Skip to main content
OSTI.GOVU.S. Department of Energy Office of Scientific and Technical Information
U.S. Department of Energy
Office of Scientific and Technical Information
 

Genome mapping and characterization of the Anopheles gambiae heterochromatin

Journal Article · · BMC Genomics
 [1];  [2];  [3];  [4];  [5];  [6];  [2]
  1. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Dept. of Entomology; DOE/OSTI
  2. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Dept. of Entomology
  3. Russian Academy of Sciences (RAS), Novosibirsk (Russian Federation). Siberian Branch. Inst. of Chemical Biology and Fundamental Medicine. Dept. of Molecular and Cell Biology
  4. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Dept. of Statistics
  5. Univ. of Massachusetts, Worcester, MA (United States). Medical School. Division of Trnsfusion Medicine. Dept. of Medicine. Program in Bioinformatics and Integrative Biology
  6. San Francisco State Univ., CA (United States). Dept. of Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Drosophila Heterochromatin Genome Project
+ Show Author Affiliations

Background: Heterochromatin plays an important role in chromosome function and gene regulation. Despite the availability of polytene chromosomes and genome sequence, the heterochromatin of the major malaria vector Anopheles gambiae has not been mapped and characterized. Results: To determine the extent of heterochromatin within the An. gambiae genome, genes were physically mapped to the euchromatin-heterochromatin transition zone of polytene chromosomes. The study found that a minimum of 232 genes reside in 16.6 Mb of mapped heterochromatin. Gene ontology analysis revealed that heterochromatin is enriched in genes with DNA-binding and regulatory activities. Immunostaining of the An. gambiae chromosomes with antibodies against Drosophila melanogaster heterochromatin protein 1 (HP1) and the nuclear envelope protein lamin Dm0 identified the major invariable sites of the proteins’ localization in all regions of pericentric heterochromatin, diffuse intercalary heterochromatin, and euchromatic region 9C of the 2R arm, but not in the compact intercalary heterochromatin. To better understand the molecular differences among chromatin types, novel Bayesian statistical models were developed to analyze genome features. The study found that heterochromatin and euchromatin differ in gene density and the coverage of retroelements and segmental duplications. The pericentric heterochromatin had the highest coverage of retroelements and tandem repeats, while intercalary heterochromatin was enriched with segmental duplications. We also provide evidence that the diffuse intercalary heterochromatin has a higher coverage of DNA transposable elements, minisatellites, and satellites than does the compact intercalary heterochromatin. The investigation of 42-Mb assembly of unmapped genomic scaffolds showed that it has molecular characteristics similar to cytologically mapped heterochromatin. Conclusions: Our results demonstrate that Anopheles polytene chromosomes and whole-genome shotgun assembly render the mapping and characterization of a significant part of heterochromatic scaffolds a possibility. These results reveal the strong association between characteristics of the genome features and morphological types of chromatin. Initial analysis of the An. gambiae heterochromatin provides a framework for its functional characterization and comparative genomic analyses with other organisms.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1626406
Journal Information:
BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 11; ISSN 1471-2164
Publisher:
SpringerCopyright Statement
Country of Publication:
United States
Language:
English

References (67)

