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...

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Autores principales:	Feng Gao, Scott W. Roy, Laura A. Katz
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
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spelling	oai:doaj.org-article:6bc0454833344a969798b1d80bd8586f2021-11-15T15:41:19ZAnalyses of Alternatively Processed Genes in Ciliates Provide Insights into the Origins of Scrambled Genomes and May Provide a Mechanism for Speciation10.1128/mBio.01998-142150-7511https://doaj.org/article/6bc0454833344a969798b1d80bd8586f2015-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01998-14https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE 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.Feng GaoScott W. RoyLaura A. KatzAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 1 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Feng Gao Scott W. Roy Laura A. Katz Analyses of Alternatively Processed Genes in Ciliates Provide Insights into the Origins of Scrambled Genomes and May Provide a Mechanism for Speciation
description	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. IMPORTANCE 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.
format	article
author	Feng Gao Scott W. Roy Laura A. Katz
author_facet	Feng Gao Scott W. Roy Laura A. Katz
author_sort	Feng Gao
title	Analyses of Alternatively Processed Genes in Ciliates Provide Insights into the Origins of Scrambled Genomes and May Provide a Mechanism for Speciation
title_short	Analyses of Alternatively Processed Genes in Ciliates Provide Insights into the Origins of Scrambled Genomes and May Provide a Mechanism for Speciation
title_full	Analyses of Alternatively Processed Genes in Ciliates Provide Insights into the Origins of Scrambled Genomes and May Provide a Mechanism for Speciation
title_fullStr	Analyses of Alternatively Processed Genes in Ciliates Provide Insights into the Origins of Scrambled Genomes and May Provide a Mechanism for Speciation
title_full_unstemmed	Analyses of Alternatively Processed Genes in Ciliates Provide Insights into the Origins of Scrambled Genomes and May Provide a Mechanism for Speciation
title_sort	analyses of alternatively processed genes in ciliates provide insights into the origins of scrambled genomes and may provide a mechanism for speciation
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/6bc0454833344a969798b1d80bd8586f
work_keys_str_mv	AT fenggao analysesofalternativelyprocessedgenesinciliatesprovideinsightsintotheoriginsofscrambledgenomesandmayprovideamechanismforspeciation AT scottwroy analysesofalternativelyprocessedgenesinciliatesprovideinsightsintotheoriginsofscrambledgenomesandmayprovideamechanismforspeciation AT lauraakatz analysesofalternativelyprocessedgenesinciliatesprovideinsightsintotheoriginsofscrambledgenomesandmayprovideamechanismforspeciation
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Analyses of Alternatively Processed Genes in Ciliates Provide Insights into the Origins of Scrambled Genomes and May Provide a Mechanism for Speciation

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