Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution

Mudd, Austin B.; Bredeson, Jessen V.; Baum, Rachel; Hockemeyer, Dirk; Rokhsar, Daniel S.

doi:10.1038/s42003-020-1096-9

Title: Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution

Abstract

Abstract Closely related muntjac deer show striking karyotype differences. Here we describe chromosome-scale genome assemblies for Chinese and Indian muntjacs, Muntiacus reevesi (2 n = 46) and Muntiacus muntjak vaginalis (2 n = 6/7), and analyze their evolution and architecture. The genomes show extensive collinearity with each other and with other deer and cattle. We identified numerous fusion events unique to and shared by muntjacs relative to the cervid ancestor, confirming many cytogenetic observations with genome sequence. One of these M. muntjak fusions reversed an earlier fission in the cervid lineage. Comparative Hi-C analysis showed that the chromosome fusions on the M. muntjak lineage altered long-range, three-dimensional chromosome organization relative to M. reevesi in interphase nuclei including A/B compartment structure. This reshaping of multi-megabase contacts occurred without notable change in local chromatin compaction, even near fusion sites. A few genes involved in chromosome maintenance show evidence for rapid evolution, possibly associated with the dramatic changes in karyotype.

Authors:

;

; Baum, Rachel;

;

Publication Date:: 2020-09-01

Research Org.:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Institutes of Health (NIH)

OSTI Identifier:: 1657263

Alternate Identifier(s):: OSTI ID: 1817128

Grant/Contract Number:: AC02-05CH11231; R01GM086321; R01HD080708; R01CA196884; T32GM007127; T32HG000047; T32GM066698; S10OD018174; S10OD010786

Resource Type:: Published Article

Journal Name:: Communications Biology

Additional Journal Information:: Journal Name: Communications Biology Journal Volume: 3 Journal Issue: 1; Journal ID: ISSN 2399-3642

Publisher:: Nature Publishing Group

Country of Publication:: United Kingdom

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; comparative genomics; evolutionary genetics; genome evolution

Citation Formats


                    Mudd, Austin B., Bredeson, Jessen V., Baum, Rachel, Hockemeyer, Dirk, and Rokhsar, Daniel S. Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution.  United Kingdom: N. p., 2020. 
Web.  doi:10.1038/s42003-020-1096-9.

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                    Mudd, Austin B., Bredeson, Jessen V., Baum, Rachel, Hockemeyer, Dirk, & Rokhsar, Daniel S. Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution.  United Kingdom.  https://doi.org/10.1038/s42003-020-1096-9

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                    Mudd, Austin B., Bredeson, Jessen V., Baum, Rachel, Hockemeyer, Dirk, and Rokhsar, Daniel S. Tue .  
"Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution".  United Kingdom.  https://doi.org/10.1038/s42003-020-1096-9.

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@article{osti_1657263,

  title        = {Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution},

  author       = {Mudd, Austin B. and Bredeson, Jessen V. and Baum, Rachel and Hockemeyer, Dirk and Rokhsar, Daniel S.},

  abstractNote = {Abstract Closely related muntjac deer show striking karyotype differences. Here we describe chromosome-scale genome assemblies for Chinese and Indian muntjacs, Muntiacus reevesi (2 n  = 46) and Muntiacus muntjak vaginalis (2 n  = 6/7), and analyze their evolution and architecture. The genomes show extensive collinearity with each other and with other deer and cattle. We identified numerous fusion events unique to and shared by muntjacs relative to the cervid ancestor, confirming many cytogenetic observations with genome sequence. One of these M. muntjak fusions reversed an earlier fission in the cervid lineage. Comparative Hi-C analysis showed that the chromosome fusions on the M. muntjak lineage altered long-range, three-dimensional chromosome organization relative to M. reevesi in interphase nuclei including A/B compartment structure. This reshaping of multi-megabase contacts occurred without notable change in local chromatin compaction, even near fusion sites. A few genes involved in chromosome maintenance show evidence for rapid evolution, possibly associated with the dramatic changes in karyotype.},

