A close-up view on ITS2 evolution and speciation - a case study in the Ulvophyceae (Chlorophyta, Viridiplantae).

Publisher: BioMed Central Country of Publication: England NLM ID: 100966975 Publication Model: Electronic Cited Medium: Internet ISSN: 1471-2148 (Electronic) Linking ISSN: 14712148 NLM ISO Abbreviation: BMC Evol Biol Subsets: MEDLINE

Original Publication: London : BioMed Central, [2001-

Evolution, Molecular* ; Genetic Speciation* ; Models, Molecular* ; Phylogeny*; Chlorophyta/*genetics ; DNA, Ribosomal Spacer/*genetics; Base Pairing/genetics ; Base Sequence ; Bayes Theorem ; Cluster Analysis ; DNA Primers/genetics ; Likelihood Functions ; Models, Genetic ; Molecular Sequence Data ; Sequence Alignment ; Sequence Analysis, DNA

Background: The second Internal Transcriber Spacer (ITS2) is a fast evolving part of the nuclear-encoded rRNA operon located between the 5.8S and 28S rRNA genes. Based on crossing experiments it has been proposed that even a single Compensatory Base Change (CBC) in helices 2 and 3 of the ITS2 indicates sexual incompatibility and thus separates biological species. Taxa without any CBC in these ITS2 regions were designated as a 'CBC clade'. However, in depth comparative analyses of ITS2 secondary structures, ITS2 phylogeny, the origin of CBCs, and their relationship to biological species have rarely been performed. To gain 'close-up' insights into ITS2 evolution, (1) 86 sequences of ITS2 including secondary structures have been investigated in the green algal order Ulvales (Chlorophyta, Viridiplantae), (2) after recording all existing substitutions, CBCs and hemi-CBCs (hCBCs) were mapped upon the ITS2 phylogeny, rather than merely comparing ITS2 characters among pairs of taxa, and (3) the relation between CBCs, hCBCs, CBC clades, and the taxonomic level of organisms was investigated in detail.
Results: High sequence and length conservation allowed the generation of an ITS2 consensus secondary structure, and introduction of a novel numbering system of ITS2 nucleotides and base pairs. Alignments and analyses were based on this structural information, leading to the following results: (1) in the Ulvales, the presence of a CBC is not linked to any particular taxonomic level, (2) most CBC 'clades' sensu Coleman are paraphyletic, and should rather be termed CBC grades. (3) the phenetic approach of pairwise comparison of sequences can be misleading, and thus, CBCs/hCBCs must be investigated in their evolutionary context, including homoplasy events (4) CBCs and hCBCs in ITS2 helices evolved independently, and we found no evidence for a CBC that originated via a two-fold hCBC substitution.
Conclusions: Our case study revealed several discrepancies between ITS2 evolution in the Ulvales and generally accepted assumptions underlying ITS2 evolution as e.g. the CBC clade concept. Therefore, we developed a suite of methods providing a critical 'close-up' view into ITS2 evolution by directly tracing the evolutionary history of individual positions, and we caution against a non-critical use of the ITS2 CBC clade concept for species delimitation.

Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1840-3. (PMID: 11607157)
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W704-7. (PMID: 16845103)
J Mol Evol. 2002 Feb;54(2):246-57. (PMID: 11821917)
Nucleic Acids Res. 2007;35(10):3322-9. (PMID: 17459886)
Genetics. 2004 Jan;166(1):637-40. (PMID: 15020451)
Trends Genet. 2003 Jul;19(7):370-5. (PMID: 12850441)
Mycol Res. 2008 Mar;112(Pt 3):316-30. (PMID: 18342242)
Mol Phylogenet Evol. 2009 Dec;53(3):749-57. (PMID: 19654048)
Mol Phylogenet Evol. 2009 Aug;52(2):520-3. (PMID: 19489124)
RNA. 2000 Dec;6(12):1698-703. (PMID: 11142370)
Mol Phylogenet Evol. 2003 Nov;29(2):216-34. (PMID: 13678678)
RNA. 1999 Nov;5(11):1490-4. (PMID: 10580477)
Nucleic Acids Res. 1999 Dec 1;27(23):4533-40. (PMID: 10556307)
Am J Bot. 2002 Sep;89(9):1523-30. (PMID: 21665754)
Nat Genet. 2004 Nov;36(11):1207-12. (PMID: 15502829)
Syst Parasitol. 2010 Nov;77(3):185-204. (PMID: 20960090)
Biol Direct. 2010 Jan 15;5:4. (PMID: 20078867)
Protist. 2000 May;151(1):1-9. (PMID: 10896128)
Protist. 2003 Apr;154(1):99-145. (PMID: 12812373)
BMC Bioinformatics. 2010 Mar 15;11:129. (PMID: 20230624)
J Mol Evol. 2009 Aug;69(2):150-63. (PMID: 19609478)
Mol Biol Evol. 1993 Jan;10(1):256-67. (PMID: 8450759)
Genes Genet Syst. 1999 Dec;74(6):271-86. (PMID: 10791023)
Mol Phylogenet Evol. 2009 Jan;50(1):197-203. (PMID: 18992828)
J Mol Evol. 1999 Jan;48(1):94-101. (PMID: 9873081)
Genetics. 1998 Apr;148(4):1993-2002. (PMID: 9560412)
Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10032-6. (PMID: 1946420)
Genetics. 1998 May;149(1):243-56. (PMID: 9584100)
J Eukaryot Microbiol. 2005 Jan-Feb;52(1):68-77. (PMID: 15702983)
Biosystems. 1978 Apr;10(1-2):117-44. (PMID: 350301)
RNA. 2007 Sep;13(9):1469-72. (PMID: 17652131)
Mol Biol Evol. 2008 Jul;25(7):1253-6. (PMID: 18397919)
Fungal Genet Biol. 2009 Nov;46(11):855-67. (PMID: 19665572)
J Cell Sci. 1981 Aug;50:149-64. (PMID: 7320063)
BMC Evol Biol. 2009 Dec 26;9:300. (PMID: 20035628)
Protist. 2005 Dec;156(4):425-32. (PMID: 16310747)
Nucleic Acids Res. 1998 Aug 1;26(15):3513-20. (PMID: 9671812)
Curr Opin Struct Biol. 2002 Jun;12(3):301-10. (PMID: 12127448)
RNA. 2005 Apr;11(4):361-4. (PMID: 15769870)
PLoS One. 2011 Feb 10;6(2):e16931. (PMID: 21347329)
Nucleic Acids Res. 2010 Jul;38(13):4487-502. (PMID: 20338880)
Gene. 2003 Aug 14;313:17-42. (PMID: 12957375)
RNA. 1995 Oct;1(8):807-14. (PMID: 7493326)
J Plant Res. 2010 Mar;123(2):231-9. (PMID: 19941029)
Protist. 2007 Apr;158(2):193-207. (PMID: 17145201)
Mol Phylogenet Evol. 2009 May;51(2):215-26. (PMID: 19059352)
Mol Phylogenet Evol. 2007 Apr;43(1):124-39. (PMID: 17070713)
Mol Phylogenet Evol. 2004 Jan;30(1):236-42. (PMID: 15022773)
Microbiol Rev. 1994 Mar;58(1):10-26. (PMID: 8177168)
Am J Bot. 2002 Nov;89(11):1756-63. (PMID: 21665602)
Mol Phylogenet Evol. 2009 Feb;50(2):364-75. (PMID: 19056501)
Mol Biol Evol. 1999 Aug;16(8):1011-8. (PMID: 10474897)
Nucleic Acids Res. 2010 Aug;38(15):5177-92. (PMID: 20392820)
Mol Phylogenet Evol. 2010 Jan;54(1):36-46. (PMID: 19853051)
Genetica. 2007 Jan;129(1):45-55. (PMID: 17109184)
RNA. 2010 Feb;16(2):375-81. (PMID: 20038632)
PLoS One. 2009 Dec 11;4(12):e8249. (PMID: 20011513)
J Mol Evol. 2008 Oct;67(4):389-96. (PMID: 18781354)
Bioinformatics. 2003 Aug 12;19(12):1572-4. (PMID: 12912839)
Mol Cell Biol. 2010 Feb;30(4):976-84. (PMID: 20008552)
J Mol Evol. 1997 Mar;44(3):258-71. (PMID: 9060392)
J Mol Biol. 2001 Mar 16;307(1):213-28. (PMID: 11243815)
RNA. 2005 Nov;11(11):1616-23. (PMID: 16244129)
EMBO Rep. 2000 Jul;1(1):18-23. (PMID: 11256617)
BMC Res Notes. 2008 Oct 14;1:91. (PMID: 18854023)
Nucleic Acids Res. 2006 Mar 06;34(5):1326-41. (PMID: 16522645)
Mol Phylogenet Evol. 2007 Jun;43(3):774-86. (PMID: 17254805)
RNA. 2002 Jun;8(6):786-97. (PMID: 12088151)
Mol Phylogenet Evol. 2010 Feb;54(2):664-9. (PMID: 19660561)
J Mol Evol. 2005 Mar;60(3):327-36. (PMID: 15871043)
Evolution. 2005 Nov;59(11):2362-9. (PMID: 16396177)
BMC Bioinformatics. 2007 Nov 28;8:464. (PMID: 18045491)

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Date Created: 20110922 Date Completed: 20120105 Latest Revision: 20211020

20250114

PMC3225284

10.1186/1471-2148-11-262

21933414