Role of Drosophila HP1 in euchromatic gene expression journal March 2005
High Density of an SAR-Associated Motif Differentiates Heterochromatin From Euchromatin journal November 1996
Intraspecific polymorphism of sex chromosome heterochromatin in two species of the Anopheles gambiae complex journal January 1980
Satellite DNA of Anopheles stephensi liston (Diptera: Culicidae) journal May 1981
The ? heterochromatic sequences flanking the I elements are themselves defective transposable elements journal September 1989
General characteristics of the polytene chromosomes from ovarian pseudonurse cells of theDrosophila melanogaster otu 11 andfs(2)B mutants journal May 1995
Telomeres and meiosis in health and disease journal January 2007
Germline cyst development and imprinting in male mealybug Planococcus citri journal October 2004
The SuUR gene influences the distribution of heterochromatic proteins HP1 and SU(VAR)3–9 on nurse cell polytene chromosomes of Drosophila melanogaster journal April 2006
DNA underreplication in intercalary heterochromatin regions in polytene chromosomes of Drosophila melanogaster correlates with the formation of partial chromosomal aberrations and ectopic pairing journal April 2006
The dot chromosome of Drosophila: Insights into chromatin states and their change over evolutionary time journal May 2006
Binding of matrix attachment regions to lamin B1 journal September 1992
DNA from Drosophila melanogaster β-heterochromatin binds specifically to nuclear lamins in vitro and the nuclear envelope in situ journal June 1996
The molecular forms of Anopheles gambiae: A phenotypic perspective journal September 2008
Direct Evidence of a Role for Heterochromatin in Meiotic Chromosome Segregation journal July 1996
HP1: Facts, open questions, and speculation journal October 2002
Why repetitive DNA is essential to genome function journal May 2005
The Carboxyl-Terminal Region Common to Lamins A and C Contains a DNA Binding Domain journal April 2003
Y chromosome controls mating behaviour on Anopheles mosquitoes journal January 1977
Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins journal March 2001
Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain journal March 2001
Transcription and RNA interference in the formation of heterochromatin journal May 2007
Characterization of the Drosophila melanogaster genome at the nuclear lamina journal July 2006
The nuclear envelope and transcriptional control journal June 2007
Dietary palmitic acid promotes a prometastatic memory via Schwann cells journal November 2021
DNA organization and length polymorphism at the 2L telomeric region of Anopheles gambiae journal February 1998
Genomic analysis of Drosophila chromosome underreplication reveals a link between replication control and transcriptional territories journal May 2005
High-resolution analysis of Drosophila heterochromatin organization using SuUR Su(var)3-9 double mutants journal July 2007
Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome 4 and the beta-heterochromatin of Drosophila melanogaster. journal April 1988
A long interspersed repetitive element--the I factor of Drosophila teissieri--is able to transpose in different Drosophila species. journal November 1989
Interaction between an Integral Protein of the Nuclear Envelope Inner Membrane and Human Chromodomain Proteins Homologous to HP1 journal June 1996
Domain-specific Interactions of Human HP1-type Chromodomain Proteins and Inner Nuclear Membrane Protein LBR journal June 1997
Spatial organization of chromosomes in the salivary gland nuclei of Drosophila melanogaster. journal January 1986
Three-dimensional organization of Drosophila melanogaster interphase nuclei. I. Tissue-specific aspects of polytene nuclear architecture. journal June 1987
Heterochromatin protein 1 (HP1) is associated with induced gene expression in Drosophila euchromatin journal May 2003
Is HP1 an RNA detector that functions both in repression and activation? journal May 2003
InterProScan - an integration platform for the signature-recognition methods in InterPro journal September 2001
Selective Introgression of Paracentric Inversions Between Two Sibling Species of the Anopheles gambiae Complex journal May 1997
Linear and Spatial Organization of Polytene Chromosomes of the African Malaria Mosquito Anopheles funestus journal September 2001
Reassociation Kinetics of Anopheles gambiae (Diptera: Culicidae) DNA journal January 1992
A Standard Cytogenetic Photomap for the Mosquito Anopheles stephensi (Diptera: Culicidae): Application for Physical Mapping journal September 2006
The chromo shadow domain, a second chromo domain in heterochromatin-binding protein 1, HP1 journal January 1995
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
Molecular characterization of the Anopheles gambiae 2L telomeric region via an integrated transgene journal February 1996
Genetic association of physically unlinked islands of genomic divergence in incipient species ofAnopheles gambiae journal March 2010
Requirement of Heterochromatin for Cohesion at Centromeres journal October 2001
The Genome Sequence of the Malaria Mosquito Anopheles gambiae journal October 2002
Two Dobzhansky-Muller Genes Interact to Cause Hybrid Lethality in Drosophila journal November 2006
The Release 5.1 Annotation of Drosophila melanogaster Heterochromatin journal June 2007
Sequence Finishing and Mapping of Drosophila melanogaster Heterochromatin journal June 2007
Identification of a Nonhistone Chromosomal Protein Associated with Heterochromatin in Drosophila melanogaster and Its Gene journal November 1986
A genetic and molecular profile of third chromosome centric heterochromatin inDrosophilamelanogaster journal August 2005
Multiple Roles for Heterochromatin Protein 1 Genes in Drosophila journal December 2009
Heterochromatin and Gene Expression in Drosophila journal December 1995
Heterochromatic sequences in a Drosophila whole-genome shotgun assembly journal January 2002
Comparison of dot chromosome sequences from D. melanogaster and D. virilisreveals an enrichment of DNA transposon sequences in heterochromatic domains journal February 2006
The Heterochromatin Protein 1 family journal July 2006
In vivo association of lamins with nucleic acids in Drosophila melanogaster journal January 1998
Genomic Islands of Speciation in Anopheles gambiae journal August 2005
Positive Selection Drives the Evolution of rhino, a Member of the Heterochromatin Protein 1 Family in Drosophila journal January 2005
Mosaic Genome Architecture of the Anopheles gambiae Species Complex journal November 2007
An Investigation of Heterochromatin Domains on the Fourth Chromosome ofDrosophila melanogaster journal March 2008