  doi          = {10.1038/s42003-020-1096-9},

  journal      = {Communications Biology},

  number       = 1,

  volume       = 3,

  place        = {United Kingdom},

  year         = {2020},

  month        = {9}

}

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Many animal species are susceptible to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection and could act as reservoirs; however, transmission in free-living animals has not been documented. White-tailed deer, the predominant cervid in North America, are susceptible to SARS-CoV-2 infection, and experimentally infected fawns can transmit the virus. To test the hypothesis that SARS-CoV-2 is circulating in deer, 283 retropharyngeal lymph node (RPLN) samples collected from 151 free-living and 132 captive deer in Iowa from April 2020 through January of 2021 were assayed for the presence of SARS-CoV-2 RNA. Ninety-four of the 283 (33.2%) deer samples were positive formore »« less
https://doi.org/10.1073/pnas.2121644119

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A correlation between ultraviolet-induced sister chromatid exchanges and ultraviolet-indced mutagenesis in ''Muntiacus muntjak'' (Indian Muntjac) skin fibroblasts in culture

Thesis/Dissertation Lugo, M H

The purpose of this thesis was to develop the capability of simultaneously assaying SCEs and mutations in Indian muntjac cells to determine (1) the relationship between the ultraviolet radiation (UVR) induction of SCEs and the UVR induction of mutations at the (UVR) HGPRT locus in Indian muntjac cells and (2) the possible role of DNA repair in the UVR induction of these two events. Indian muntjac skin fibroblasts were chosen for this study because of a unique karyotype consisting of a diploid chromosome number of 6 in females and 7 in males. An HGPRT mutation assay in Indian muntjac cellsmore »« less
Purification of the chromosomes of the Indian muntjac by flow sorting

Journal Article Carrano, A V ; Gray, J W ; Moore, II, D H ; ... - J. Histochem. Cytochem.; (United States)

Metaphase chromosomes were isolated from a male Indian muntjac cell line, were stained with ethidium bromide and were analyzed by flow microfluorometry to establish a deoxyribonucleic acid (DNA)-based karyotype. Five major peaks were evident on the chromosomal DNA distribution corresponding to the five chromosome types in this species. The amount of DNA in each chromosome was confirmed by cytophotometric measurements of intact metaphase spreads. The five chromosome types were separated by flow sorting at rates up to several hundred chromosomes per second. The sorted chromosomes were identified by morphology and by Giemsa banding patterns. The autosomes, Numbers 1, 2 andmore »« less
https://doi.org/10.1177/24.1.1254929

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Title: Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution

Abstract

Citation Formats

Rapid and Parallel Chromosomal Number Reductions in Muntjac Deer Inferred from Mitochondrial DNA Phylogeny journal, September 2000

Evolutionary rate of the mammalian karyotype journal, May 1981

Origin of human chromosome 2: an ancestral telomere-telomere fusion. journal, October 1991

UniProt: the universal protein knowledgebase journal, November 2016

Rapid speciation and chromosomal evolution in mammals. journal, September 1977

HAL: a hierarchical format for storing and analyzing multiple genome alignments journal, March 2013

Rates of Karyotype Evolution journal, June 1983

Clustal W and Clustal X version 2.0 journal, September 2007

Rapid Karyotype Evolution in Lasiopodomys Involved at Least Two Autosome – Sex Chromosome Translocations journal, December 2016

Chromosome Studies in Some Deer, the Springbok, and the Pronghorn, with Notes on Placentation in Deer journal, January 1967

Aligning Multiple Genomic Sequences With the Threaded Blockset Aligner journal, April 2004

Cactus: Algorithms for genome multiple sequence alignment journal, June 2011

Fast and accurate short read alignment with Burrows-Wheeler transform journal, May 2009

Indian Momtjac, Muntiacus muntiak: A Deer with a Low Diploid Chromosome Number journal, June 1970

Cetartiodactyla: Updating a time-calibrated molecular phylogeny journal, April 2019

Characterization of ancestral chromosome fusion points in the Indian muntjac deer journal, February 2004

A comparative study of karyotypes of muntjacs by chromosome painting journal, May 1995

Circos: An information aesthetic for comparative genomics journal, June 2009

POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end journal, June 2005

Segmental homology among cattle (Bos taurus), Indian muntjac (Muntiacus muntjak vaginalis), and Chinese muntjac (M. reevesi) karyotypes journal, January 1997

Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments journal, July 2016

Estimating divergence times in large molecular phylogenies journal, November 2012

Karyotypic Evolution in Bats: Evidence of Extensive and Conservative Chromosomal Evolution in Closely Related Taxa journal, September 1980

Estimating TimeTrees with MEGA and the TimeTree Resource journal, June 2018

Draft genomic data of the Reindeer (Rangifer tarandus). dataset, January 2017

Repbase Update, a database of repetitive elements in eukaryotic genomes journal, June 2015

SeqKit: A Cross-Platform and Ultrafast Toolkit for FASTA/Q File Manipulation journal, October 2016

Gametogenesis in a male Indian muntjac × Chinese muntjac hybrid journal, January 1981

A Deer (Subfamily Cervinae) Genetic Linkage Map and the Evolution of Ruminant Genomes journal, April 2002

Karyotype relationships among selected deer species and cattle revealed by bovine FISH probes journal, November 2017

Genome evolution in the allotetraploid frog Xenopus laevis journal, October 2016

Millions of Years Behind: Slow Adaptation of Ruminants to Grasslands journal, June 2017

New evidence for tandem chromosome fusions in the karyotypic evolution of Asian muntjacs journal, October 1991

Causes and consequences of aneuploidy in cancer journal, January 2012

Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression journal, July 2019

Likelihood Models for Detecting Positively Selected Amino Acid Sites and Applications to the HIV-1 Envelope Gene journal, March 1998

New insights into the karyotypic relationships of Chinese muntjac (Muntiacus reevesi), forest musk deer (Moschus berezovskii) and gayal (Bos frontalis) journal, December 2004

The 10kTrees website: A new online resource for primate phylogeny journal, May 2010

Comparative genomic analysis links karyotypic evolution with genomic evolution in the Indian Muntjac (Muntiacus muntjak vaginalis) journal, June 2006

Chromosome Segregation Is Biased by Kinetochore Size journal, May 2018

Phylogenomics of several deer species revealed by comparative chromosome painting with Chinese muntjac paints journal, May 2006

Comparative and demographic analysis of orang-utan genomes journal, January 2011

Juicebox Provides a Visualization System for Hi-C Contact Maps with Unlimited Zoom journal, July 2016

The sheep genome illuminates biology of the rumen and lipid metabolism journal, June 2014

InterProScan 5: genome-scale protein function classification journal, January 2014

Using intron position conservation for homology-based gene prediction journal, February 2016

Adaptive seeds tame genomic sequence comparison journal, January 2011

Localization of the repetitive telomeric sequence (TTAGGG)n in two muntjac species and implications for their karyotypic evolution journal, January 1990

A whole-genome assembly of the domestic cow, Bos taurus journal, January 2009

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal, January 2014

Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads journal, April 2014

Human Telomerase Can Immortalize Indian Muntjac Cells journal, November 2002

Comparative cytogenetic studies on the red muntjac, Chinese muntjac, and their F1 hybrids journal, January 1980

Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome journal, October 2009

De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds journal, March 2017

OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species journal, May 2015

Comparative gene mapping in cattle, Indian muntjac, and Chinese muntjac by fluorescence in situ hybridization journal, February 2008

High-density comparative BAC mapping in the black muntjac (Muntiacus crinifrons): Molecular cytogenetic dissection of the origin of MCR 1p+4 in the X1X2Y1Y2Y3 sex chromosome system journal, May 2006

Taxonomic structure and functional association of foxtail millet root microbiome journal, September 2017

Comparative sequence analyses reveal sites of ancestral chromosomal fusions in the Indian muntjac genome journal, January 2008

Massive Genomic Rearrangement Acquired in a Single Catastrophic Event during Cancer Development journal, January 2011

BLAST+: architecture and applications journal, January 2009

Purification of the chromosomes of the Indian muntjac by flow sorting. journal, January 1976

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets journal, March 2016

The red deer Cervus elaphus genome CerEla1.0: sequencing, annotating, genes, and chromosomes journal, January 2018

Direct determination of diploid genome sequences journal, April 2017

Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits journal, June 2019

Evaluation of GRCh38 and de novo haploid genome assemblies demonstrates the enduring quality of the reference assembly journal, April 2017

