title: Analyses of alternatively processed genes in ciliates provide insights into the origins of scrambled genomes and may provide a mechanism for speciation.
abstract: Chromosome rearrangements occur in a variety of eukaryotic life cycles, including during the development of the somatic macronuclear genome in ciliates. Previous work on the phyllopharyngean ciliate Chilodonella uncinata revealed that macronuclear β-tubulin and protein kinase gene families share alternatively processed germ line segments nested within divergent regions. To study genome evolution in this ciliate further, we characterized two additional alternatively processed gene families from two cryptic species of the ciliate morphospecies C. uncinata: those encoding histidine acid phosphatase protein (Hap) and leishmanolysin family protein (Lei). Analyses of the macronuclear Hap and Lei sequences reveal that each gene family consists of three members in the macronucleus that are marked by identical regions nested among highly divergent regions. Investigation of the micronuclear Hap sequences revealed a complex pattern in which the three macronuclear sequences are derived either from a single micronuclear region or from a combination of this shared region recombined with additional duplicate micronuclear copies of Hap. We propose a model whereby gene scrambling evolves by gene duplication followed by partial and reciprocal degradation of the duplicate sequences. In this model, alternative processing represents an intermediate step in the evolution of scrambled genes. Finally, we speculate on the possible role of genome architecture in speciation in ciliates by describing what might happen if changes in alternatively processed loci occur in subdivided populations.
  
  
  OBJECTIVE
  Genome rearrangements occur in a variety of eukaryotic cells and serve as an important mechanism for generating genomic diversity. The unusual genome architecture of ciliates with separate germline and somatic nuclei in each cell, provides an ideal system to study further principles of genome evolution. Previous analyses revealed complex forms of chromosome rearrangements, including gene scrambling and alternative processing of germ line chromosomes. Here we describe more complex rearrangements between germ line and somatic chromosomes than previously seen in alternatively processed gene families. Drawing on the present and previous findings, we propose a model in which alternative processing of duplicated micronuclear regions represents an intermediate stage in the evolution of scrambled genes. Under this model, alternative processing may provide insights into a mechanism for speciation in ciliates. Our data on gene scrambling and alternative processing also enhance views on the dynamic nature of genomes across the eukaryotic tree of life.
authors: Feng
authors: F
authors: Gao
authors: Department of Biology, San Francisco State University, San Francisco, California, USA.
authors: Scott W
authors: SW
authors: Roy
authors: lkatz@smith.edu.
authors: Laura A
authors: LA
authors: Katz
mesh_terms: D016798:Ciliophora / Q000145:classification / Q000235:genetics*; D019143:Evolution, Molecular; D049810:Genetic Speciation; D018503:Genome, Protozoan; D008969:Molecular Sequence Data; D010802:Phylogeny; D011544:Pseudogenes
references: Biochem J. 2008 Jan 15;409(2):333-48
references: 18092946
references: Evolution. 2014 Aug;68(8):2287-95
references: 24749903
references: Mol Biol Evol. 2008 Apr;25(4):787-94
references: 18258610
references: PLoS One. 2008;3(6):e2330
references: 18523559
references: PLoS Biol. 2008 Jul 29;6(7):e185
references: 18666832
references: Biochim Biophys Acta. 2008 Nov;1783(11):2130-6
references: 18706458
references: Bioinformatics. 2009 Jun 1;25(11):1451-2
references: 19346325
references: Curr Opin Microbiol. 2009 Dec;12(6):638-43
references: 19879799
references: Mol Biol Evol. 2010 Feb;27(2):221-4
references: 19854763
references: Proc Natl Acad Sci U S A. 2010 Feb 16;107(7):E25; author reply E26
references: 20145105
references: J Eukaryot Microbiol. 2010 Jul-Aug;57(4):369-78
references: 20553354
references: J Exp Zool B Mol Dev Evol. 2010 Sep 15;314(6):480-8
references: 20700892
references: Proc Natl Acad Sci U S A. 2010 Dec 21;107(51):22134-9
references: 20974970
references: Bioessays. 2011 May;33(5):344-9
references: 21381061
references: Genetica. 2011 May;139(5):677-84
references: 21505762
references: Bioessays. 2011 Jun;33(6):427-9
references: 21538416
references: IUBMB Life. 2011 Jul;63(7):528-37
references: 21698757
references: Annu Rev Genomics Hum Genet. 2011;12:367-89
references: 21801022
references: Nature. 2011 Sep 8;477(7363):203-6
references: 21841803
references: J Exp Zool B Mol Dev Evol. 2005 Sep 15;304(5):448-55
references: 16032699
references: Gene. 2006 Mar 1;368:72-7
references: 16316727
references: Nat Rev Immunol. 2006 Oct;6(10):728-40
references: 16998507
references: Annu Rev Genet. 2011;45:227-46
references: 21910632
references: J Mol Evol. 2011 Oct;73(3-4):70-3
references: 22037698
references: J Mol Evol. 2011 Dec;73(5-6):266-72
references: 22258433
references: Trends Genet. 2012 Aug;28(8):382-8
references: 22622227
references: PLoS One. 2012;7(8):e42371
references: 22900016
references: Cell. 2012 Dec 7;151(6):1243-55
references: 23217708
references: Biol Direct. 2012;7:35
references: 23062217
references: Science. 2000 Nov 10;290(5494):1151-5
references: 11073452
references: Mol Biol Evol. 2001 Jul;18(7):1372-7
references: 11420375
references: Int J Syst Evol Microbiol. 2001 Jul;51(Pt 4):1587-92
references: 11491362
references: Syst Biol. 2003 Oct;52(5):696-704
references: 14530136
references: Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3298-303
references: 10725348
references: Gene. 2003 Oct 2;315:15-9
references: 14557060
references: Protist. 2003 Oct;154(3-4):411-8
references: 14658497
references: Genetics. 2003 Dec;165(4):1761-77
references: 14704164
references: J Biol Chem. 1985 Dec 15;260(29):15504-9
references: 4066680
references: J Biol Chem. 1986 Jul 15;261(20):9098-101
references: 3522584
references: Genes Dev. 1992 May;6(5):788-800
references: 1577273
references: Dev Genet. 1992;13(1):66-74
references: 1395144
references: Microbiol Rev. 1994 Jun;58(2):233-67
references: 8078435
references: Mol Cell Biol. 1997 Jan;17(1):326-37
references: 8972213
references: Genetics. 1999 Apr;151(4):1531-45
references: 10101175
references: J Mol Evol. 1999 Aug;49(2):169-81
references: 10441669
references: Cell. 2013 Jan 31;152(3):406-16
references: 23374338
references: PLoS Biol. 2013;11(1):e1001473
references: 23382650
references: Eukaryot Cell. 2013 Mar;12(3):430-7
references: 23314963
references: PLoS Biol. 2013;11(3):e1001518
references: 23555191
references: Epigenomics. 2013 Apr;5(2):229-36
references: 23566098
references: Mol Phylogenet Evol. 2013 Jul;68(1):55-63
references: 23541839
references: Mol Phylogenet Evol. 2014 Jan;70:162-70
references: 24075983
references: Mol Phylogenet Evol. 2014 Jan;70:337-47
references: 24140978
references: Cold Spring Harb Perspect Biol. 2013 Dec;5(12):a017764
references: 24296171
references: Nature. 2008 Jan 10;451(7175):153-8
references: 18046331