The 185/333 Gene Family Is a Rapidly Diversifying Host-Defense Gene Cluster in the Purple Sea Urchin Strongylocentrotus purpuratus

Journal of Molecular Biology

Volumn 379, Issue 4, 2008, Pages 912-928

  Buckley, K M ^a   Munshaw, S ^b   Kepler, T B ^b   Smith, L C ^a  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

echinoderm; innate immunology; invertebrate; molecular evolution; repeats

Indexed keywords

ARTICLE; GENE CLUSTER; GENE STRUCTURE; HOST RESISTANCE; IMMUNE SYSTEM; INVERTEBRATE; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; STRONGYLOCENTROTUS;

ECHINODERMATA; ECHINOIDEA; INVERTEBRATA; STRONGYLOCENTROTUS PURPURATUS;

EID: 44149084190     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.04.037     Document Type: Article

References (59)

1. M.F. Flajnik L. Du Pasquier Evolution of innate and adaptive immunity: can we draw a line? Trends Immunol. 25 2004 640 644
2. C.M. Adema L.A. Hertel R.D. Miller E.S. Loker A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection Proc. Natl Acad. Sci. USA 94 1997 8691 8696
3. J.P. Cannon R.N. Haire G.W. Litman Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate Nat. Immunol. 3 2002 1200 1207
4. D. Destoumieux P. Bulet D. Loew A. Van Dorsselaer J. Rodriguez E. Bachere Penaeidins, a new family of antimicrobial peptides isolated from the shrimp Penaeus vannamei (Decapoda) J. Biol. Chem. 272 1997 28398 28406
5. L.A. Hertel C.M. Adema E.S. Loker Differential expression of FREP genes in two strains of Biomphalaria glabrata following exposure to the digenetic trematodes Schistosoma mansoni and Echinostoma paraensei Dev. Comp. Immunol. 29 2005 295 303
6. J.D. Jones J.L. Dangl The plant immune system Nature 444 2006 323 329
7. P.M. Leonard C.M. Adema S.M. Zhang E.S. Loker Structure of two FREP genes that combine IgSF and fibrinogen domains, with comments on diversity of the FREP gene family in the snail Biomphalaria glabrata Gene 269 2001 155 165
8. J.M. McDowell S.A. Simon Molecular diversity at the plant–pathogen interface Dev. Comp. Immunol. 32 2008 736 744
9. N.A. O'Leary P.S. Gross Genomic structure and transcriptional regulation of the penaeidin gene family from Litopeneaus vannamei Gene 371 1999 75 83
10. M. Parniske J.D. Jones Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family Proc. Natl Acad. Sci. USA 96 1999 5850 5855
11. S.M. Zhang C.M. Adema T.B. Kepler E.S. Loker Diversification of Ig superfamily genes in an invertebrate Science 305 2004 251 254
12. E. Sodergren G.M. Weinstock E.H. Davidson R.A. Cameron R.A. Gibbs R.C. Angerer The genome of the sea urchin Strongylocentrotus purpuratus Science 314 2006 941 952
13. T. Hibino M.L. Coll C. Messier A.C. Majeske D.P. Terwilliger K.M. Buckley The immune gene repertoire encoded in the purple sea urchin genome Dev. Biol. 300 2006 349 365
14. K.M. Buckley L.C. Smith Extraordinary diversity among members of the large gene family, 185/333 , from the purple sea urchin, Strongylocentrotus purpuratus BMC Mol. Biol. 8 2007 68
15. D.P. Terwilliger K.M. Buckley D. Mehta P.G. Moorjani L.C. Smith Unexpected diversity displayed in cDNAs expressed by the immune cells of the purple sea urchin, Strongylocentrotus purpuratus Physiol. Genomics 26 2006 134 144
16. S.V. Nair H. Del Valle P.S. Gross D.P. Terwilliger L.C. Smith Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate Physiol. Genomics 22 2005 33 47
17. J.P. Rast Z. Pancer E.H. Davidson New approaches towards an understanding of deuterostome immunity Curr. Top. Microbiol. Immunol. 248 2000 3 16
18. D.P. Terwilliger K.M. Buckley V. Brockton N.J. Ritter L.C. Smith Distinctive expression patterns of 185/333 genes in the purple sea urchin, Strongylocentrotus purpuratus : an unexpectedly diverse family of transcripts in response to LPS, beta-1,3-glucan, and dsRNA BMC Mol. Biol. 8 2007 16
19. J.P. Rast L.C. Smith M. Loza-Coll T. Hibino G.W. Litman Genomic insights into the immune system of the sea urchin Science 314 2006 952 956
20. V. Brockton J.H. Henson D.A. Raftos A.J. Majeske Y.O. Kim L.C. Smith Localization and diversity of 185/333 proteins from the purple sea urchin—unexpected protein-size range and protein expression in a new coelomocyte type J. Cell Sci. 121 2008 339 348
21. J.M. Hancock M. Simon Simple sequence repeats in proteins and their significance for network evolution Gene 345 2005 113 118
22. R. Durbin S. Eddy A. Krogh G. Mitchison Biological Sequence Analysis, Probability Models of Proteins and Nucleic Acids 1998 Cambridge University Press Cambridge, UK
23. S. Munshaw T.B. Kepler An information-theoretic method for the treatment of plural ancestry in phylogenetics Mol. Biol. Evol. 2008 10.1093/molbev/msn066
24. E.I. Rogaev Simple human DNA-repeats associated with genomic hypervariability, flanking the genomic retroposons and similar to retroviral sites Nucleic Acids Res. 18 1990 1879 1885
25. J. Majewski J. Ott GT repeats are associated with recombination on human chromosome 22 Genome Res. 10 2000 1108 1114
