by a parasitic-nematode and a rhizobial endosymbiont. Mol Plant Microbe Interact. 2001, 14: 1168-1177. DOI: 10.1094/MPMI.2001.14.10.1168
32. Ochman H, Moran NA: Genes lost and genes found: evolution of bacterial pathogensis and symbiosis. Science. 2001, 292: 1096-1098. 10.1126/science.1058543. DOI: 10.1126/science.1058543
33. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, Okura VK, Zhou Y, Chen L, Wood GE, Almedia Jr NF, et al: The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science. 2001, 294: 2317-2323. 10.1126/science.1066804. DOI: 10.1126/science.1066804
34. Ludwig RA: Physiological roles of glutamine synthetase I and II in ammonium assimilation in Rhizobium sp. 32H1. J Bacteriol. 1980, 141: 1209-1216.
35. Turner SL, Young JPW: The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol. 2000, 17: 309-319. DOI: 10.1093/oxfordjournals.molbev.a026311
36. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer ELL: The Pfam protein families database. Nucleic Acids Res. 2002, 30: 276-280. 10.1093/nar/30.1.276. DOI: 10.1093/nar/30.1.276
37. Downie JA, Young JPW: Genome sequencing: the ABC of symbiosis. Nature. 2001, 412: 597-598. 10.1038/35088167. DOI: 10.1038/35088167
38. Van Rhijn P, Vanderleyden J: The Rhizobium-plant symbiosis. Microbiol Rev. 1995, 59: 124-142.
39. Göttfert M: Regulation and function of rhizobial nodulation genes. FEMS Microbiol Rev. 1993, 10: 39-64. DOI: 10.1111/j.1574-6968.1993.tb05863.x
40. Ditt RF, Nester EW, Comai L: Plant gene expression response to Agrobacterium tumefaciens. Proc Natl Acad Sci USA. 2001, 98: 10954-10959. 10.1073/pnas.191383498. DOI: 10.1073/pnas.191383498
41. Ray C, Abbott AG, Hussey RS: Trans-splicing of a Meloidogyne incognita mRNA encoding a putative esophageal gland protein. Mol Biochem Parasitol. 1994, 68: 93-101. 10.1016/0166-6851(94)00153-7. DOI: 10.1016/0166-6851(94)00153-7
42. Lawrence JG, Ochman H: Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol. 1997, 44: 383-397. DOI: 10.1007/PL00006158
43. Capela D, Barloy-Hubler F, Gouzy J, Bothe G, Ampe F, Batut J, Boistard P, Becker A, Boutry M, Cadieu E, et al: Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc Natl Acad Sci USA. 2001, 98: 9877-9882. 10.1073/pnas.161294398. DOI: 10.1073/pnas.161294398
44. Sharp PM, Li W-H: The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987, 15: 1281-1295. DOI: 10.1093/nar/15.3.1281
45. Koski LB, Morton RA, Golding GB: Codon bias and base composition are poor indicators of horizontally transferred genes. Mol Biol Evol. 2001, 18: 404-412. DOI: 10.1093/oxfordjournals.molbev.a003816
46. Sullivan JT, Ronson CW: Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA. 1998, 95: 5145-5149. 10.1073/pnas.95.9.5145. DOI: 10.1073/pnas.95.9.5145
47. Wheeler DL, Church DM, Lash AE, Leipe DD, Madden TL, Pontius JU, Schuler GD, Schriml LM, Tatusova TA, Wagner L, Rapp BA: Database resources of the National Center for Biotechnology Information: 2002 update. Nucleic Acids Res. 2002, 30: 13-16. 10.1093/nar/30.1.13. DOI: 10.1093/nar/30.1.13
48. WU-BLAST. [http://blast.wustl.edu]
49. Rice P, Longden I, Bleasby A: EMBOSS: The European molecular biology open software suite. Trends Genet. 2000, 16: 276-277. 10.1016/S0168-9525(00)02024-2. DOI: 10.1016/S0168-9525(00)02024-2
50. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25: 4876-4882. 10.1093/nar/25.24.4876. DOI: 10.1093/nar/25.24.4876
51. Dayhoff MO: Atlas of Protein Sequence and Structure. Volume 5 Supplement 3. 1978, Washington, DC: National Biomedical Research Foundation
52. Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987, 4: 406-425.
53. Felsenstein J: Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985, 39: 783-791. DOI: 10.2307/2408678
54. Felsenstein J: PHYLIP (Phylogeny Inference Package) version 3.6a2. 1993, Seattle, WA: Department of Genetics, University of Washington
55. Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997, 13: 555-556.
56. Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogeny. Bioinformatics. 2001, 17: 754-755. 10.1093/bioinformatics/17.8.754. DOI: 10.1093/bioinformatics/17.8.754
57. Jones DT, Taylor WR, Thornton JM: The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992, 8: 275-282.
58. Yang Z: Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol. 1994, 39: 306-314. DOI: 10.1007/BF00160154
59. Tandingan-De Ley I, De Ley P, Vierstraete A, Karssen G, Moens M, Vanfleteren J: Phylogenetic analyses of Meloidogyne small subunit rDNA. J Nematol. 2002, 34: 319-327.