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Title: Genome Landscape and Evolutionary Plasticity of Chromosomes in Malaria Mosquitoes

Journal Article · · PLoS ONE
 [1];  [2];  [2];  [2];  [3];  [4];  [2]
  1. Virginia Polytechnic Institute and State University (Virginia Tech), Blacksburg, VA (United States); DOE/OSTI
  2. Virginia Polytechnic Institute and State University (Virginia Tech), Blacksburg, VA (United States)
  3. University of Massachusetts, Worcester, MA (United States)
  4. San Francisco State University, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Nonrandom distribution of rearrangements is a common feature of eukaryotic chromosomes that is not well understood in terms of genome organization and evolution. In the major African malaria vector Anopheles gambiae, polymorphic inversions are highly nonuniformly distributed among five chromosomal arms and are associated with epidemiologically important adaptations. However, it is not clear whether the genomic content of the chromosomal arms is associated with inversion polymorphism and fixation rates. To better understand the evolutionary dynamics of chromosomal inversions, we created a physical map for an Asian malaria mosquito, Anopheles stephensi, and compared it with the genome of An. gambiae. We also developed and deployed novel Bayesian statistical models to analyze genome landscapes in individual chromosomal arms An. gambiae. Here, we demonstrate that, despite the paucity of inversion polymorphisms on the X chromosome, this chromosome has the fastest rate of inversion fixation and the highest density of transposable elements, simple DNA repeats, and GC content. The highly polymorphic and rapidly evolving autosomal 2R arm had overrepresentation of genes involved in cellular response to stress supporting the role of natural selection in maintaining adaptive polymorphic inversions. In addition, the 2R arm had the highest density of regions involved in segmental duplications that clustered in the breakpoint-rich zone of the arm. In contrast, the slower evolving 2L, 3R, and 3L, arms were enriched with matrixattachment regions that potentially contribute to chromosome stability in the cell nucleus. These results highlight fundamental differences in evolutionary dynamics of the sex chromosome and autosomes and revealed the strong association between characteristics of the genome landscape and rates of chromosomal evolution. We conclude that a unique combination of various classes of genes and repetitive DNA in each arm, rather than a single type of repetitive element, is likely responsible for arm-specific rates of rearrangements.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1627408
Journal Information:
PLoS ONE, Journal Name: PLoS ONE Journal Issue: 5 Vol. 5; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (107)

Breakpoints of variant 9;22 translocations in chronic myeloid leukemia locate preferentially in the CG-richest regions of the genome journal January 2005
DNA from Drosophila melanogaster β-heterochromatin binds specifically to nuclear lamins in vitro and the nuclear envelope in situ journal June 1996
Nuclear architecture, chromosome domains and genetic damage journal March 2008
Chromosome evolution in eukaryotes: a multi-kingdom perspective journal December 2005
Developmental and evolutionary basis for drought tolerance of the Anopheles gambiae embryo journal June 2009
Analysis of the complete mitochondrial DNA from Anopheles funestus: An improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution journal May 2006
Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences journal May 2007
Chromosome speciation: Humans, Drosophila, and mosquitoes journal May 2005
Breakpoint structure reveals the unique origin of an interspecific chromosomal inversion (2La) in the Anopheles gambiae complex journal April 2006
Z-DNA-forming sequences generate large-scale deletions in mammalian cells journal February 2006
A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae journal February 2008
Cloning of inversion breakpoints in the Anopheles gambiae complex traces a transposable element at the inversion junction journal October 1998
InterProScan - an integration platform for the signature-recognition methods in InterPro journal September 2001
Maintenance of chromosome arm integrity between two Anopheles mosquito subgenera journal September 2000
A Microsatellite Map of the African Human Malaria Vector Anopheles funestus journal January 2004
Tandem repeats finder: a program to analyze DNA sequences journal January 1999
VectorBase: a data resource for invertebrate vector genomics journal January 2009
BioMart Central Portal—unified access to biological data journal May 2009
Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin journal April 2008
Segmental Duplications: Organization and Impact Within the Current Human Genome Project Assembly journal May 2001
In Silico Prediction of Scaffold/Matrix Attachment Regions in Large Genomic Sequences journal February 2002
Comparative genome sequencing of Drosophila pseudoobscura: Chromosomal, gene, and cis-element evolution journal January 2005
Comparative analysis of chicken chromosome 28 provides new clues to the evolutionary fragility of gene-rich vertebrate regions journal November 2007
