The complex hybrid origins of the root knot nematodes revealed through comparative genomics

PeerJ

Volumn 2014, Issue 1, 2014, Pages

  Lunt, David H ^a   Kumar, Sujai ^b   Koutsovoulos, Georgios ^b   Blaxter, Mark L ^b  

^a UNIVERSITY OF HULL   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Comparative genomics; Genome sequencing; Hybrid speciation; Meloidogyne floridensis; Meloidogyne hapla; Meloidogyne incognita; Phylogenomics

Indexed keywords

ARTICLE; DUPLICATE GENE; FEMALE; GENE DOSAGE; GENE SEQUENCE; GENETIC ANALYSIS; MELOIDOGYNE; MELOIDOGYNE FLORIDENSIS; MELOIDOGYNE HAPLA; MELOIDOGYNE INCOGNITA; NONHUMAN; PHYLOGENOMICS; PHYLOGENY; PREDICTION; SEQUENCE ALIGNMENT;

EID: 84903828669     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.356     Document Type: Article

References (78)

1. Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EGJ, 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. 2008. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 268:909-915 DOI 10.1038/nbt.1482.
2. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R, Butlin RK, Dieckmann U, EroukhmanoffF, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-Rodriguez P, Möst M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, Väinölä R, Wolf JBW, Zinner D. 2013. Hybridization and speciation. Journal of Evolutionary Biology 262:229-246 DOI 10.1111/j.1420-9101.2012.02599.x.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 2153:403-410 DOI 10.1016/S0022-2836(05)80360-2.
4. Arnold ML. 1997. Natural hybridization and evolution. New York: Oxford University Press.
5. Avise JC. 2008. Clonality: the genetics, ecology, and evolution of sexual abstinence in vertebrate animals. Oxford University Press.
6. Barton NH. 2001. The role of hybridization in evolution. Molecular Ecology 103:551-568 DOI 10.1046/j.1365-294x.2001.01216.x.
7. Bell G. 1982. The masterpiece of nature: the evolution and genetics of sexuality. Berkeley: University of California Press.
8. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. 2011. GenBank. Nucleic Acids Research 39(Database issue):D32-D37 DOI 10.1093/nar/gkq1079.
9. Bisharat N, Cohen DI, Harding RM, Falush D, Crook DW, Peto T, Maiden MC. 2005. Hybrid Vibrio vulnificus. Emerging Infectious Diseases 111:30-35 DOI 10.3201/eid1101.040440.
10. Blok VC, Powers TO. 2009. Biochemical and molecular identification. In: Root-knot nematodes. Wallingford: CABI Publishing, 98-118.
11. Brasier CM. 2001. Rapid evolution of introduced plant pathogens via interspecific hybridization. Bioscience 512:123-133 DOI 10.1641/0006-3568(2001)051[0123:REOIPP]2.0.CO;2.
12. Bullini L. 1994. Origin and evolution of animal hybrid species. Trends In Ecology & Evolution 911:422-426 DOI 10.1016/0169-5347(94)90124-4.
13. Castagnone-Sereno P. 2006. Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity 964:282-289 DOI 10.1038/sj.hdy.6800794.
14. Chitwood DJ, Perry RN. 2009. Reproduction, Physiology and Biochemistry. In: Perry RN, Moens M, Starr JL, eds. Root-knot nematodes. CAB International, 182-200.
15. Czypionka T, Cheng J, Pozhitkov A, Nolte AW. 2012. Transcriptome changes after genomewide admixture in invasive sculpins (Cottus). Molecular Ecology 2119:4797-4810 DOI 10.1111/j.1365-294X.2012.05645.x.
16. Dalmasso A, Berge JB. 1983. Enzyme polymorphism and the concept of parthenogenetic species, exemplified by Meloidogyne. In: Stone AR, Platt HM, Khalil LF, eds. Concepts in nematode systmatics. London: Academic Press, 187-196.
17. De Ley IT, De Ley P, Vierstraete A, Karssen G, Moens M, Vanfleteren J. 2002. Phylogenetic analyses of Meloidogyne small subunit rDNA. Journal of Nematology 34(4):319-327.
18. Genner MJ, Turner GF. 2012. Ancient hybridization and phenotypic novelty within Lake Malawi's cichlid fish radiation. Molecular Biology and Evolution 291:195-206 DOI 10.1093/molbev/msr183.