Gibbon genome and the fast karyotype evolution of small apes journal, September 2014

Comparison of G-, Q-, and EM-banding patterns exhibited by the chromosome complement of the Indian muntjac, Muntiacus muntjak, with reference to nuclear DNA content and chromatin ultrastructure journal, January 1975

Comparative genomics: tracking chromosome evolution in the family Ursidae using reciprocal chromosome painting journal, January 1998

Defining the orientation of the tandem fusions that occurred during the evolution of Indian muntjac chromosomes by BAC mapping journal, July 2005

The possibility of latent centromeres and a proposed nomenclature system for total chromosome and whole arm translocations journal, January 1975

Evolution's cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes journal, September 2003

PAML 4: Phylogenetic Analysis by Maximum Likelihood journal, April 2007

Interstitial localization of telomeric DNA sequences in the Indian muntjac chromosomes: further evidence for tandem chromosome fusions in the karyotypic evolution of the Asian muntjacs journal, January 1993

Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks journal, February 2019

Rapid and Parallel Chromosomal Number Reductions in Muntjac Deer Inferred from Mitochondrial DNA Phylogeny
journal, September 2000

Evolutionary rate of the mammalian karyotype
journal, May 1981

Origin of human chromosome 2: an ancestral telomere-telomere fusion.
journal, October 1991

UniProt: the universal protein knowledgebase
journal, November 2016

Rapid speciation and chromosomal evolution in mammals.
journal, September 1977

HAL: a hierarchical format for storing and analyzing multiple genome alignments
journal, March 2013

Rates of Karyotype Evolution
journal, June 1983

Clustal W and Clustal X version 2.0
journal, September 2007

Rapid Karyotype Evolution in Lasiopodomys Involved at Least Two Autosome – Sex Chromosome Translocations
journal, December 2016

Chromosome Studies in Some Deer, the Springbok, and the Pronghorn, with Notes on Placentation in Deer
journal, January 1967

Aligning Multiple Genomic Sequences With the Threaded Blockset Aligner
journal, April 2004

Cactus: Algorithms for genome multiple sequence alignment
journal, June 2011

Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009

Indian Momtjac, Muntiacus muntiak: A Deer with a Low Diploid Chromosome Number
journal, June 1970

Cetartiodactyla: Updating a time-calibrated molecular phylogeny
journal, April 2019

Characterization of ancestral chromosome fusion points in the Indian muntjac deer
journal, February 2004

A comparative study of karyotypes of muntjacs by chromosome painting
journal, May 1995

Circos: An information aesthetic for comparative genomics
journal, June 2009

POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end
journal, June 2005

Segmental homology among cattle (Bos taurus), Indian muntjac (Muntiacus muntjak vaginalis), and Chinese muntjac (M. reevesi) karyotypes
journal, January 1997

Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments
journal, July 2016

Estimating divergence times in large molecular phylogenies
journal, November 2012

Karyotypic Evolution in Bats: Evidence of Extensive and Conservative Chromosomal Evolution in Closely Related Taxa
journal, September 1980

Estimating TimeTrees with MEGA and the TimeTree Resource
journal, June 2018

Draft genomic data of the Reindeer (Rangifer tarandus).
dataset, January 2017

Repbase Update, a database of repetitive elements in eukaryotic genomes
journal, June 2015

SeqKit: A Cross-Platform and Ultrafast Toolkit for FASTA/Q File Manipulation
journal, October 2016

Gametogenesis in a male Indian muntjac × Chinese muntjac hybrid
journal, January 1981

A Deer (Subfamily Cervinae) Genetic Linkage Map and the Evolution of Ruminant Genomes
journal, April 2002

Karyotype relationships among selected deer species and cattle revealed by bovine FISH probes
journal, November 2017

Genome evolution in the allotetraploid frog Xenopus laevis
journal, October 2016

Millions of Years Behind: Slow Adaptation of Ruminants to Grasslands
journal, June 2017

New evidence for tandem chromosome fusions in the karyotypic evolution of Asian muntjacs
journal, October 1991