Female Sterility in Hybrids Between Anopheles Gambiae and a. Arabiensis, and the Causes of Haldane'S rule journal May 2005
INVERSION LENGTH AND BREAKPOINT DISTRIBUTION IN THE DROSOPHILA BUZZATII SPECIES COMPLEX: IS INVERSION LENGTH A SELECTED TRAIT? journal August 1997
The Genome Sequence of the Malaria Mosquito Anopheles gambiae journal October 2002
Inversions and Gene Order Shuffling in Anopheles gambiae and A. funestus journal October 2002
A Polytene Chromosome Analysis of the Anopheles gambiae Species Complex journal October 2002
Structural Dynamics of Eukaryotic Chromosome Evolution journal August 2003
Dynamics of Mammalian Chromosome Evolution Inferred from Multispecies Comparative Maps journal July 2005
Generation of a Widespread Drosophila Inversion by a Transposable Element journal July 1999
Inversion polymorphisms in natural populations of Anopheles stephensi journal October 1984
Mapping a Quantitative Trait Locus (QTL) conferring pyrethroid resistance in the African malaria vector Anopheles funestus journal January 2007
Inversion 2La is associated with enhanced desiccation resistance in Anopheles gambiae journal January 2009
ISWI Regulates Higher-Order Chromatin Structure and Histone H1 Assembly In Vivo journal August 2007
Genome Organization and Gene Expression Shape the Transposable Element Distribution in the Drosophila melanogaster Euchromatin journal November 2007
Segmental Duplication Implicated in the Genesis of Inversion 2Rj of Anopheles gambiae journal September 2007
Evaluation of the Genomic Extent of Effects of Fixed Inversion Differences on Intraspecific Variation and Interspecific Gene Flow in Drosophila pseudoobscura and D. persimilis journal March 2007
The Genetics of Inviability and Male Sterility in Hybrids Between Anopheles gambiae and An. arabiensis journal May 2004
Breakpoints of variant 9;22 translocations in chronic myeloid leukemia locate preferentially in the CG-richest regions of the genome journal January 2005
The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster book January 1993
Interpretation of variation in ovarian polytene chromosomes of Anopheles Funestus Giles, A. Parensis Gillies, and A. Aruni? journal July 1980
The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster journal January 1992
Segmental duplication associated with the human-specific inversion of chromosome�18: a further example of the impact of segmental duplications on karyotype and genome evolution in primates journal May 2004
DNA from Drosophila melanogaster β-heterochromatin binds specifically to nuclear lamins in vitro and the nuclear envelope in situ journal June 1996
Order and Disorder in the Nucleus journal March 2002
Nuclear architecture, chromosome domains and genetic damage journal March 2008
Chromosome evolution in eukaryotes: a multi-kingdom perspective journal December 2005
Developmental and evolutionary basis for drought tolerance of the Anopheles gambiae embryo journal June 2009
Analysis of the complete mitochondrial DNA from Anopheles funestus: An improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution journal May 2006
Gene Ontology: tool for the unification of biology journal May 2000
Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences journal May 2007
Maintenance of a large pericentric inversion generated by the hobo transposable element in a transgenic line of Drosophila melanogaster journal January 2004
Chromosome speciation: Humans, Drosophila, and mosquitoes journal May 2005
Breakpoint structure reveals the unique origin of an interspecific chromosomal inversion (2La) in the Anopheles gambiae complex journal April 2006
Z-DNA-forming sequences generate large-scale deletions in mammalian cells journal February 2006
A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae journal February 2008
Lengths of chromosomal segments conserved since divergence of man and mouse. journal February 1984
Cloning of inversion breakpoints in the Anopheles gambiae complex traces a transposable element at the inversion junction journal October 1998
The Relative Rates of Evolution of Sex Chromosomes and Autosomes journal July 1987
InterProScan - an integration platform for the signature-recognition methods in InterPro journal September 2001
GRIMM: genome rearrangements web server journal March 2002
GO::TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes journal August 2004
Chromosomal Elements Evolve at Different Rates in the Drosophila Genome journal July 2002
Maintenance of chromosome arm integrity between two Anopheles mosquito subgenera journal September 2000
A Microsatellite Map of the African Human Malaria Vector Anopheles funestus journal January 2004
A Standard Cytogenetic Photomap for the Mosquito Anopheles stephensi (Diptera: Culicidae): Application for Physical Mapping journal September 2006
Tandem repeats finder: a program to analyze DNA sequences journal January 1999
VectorBase: a data resource for invertebrate vector genomics journal January 2009
BioMart Central Portal—unified access to biological data journal May 2009
Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin journal April 2008
Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories journal April 2009