19. Genner MJ, Seehausen O, Lunt DH, Joyce DA, Shaw PW, Carvalho GR, Turner GF. 2007. Age of cichlids: new dates for ancient lake fish radiations. Molecular Biology and Evolution 245:1269-1282 DOI 10.1093/molbev/msm050.
20. Goldberg EE, Igíc B. 2008. On phylogenetic tests of irreversible evolution. Evolution; International Journal of Organic Evolution 6211:2727-2741 DOI 10.1111/j.1558-5646.2008.00505.x.
21. Goss EM, Cardenas ME, Myers K, Forbes GA, Fry WE, Restrepo S, Grünwald NJ. 2011. The plant pathogen Phytophthora andina emerged via hybridization of an unknown Phytophthora species and the Irish potato famine pathogen, P. infestans. PLoS ONE 6(9):e24543 DOI 10.1371/journal.pone.0024543.
22. Hailer F, Kutschera VE, HallstromBM, Klassert D, Fain SR, Leonard JA, Arnason U, Janke A. 2012. Nuclear genomic sequences reveal that polar bears are an old and distinct bear lineage. Science 3366079:344-347 DOI 10.1126/science.1216424.
23. Handoo ZA, Nyczepir AP, Esmenjaud D, van der Beek JG, Castagnone-Sereno P, Carta LK, Skantar AM, Higgins JA. 2004. Morphological, molecular, and differential-host characterization of Meloidogyne floridensis n. sp. (Nematoda: Meloidogynidae), a root-knot nematode parasitizing peach in Florida. Journal of Nematology 36(1):20-35.
24. Heliconius Genome Consortium. 2012. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487:94-98 DOI 10.1038/nature11041.
25. Hermansen JS, Saether SA, Elgvin TO, Borge T, Hjelle E, Saetre G-P. 2011. Hybrid speciation in sparrows I: phenotypic intermediacy, genetic admixture and barriers to gene flow. Molecular Ecology 2018:3812-3822 DOI 10.1111/j.1365-294X.2011.05183.x.
26. Holterman M, Karssen G, van den Elsen S, vanMegen H, Bakker J, Helder J. 2009. Small subunit rDNA-based phylogeny of the tylenchida sheds light on relationships among some high-impact plant-parasitic nematodes and the evolution of plant feeding. Phytopathology 993:227-235 DOI 10.1094/PHYTO-99-3-0227.
27. Hood ME, Antonovics J. 2004. Mating within the meiotic tetrad and the maintenance of genomic heterozygosity. Genetics 1664:1751-1759 DOI 10.1534/genetics.166.4.1751.
28. Hugall A, Stanton J, Moritz C. 1999. Reticulate evolution and the origins of ribosomal internal transcribed spacer diversity in apomictic Meloidogyne. Molecular Biology and Evolution 162:157-164 DOI 10.1093/oxfordjournals.molbev.a026098.
29. Inderbitzin P, Davis RM, Bostock RM, Subbarao KV. 2011. The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PLoS ONE 6(3):e18260 DOI 10.1371/journal.pone.0018260.
30. Jeyaprakash A, Tigano MS, Brito J, Carneiro RMDG, Dickson DW. 2006. Differentiation of Meloidogyne floridensis from M. arenaria using high-fidelity PCR amplified mitochondrial AT-rich sequences. Nematropica 36(1):1-12.
31. Joyce DA, Lunt DH, Genner MJ, Turner GF, Bills R, Seehausen O. 2011. Repeated colonization and hybridization in Lake Malawi cichlids. Current Biology 21(3):R108-R109 DOI 10.1016/j.cub.2010.11.029.
32. Judson OP, Normark BB. 1996. Ancient asexual scandals. Trends In Ecology & Evolution 112:41-46 DOI 10.1016/0169-5347(96)81040-8.
33. Kearney M. 2005. Hybridization, glaciation and geographical parthenogenesis. Trends In Ecology & Evolution 209:495-502 DOI 10.1016/j.tree.2005.06.005.
34. Kim T, Park S. QuickParanoid-a tool for ortholog clustering. Available at http://pl.postech.ac.kr/QuickParanoid.
35. Kumar S, Blaxter ML. 2012. Simultaneous genome sequencing of symbionts and their hosts. Symbiosis 553:119-126 DOI 10.1007/s13199-012-0154-6.
36. Li W, Godzik A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2213:1658-1659 DOI 10.1093/bioinformatics/btl158.