26. F. Nagawa N. Kishishita K. Shimizu S. Hirose M. Miyoshi J. Nezu Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice Nat. Immunol. 8 2007 206 213
27. M.F. Mickevich J.S. Farris The implications of congruence in Mendida Syst. Zool. 30 1981 351 370
28. G. Siu S.P. Clark Y. Yoshikai M. Malissen Y. Yanagi E. Strauss The human T cell antigen receptor is encoded by variable, diversity, and joining gene segments that rearrange to generate a complete V gene Cell 37 1984 393 401
29. A.P. Rooney H. Piontkivska M. Nei Molecular evolution of the nontandemly repeated genes of the histone 3 multigene family Mol. Biol. Evol. 19 2002 68 75
30. E.G. Bakker C. Toomajian M. Kreitman J. Bergelson A genome-wide survey of R gene polymorphisms in Arabidopsis Plant Cell 18 2006 1803 1818
31. B.C. Meyers A. Kozik A. Griego H. Kuang R.W. Michelmore Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis Plant Cell 15 2003 809 834
32. E. Richly J. Kurth D. Leister Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution Mol. Biol. Evol. 19 2002 76 94
33. R.W. Michelmore B.C. Meyers Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process Genome Res. 8 1998 1113 1130
34. K.E. Hammond-Kosack J.D. Jones Plant disease resistance genes Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 1997 575 607
35. S.H. Hulbert C.A. Webb S.M. Smith Q. Sun Resistance gene complexes: evolution and utilization Annu. Rev. Phytopathol. 39 2001 285 312
36. D. Leister Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene Trends Genet. 20 2004 116 1122
37. B.C. Meyers S. Kaushik R.S. Nandety Evolving disease resistance genes Curr. Opin. Plant. Biol. 8 2005 129 134
38. S.M. Smith A.J. Pryor S.H. Hulbert Allelic and haplotypic diversity at the rp1 rust resistance locus of maize Genetics 167 2004 1939 1947
39. J. Ellis G. Lawrence M. Ayliffe P. Anderson N. Collins J. Finnegan Advances in the molecular genetic analysis of the flax–flax rust interaction Annu. Rev. Phytopathol. 35 1997 271 291
40. W.Y. Song L.Y. Pi G.L. Wang J. Gardner T. Holsten P.C. Ronald Evolution of the rice Xa21 disease resistance gene family Plant Cell 9 1997 1279 1287
41. B.C. Meyers D.B. Chin K.A. Shen S. Sivaramakrishnan D.O. Lavelle Z. Zhang R.W. Michelmore The major resistance gene cluster in lettuce is highly duplicated and spans several megabases Plant Cell 10 1998 1817 1832
42. M. Mondragon-Palomino B.C. Meyers R.W. Michelmore B.S. Gaut Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana Genome Res. 12 2002 1305 1315
43. S.M. Zhang E.S. Loker Representation of an immune responsive gene family encoding fibrinogen-related proteins in the freshwater mollusc Biomphalaria glabrata , an intermediate host for Schistosoma mansoni Gene 341 2004 255 266
44. Y.H. Lee Molecular phylogenies and divergence times of sea urchin species of Strongylocentrotidae, Echinoida Mol. Biol. Evol. 20 2003 1211 1221
45. L.C. Smith Host responses to bacteria: innate immunity in invertebrates M.J. McFall-Ngai B. Henderson E.G. Ruby The Influence of Cooperative Bacteria on Animal Host Biology Advances in Molecular and Cellular Microbiology vol. 10 2005 Cambridge University Press 293 320
46. R. Massana L. Guillou B. Diez C. Pedros-Alio Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean Appl. Environ. Microbiol. 68 2002 4554 4558
47. T.A. Hall BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symp. Ser. 41 1999 95 98
48. R.D. Page TreeView: an application to display phylogenetic trees on personal computers Comput. Appl. Biosci. 12 1996 357 358
49. M.P. Simmons H. Ochoterena Gaps as characters in sequence-based phylogenetic analyses Syst. Biol. 49 2000 369 381
50. N.D. Young J. Healy GapCoder automates the use of indel characters in phylogenetic analysis BMC Bioinf. 4 2003 6
51. R.K. Barth B.S. Kim N.C. Lan T. Hunkapiller N. Sobieck A. Winoto The murine T-cell receptor uses a limited repertoire of expressed V gene segments Nature 316 1985 517 523
52. Goloboff, P., Farris, J. & Nixon, K. C. (2003). TNT: Tree Analysis Using New Technology . Program and documentation available from the authors and at www.zmuc.dk/publnic/phylogeny .
53. J. Felsenstein PHYLIP (Phylogeny Inference Package) Version 3.6 2005 Department of Genome Sciences, University of Washington Seattle, WA distributed by the author
54. D. Posada K.A. Crandall MODELTEST: testing the model of DNA substitution Bioinformatics 14 1998 817 818
55. J.P. Huelsenbeck F. Ronquist MRBAYES: Bayesian inference of phylogenetic trees Bioinformatics 17 2001 754 755
56. K. Bremer The limits of amino acid sequence data in angiosperm phylogenetic reconstruction Evolution 42 1988 795 803
57. K.C. Nixon WinClada Ver. 1.00.08 1999–2002 Nixon K.C. Ithaca, NY, USA
58. R.R. Hudson Properties of a neutral allele model with intragenic recombination Theor. Popul. Biol. 23 1983 183 201
59. W.F. Marzluff S. Sakallah H. Kelkar The sea urchin histone gene complement Dev. Biol. 300 2006 308 320