Causes and consequences of aneuploidy in cancer
journal, January 2012

Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression
journal, July 2019

Likelihood Models for Detecting Positively Selected Amino Acid Sites and Applications to the HIV-1 Envelope Gene
journal, March 1998

New insights into the karyotypic relationships of Chinese muntjac (Muntiacus reevesi), forest musk deer (Moschus berezovskii) and gayal (Bos frontalis)
journal, December 2004

The 10kTrees website: A new online resource for primate phylogeny
journal, May 2010

Comparative genomic analysis links karyotypic evolution with genomic evolution in the Indian Muntjac (Muntiacus muntjak vaginalis)
journal, June 2006

Chromosome Segregation Is Biased by Kinetochore Size
journal, May 2018

Phylogenomics of several deer species revealed by comparative chromosome painting with Chinese muntjac paints
journal, May 2006

Comparative and demographic analysis of orang-utan genomes
journal, January 2011

Juicebox Provides a Visualization System for Hi-C Contact Maps with Unlimited Zoom
journal, July 2016

The sheep genome illuminates biology of the rumen and lipid metabolism
journal, June 2014

InterProScan 5: genome-scale protein function classification
journal, January 2014

Using intron position conservation for homology-based gene prediction
journal, February 2016

Adaptive seeds tame genomic sequence comparison
journal, January 2011

Localization of the repetitive telomeric sequence (TTAGGG)_n in two muntjac species and implications for their karyotypic evolution
journal, January 1990

A whole-genome assembly of the domestic cow, Bos taurus
journal, January 2009

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014

Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads
journal, April 2014

Human Telomerase Can Immortalize Indian Muntjac Cells
journal, November 2002

Comparative cytogenetic studies on the red muntjac, Chinese muntjac, and their F₁ hybrids
journal, January 1980

Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome
journal, October 2009

De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds
journal, March 2017

OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species
journal, May 2015

Comparative gene mapping in cattle, Indian muntjac, and Chinese muntjac by fluorescence in situ hybridization
journal, February 2008

High-density comparative BAC mapping in the black muntjac (Muntiacus crinifrons): Molecular cytogenetic dissection of the origin of MCR 1p+4 in the X1X2Y1Y2Y3 sex chromosome system
journal, May 2006

Taxonomic structure and functional association of foxtail millet root microbiome
journal, September 2017

Comparative sequence analyses reveal sites of ancestral chromosomal fusions in the Indian muntjac genome
journal, January 2008

Massive Genomic Rearrangement Acquired in a Single Catastrophic Event during Cancer Development
journal, January 2011

BLAST+: architecture and applications
journal, January 2009

Purification of the chromosomes of the Indian muntjac by flow sorting.
journal, January 1976

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

The red deer Cervus elaphus genome CerEla1.0: sequencing, annotating, genes, and chromosomes
journal, January 2018

Direct determination of diploid genome sequences
journal, April 2017

Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits
journal, June 2019

Evaluation of GRCh38 and de novo haploid genome assemblies demonstrates the enduring quality of the reference assembly
journal, April 2017

Gibbon genome and the fast karyotype evolution of small apes
journal, September 2014

Comparison of G-, Q-, and EM-banding patterns exhibited by the chromosome complement of the Indian muntjac, Muntiacus muntjak, with reference to nuclear DNA content and chromatin ultrastructure
journal, January 1975

Comparative genomics: tracking chromosome evolution in the family Ursidae using reciprocal chromosome painting
journal, January 1998

Defining the orientation of the tandem fusions that occurred during the evolution of Indian muntjac chromosomes by BAC mapping
journal, July 2005

The possibility of latent centromeres and a proposed nomenclature system for total chromosome and whole arm translocations
journal, January 1975

Evolution's cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes
journal, September 2003

PAML 4: Phylogenetic Analysis by Maximum Likelihood
journal, April 2007

Interstitial localization of telomeric DNA sequences in the Indian muntjac chromosomes: further evidence for tandem chromosome fusions in the karyotypic evolution of the Asian muntjacs
journal, January 1993

Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks
journal, February 2019

Insights into Conifer Giga-Genomes
journal, October 2014

Ensembl 2019
journal, November 2018

Tandem chromosome fusions in karyotypic evolution of Muntiacus: evidence from M. feae and M. gongshanensis
journal, September 2006