37. Liu QL, Thomas VP, Williamson VM. 2007. Meiotic parthenogenesis in a root-knot nematode results in rapid genomic homozygosity. Genetics 1763:1483-1490 DOI 10.1534/genetics.107.071134.
38. Loh Y-HE, Bezault E, Muenzel FM, Roberts RB, Swofford R, Barluenga M, Kidd CE, Howe AE, Di Palma F, Lindblad-Toh K, Hey J, Seehausen O, Salzburger W, Kocher TD, Streelman JT. 2012. Origins of shared genetic variation in African cichlids. Molecular Biology and Evolution 30:906-917 DOI 10.1093/molbev/mss326.
39. Lunt DH. 2008. Genetic tests of ancient asexuality in root knot nematodes reveal recent hybrid origins. BMC Evolutionary Biology 8(1):194 DOI 10.1186/1471-2148-8-194.
40. Mallet J. 2007. Hybrid speciation. Nature 4467133:279-283 DOI 10.1038/nature05706.
41. Mallet J. 2005. Hybridization as an invasion of the genome. Trends In Ecology & Evolution 205:229-237 DOI 10.1016/j.tree.2005.02.010.
42. Mavarez J, Linares M. 2008. Homoploid hybrid speciation in animals. Molecular Ecology 1719:4181-4185 DOI 10.1111/j.1365-294X.2008.03898.x.
43. Mayr E. 1963. Animal species and evolution. Harvard University Press.
44. Meyer M, Kircher M, Gansauge M-T, Li H, Racimo F, Mallick S, Schraiber JG, Jay F, Prufer K, de Filippo C, Sudmant PH, Alkan C, Fu Q, Do R, Rohland N, Tandon A, Siebauer M, Green RE, Bryc K, Briggs AW, Stenzel U, Dabney J, Shendure J, Kitzman J, Hammer MF, Shunkov MV, Derevianko AP, Patterson N, Andres AM, Eichler EE, Slatkin M, Reich D, Kelso J, Paabo S. 2012. A high-coverage genome sequence from an archaic denisovan individual. Science 3386104:222-226 DOI 10.1126/science.1224344.
45. Mitreva M, Jasmer DP, Zarlenga DS, Wang Z, Abubucker S, Martin J, Taylor CM, Yin Y, Fulton L, Minx P, Yang S-P, WarrenWC, Fulton RS, Bhonagiri V, Zhang X, Hallsworth-Pepin K, Clifton SW, McCarter JP, Appleton J, Mardis ER, Wilson RK. 2011. The draft genome of the parasitic nematode Trichinella spiralis. Nature Genetics 433:228-235 DOI 10.1038/ng.769.
46. Moens M, Perry RN, Starr JL. 2009. Meloidogyne species-a diverse group of novel and important plant parasites. In: Root-knot nematodes. CAB International, 1-17.
47. Nolte AW, Tautz D. 2010. Understanding the onset of hybrid speciation. Trends in Genetics 262:54-58 DOI 10.1016/j.tig.2009.12.001.
48. Opperman CH, Bird DM, Williamson VM, Rokhsar DS, Burke M, Cohn J, Cromer J, Diener S, Gajan J, Graham S, Houfek TD, Liu Q, Mitros T, SchaffJ, Schaffer R, Scholl E, Sosinski BR, Thomas VP, Windham E. 2008. Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences of the United States of America 10539:14802-14807 DOI 10.1073/pnas.0805946105.
49. Ostlund G, Schmitt T, Forslund K, Kostler T, Messina DN, Roopra S, Frings O, Sonnhammer ELL. 2010. InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Research 38(Database issue):D196-D203 DOI 10.1093/nar/gkp931.
50. Pableo EC, Triantaphyllou AC. 1989. DNA complexity of the root-knot nematode (Meloidgyne spp.) genome. Journal of Nematology 21:260-263.
51. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 202:289-290 DOI 10.1093/bioinformatics/btg412.
52. Parra G, Bradnam K, Korf I. 2007. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 239:1061-1067 DOI 10.1093/bioinformatics/btm071.
53. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European molecular biology open software suite. Trends in Genetics 166:276-277 DOI 10.1016/S0168-9525(00)02024-2.
54. Rieseberg LH, Archer MA, Wayne RK. 1999. Transgressive segregation, adaptation and speciation. Heredity 83(Pt 4):363-372 DOI 10.1038/sj.hdy.6886170.
55. Rieseberg LH, Whitton J, Gardner K. 1999. Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152(2):713-727.
56. Sasser JN, Carter CC. 1985. Overview of the international meloidogyne project 1975-1984. In: Barker KR, Carter CC, Sasser JN, eds. An advanced treatise on Meloidogyne. Raleigh, NC:North Carolina State University.