Segmental Duplications: Organization and Impact Within the Current Human Genome Project Assembly journal May 2001
In Silico Prediction of Scaffold/Matrix Attachment Regions in Large Genomic Sequences journal January 2002
In Silico Prediction of Scaffold/Matrix Attachment Regions in Large Genomic Sequences journal January 2002
Comparative genome sequencing of Drosophila pseudoobscura: Chromosomal, gene, and cis-element evolution journal January 2005
Comparative analysis of chicken chromosome 28 provides new clues to the evolutionary fragility of gene-rich vertebrate regions journal November 2007
Segmental Duplications: Organization and Impact Within the Current Human Genome Project Assembly journal May 2001
Female Sterility in Hybrids Between Anopheles Gambiae and a. Arabiensis, and the Causes of Haldane'S rule journal May 2005
Differential gene expression in incipient species of Anopheles gambiae: DIFFERENTIAL GENE EXPRESSION IN A. GAMBIAE journal April 2008
INVERSION LENGTH AND BREAKPOINT DISTRIBUTION IN THE DROSOPHILA BUZZATII SPECIES COMPLEX: IS INVERSION LENGTH A SELECTED TRAIT? journal August 1997
The Genome Sequence of the Malaria Mosquito Anopheles gambiae journal October 2002
Inversions and Gene Order Shuffling in Anopheles gambiae and A. funestus journal October 2002
A Polytene Chromosome Analysis of the Anopheles gambiae Species Complex journal October 2002
Structural Dynamics of Eukaryotic Chromosome Evolution journal August 2003
Dynamics of Mammalian Chromosome Evolution Inferred from Multispecies Comparative Maps journal July 2005
Generation of a Widespread Drosophila Inversion by a Transposable Element journal July 1999
Inversion polymorphisms in natural populations of Anopheles stephensi journal October 1984
Revisiting the Impact of Inversions in Evolution: From Population Genetic Markers to Drivers of Adaptive Shifts and Speciation? journal December 2008
Chromosomal plasticity and evolutionary potential in the malaria vector Anopheles gambiae sensu stricto: insights from three decades of rare paracentric inversions journal January 2008
Identification and analysis of Single Nucleotide Polymorphisms (SNPs) in the mosquito Anopheles funestus, malaria vector journal January 2007
Inversion 2La is associated with enhanced desiccation resistance in Anopheles gambiae journal January 2009
Hotspots of mammalian chromosomal evolution journal January 2004
Update of the Anopheles gambiaePEST genome assembly journal January 2007
Principles of Genome Evolution in the Drosophila melanogaster Species Group journal June 2007
ISWI Regulates Higher-Order Chromatin Structure and Histone H1 Assembly In Vivo journal August 2007
Genome Organization and Gene Expression Shape the Transposable Element Distribution in the Drosophila melanogaster Euchromatin journal November 2007
Segmental Duplication Implicated in the Genesis of Inversion 2Rj of Anopheles gambiae journal September 2007
Chromosome Inversions, Local Adaptation and Speciation journal October 2005
Evaluation of the Genomic Extent of Effects of Fixed Inversion Differences on Intraspecific Variation and Interspecific Gene Flow in Drosophila pseudoobscura and D. persimilis journal March 2007
Chromosomal Rearrangement Inferred From Comparisons of 12 Drosophila Genomes journal July 2008
Chromosome Inversions, Local Adaptation and Speciation [Correction] journal January 2018
The Genetics of Inviability and Male Sterility in Hybrids Between Anopheles gambiae and An. arabiensis journal May 2004
Female Sterility in Hybrids Between Anopheles Gambiae and a. Arabiensis, and the Causes of Haldane'S rule journal January 2005
A Standard Cytogenetic Photomap for the Mosquito Anopheles stephensi (Diptera: Culicidae): Application for Physical Mapping journal September 2006
Inversion Length and Breakpoint Distribution in the Drosophila buzzatii Species Complex: Is Inversion Length a Selected Trait? journal August 1997
Hairpin- and cruciform-mediated chromosome breakage: causes and consequences in eukaryotic cells journal January 2007

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Genomic composition and evolution of Aedes aegyptichromosomes revealed by the analysis of physically mapped supercontigs journal April 2014
Partial-arm translocations in evolution of malaria mosquitoes revealed by high-coverage physical mapping of the Anopheles atroparvus genome journal April 2018
Comparative physical genome mapping of malaria vectors Anopheles sinensis and Anopheles gambiae journal June 2017
Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi journal September 2014
Structural divergence of chromosomes between malaria vectors Anopheles lesteri and Anopheles sinensis journal November 2016
Evolutionary Dynamics of the Ty3/Gypsy LTR Retrotransposons in the Genome of Anopheles gambiae journal January 2011
Genome-Wide Transcriptional Analysis of Genes Associated with Acute Desiccation Stress in Anopheles gambiae journal October 2011
Unravelling the Evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor Gene Families in Bilaterians: Insights from Anopheles Mosquitoes journal July 2015
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The Genome of Anopheles darlingi , the main neotropical malaria vector journal June 2013
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