Cited By (19)

Genome-Wide Patterns of Polymorphism in an Inbred Line of the African Malaria Mosquito Anopheles gambiae journal November 2014
In depth annotation of the Anopheles gambiae mosquito midgut transcriptome journal July 2014
Genomic composition and evolution of Aedes aegyptichromosomes revealed by the analysis of physically mapped supercontigs journal April 2014
Comparative analysis of grapevine whole-genome gene predictions, functional annotation, categorization and integration of the predicted gene sequences journal May 2012
Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi journal September 2014
Evolutionary Dynamics of the Ty3/Gypsy LTR Retrotransposons in the Genome of Anopheles gambiae journal January 2011
Tissue-Specific Differences in the Spatial Interposition of X-Chromosome and 3R Chromosome Regions in the Malaria Mosquito Anopheles messeae Fall. journal February 2015
Genome-Wide Divergence in the West-African Malaria Vector Anopheles melas journal September 2016
Three-dimensional Organization of Polytene Chromosomes in Somatic and Germline Tissues of Malaria Mosquitoes journal February 2020
The Development of Cytogenetic Maps for Malaria Mosquitoes journal September 2018
Genome-wide QTL mapping of saltwater tolerance in sibling species of Anopheles (malaria vector) mosquitoes journal April 2015
Adaptive introgression between Anopheles sibling species eliminates a major genomic island but not reproductive isolation journal June 2014
Whole-genome sequencing reveals high complexity of copy number variation at insecticide resistance loci in malaria mosquitoes journal July 2019
Chromosome inversions and ecological plasticity in the main African malaria mosquitoes: ECOLOGY OF INVERSIONS IN Anopheles journal February 2017
Increased production of piRNAs from euchromatic clusters and genes in Anopheles gambiae compared with Drosophila melanogaster journal November 2015
Ecological Genomics of Anopheles gambiae Along a Latitudinal Cline: A Population-Resequencing Approach journal April 2012
A High-Quality De novo Genome Assembly from a Single Mosquito Using PacBio Sequencing. text January 2019
A High-Quality De novo Genome Assembly from a Single Mosquito Using PacBio Sequencing journal January 2019
Chromosome and Genome Divergence between the Cryptic Eurasian Malaria Vector-Species Anopheles messeae and Anopheles daciae journal February 2020

Similar Records

Local chromatin structure of heterochromatin regulates repeated DNA stability, nucleolus structure, and genome integrity
Thesis/Dissertation · Sun Dec 31 23:00:00 EST 2006 · OSTI ID:913167
Mammalian ChlR1 has a role in heterochromatin organization
Journal Article · Sat Oct 15 00:00:00 EDT 2011 · Experimental Cell Research · OSTI ID:22212180
Molecular features of heterochromatin condensation
Conference · Thu Dec 30 23:00:00 EST 1993 · OSTI ID:28439

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biotechnology & Applied Microbiology
Genetics & Heredity