57. Schwarz D, Matta BM, Shakir-Botteri NL, McPheron BA. 2005. Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 4367050:546-549 DOI 10.1038/nature03800.
58. Schwarzer J, Swartz ER, Vreven E, Snoeks J, Cotterill FPD, Misof B, Schliewen UK. 2012. Repeated trans-watershed hybridization among haplochromine cichlids (Cichlidae) was triggered by Neogene landscape evolution. Proceedings of the Royal Society B: Biological Sciences 2791746:4389-4398 DOI 10.1098/rspb.2012.1667.
59. Schwenk K, Brede N, Streit B. 2008. Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals. Philosophical Transactions of the Royal Society B:Biological Sciences 3631505:2805-2811 DOI 10.1098/rstb.2008.0055.
60. Seehausen O. 2006. Hybridization and adaptive radiation. Trends In Ecology & Evolution 194:198-207 DOI 10.1016/j.tree.2004.01.003.
61. Seehausen O. 2013. Conditions when hybridization might predispose populations for adaptive radiation. Journal of Evolutionary Biology 262:279-281 DOI 10.1111/jeb.12026.
62. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology 7:539 DOI 10.1038/msb.2011.75.
63. Slater GSC, Birney E. 2005. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6:31 DOI 10.1186/1471-2105-6-31.
64. Smith J. 1978. The evolution of sex. Cambridge University Press.
65. Soltis PS, Soltis DE. 2009. The role of hybridization in plant speciation. Annual Review of Plant Biology 60:561-588 DOI 10.1146/annurev.arplant.043008.092039.
66. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2221:2688-2690 DOI 10.1093/bioinformatics/btl446.
67. Stelkens R, Seehausen O. 2009. Genetic distance between species predicts novel trait expression in their hybrids. Evolution 634:884-897 DOI 10.1111/j.1558-5646.2008.00599.x.
68. Stukenbrock EH, McDonald BA. 2008. The origins of plant pathogens in agro-ecosystems. Annual Review of Phytopathology 46:75-100 DOI 10.1146/annurev.phyto.010708.154114.
69. Stukenbrock EH, Christiansen FB, Hansen TT, Dutheil JY, Schierup MH. 2012. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. Proceedings of the National Academy of Sciences of the United States of America 10927:10954-10959 DOI 10.1073/pnas.1201403109.
70. Taylor AL, Sasser JN. 1978. Biology, identification and control of root-knot nematodes (Meloidogyne species). Raleigh, NC: North Carolina State University.
71. Tigano MS, Dickson D, Tigano M, Jeyaprakash A, Adams B. 2005. Phylogeny of Meloidogyne spp. based on 18S rDNA and the intergenic region of mitochondrial DNA sequences. Nematology 76:851-862 DOI 10.1163/156854105776186325.
72. Triantaphyllou AC. 1982. Cytogenetics and sexuality of root-knot and cyst nematodes. In: Riggs RD, ed. Nematology in the southern region of the United States. Arkansas Agricultural Experiment Station, Fayetteville, AK: Southern Cooperative Series Bulletin, pp. 71-76.
73. Triantaphyllou AC. 1985. Cytogenetics, cytotaxonomy and phylogeny of root-knot nematodes. In: Sasser JN, Carter CC, eds. An advanced treatise on meloidogyne. Raleigh: North Carolina State University.
74. Trudgill DL, Blok VC. 2001. Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annual Review of Phytopathology 39:53-77 DOI 10.1146/annurev.phyto.39.1.53.
75. White MJD. 1945. Animal cytology & evolution, 1st edition. Cambridge University Press.
76. Zerbino DR. 2010. Using the Velvet de novo assembler for short-read sequencing technologies. Chapter 11, In: Current protocols in bioinformatics. p. Unit 11.5.
77. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Research 185:821-829 DOI 10.1101/gr.074492.107.
78. Zhang Z, Schwartz S, Wagner L, Miller W. 2000. A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7(1-2):203-214 DOI 10.1089/10665270050081478.