Migrators within migrators: exploring transposable element dynamics in the monarch butterfly, Danaus plexippus.

Butterfly Danaus plexippus Genome Evolution Genomic Deletion Lepidoptera Repeat TE Annotation Transposon

Journal

Mobile DNA

ISSN: 1759-8753

Titre abrégé: Mob DNA

Pays: England

ID NLM: 101519891

Informations de publication

Date de publication:
16 Feb 2022

Historique:

received: 29 09 2021

accepted: 06 02 2022

entrez: 17 2 2022

pubmed: 18 2 2022

medline: 18 2 2022

Statut: epublish

Résumé

Lepidoptera (butterflies and moths) are an important model system in ecology and evolution. A high-quality chromosomal genome assembly is available for the monarch butterfly (Danaus plexippus), but it lacks an in-depth transposable element (TE) annotation, presenting an opportunity to explore monarch TE dynamics and the impact of TEs on shaping the monarch genome. We find 6.21% of the monarch genome is comprised of TEs, a reduction of 6.85% compared to the original TE annotation performed on the draft genome assembly. Monarch TE content is low compared to two closely related species with available genomes, Danaus chrysippus (33.97% TE) and Danaus melanippus (11.87% TE). The biggest TE contributions to genome size in the monarch are LINEs and Penelope-like elements, and three newly identified families, r2-hero_dPle (LINE), penelope-1_dPle (Penelope-like), and hase2-1_dPle (SINE), collectively contribute 34.92% of total TE content. We find evidence of recent TE activity, with two novel Tc1 families rapidly expanding over recent timescales (tc1-1_dPle, tc1-2_dPle). LINE fragments show signatures of genomic deletions indicating a high rate of TE turnover. We investigate associations between TEs and wing colouration and immune genes and identify a three-fold increase in TE content around immune genes compared to other host genes. We provide a detailed TE annotation and analysis for the monarch genome, revealing a considerably smaller TE contribution to genome content compared to two closely related Danaus species with available genome assemblies. We identify highly successful novel DNA TE families rapidly expanding over recent timescales, and ongoing signatures of both TE expansion and removal highlight the dynamic nature of repeat content in the monarch genome. Our findings also suggest that insect immune genes are promising candidates for future interrogation of TE-mediated host adaptation.

Sections du résumé

BACKGROUND BACKGROUND

RESULTS RESULTS

We find 6.21% of the monarch genome is comprised of TEs, a reduction of 6.85% compared to the original TE annotation performed on the draft genome assembly. Monarch TE content is low compared to two closely related species with available genomes, Danaus chrysippus (33.97% TE) and Danaus melanippus (11.87% TE). The biggest TE contributions to genome size in the monarch are LINEs and Penelope-like elements, and three newly identified families, r2-hero_dPle (LINE), penelope-1_dPle (Penelope-like), and hase2-1_dPle (SINE), collectively contribute 34.92% of total TE content. We find evidence of recent TE activity, with two novel Tc1 families rapidly expanding over recent timescales (tc1-1_dPle, tc1-2_dPle). LINE fragments show signatures of genomic deletions indicating a high rate of TE turnover. We investigate associations between TEs and wing colouration and immune genes and identify a three-fold increase in TE content around immune genes compared to other host genes.

CONCLUSIONS CONCLUSIONS

We provide a detailed TE annotation and analysis for the monarch genome, revealing a considerably smaller TE contribution to genome content compared to two closely related Danaus species with available genome assemblies. We identify highly successful novel DNA TE families rapidly expanding over recent timescales, and ongoing signatures of both TE expansion and removal highlight the dynamic nature of repeat content in the monarch genome. Our findings also suggest that insect immune genes are promising candidates for future interrogation of TE-mediated host adaptation.

Identifiants

DOI: 10.1186/s13100-022-00263-5 PMID: 35172896 PMC: PMC8848866

pubmed: 35172896

doi: 10.1186/s13100-022-00263-5

pii: 10.1186/s13100-022-00263-5

pmc: PMC8848866

doi:

Types de publication

Journal Article

Langues

eng

Pagination

Subventions

Organisme : Biotechnology and Biological Sciences Research Council

ID : BB/M009122/1

Pays : United Kingdom

Organisme : Biotechnology and Biological Sciences Research Council

ID : BB/N020146/1

Pays : United Kingdom

Informations de copyright

Références

Genetics. 2005 Nov;171(3):1183-94

pubmed: 16157677

Nat Genet. 2005 Sep;37(9):997-1002

pubmed: 16056225

Bioinformatics. 2012 Dec 1;28(23):3150-2

pubmed: 23060610

Trends Ecol Evol. 2000 Mar;15(3):95-99

pubmed: 10675923

Curr Biol. 2019 Dec 2;29(23):4071-4077.e3

pubmed: 31735674

Genome Biol Evol. 2018 Jan 1;10(1):304-318

pubmed: 29281015

Genome Res. 2002 Aug;12(8):1269-76

pubmed: 12176934

Plant Mol Biol. 2000 Jan;42(1):251-69

pubmed: 10688140

Nucleic Acids Res. 2014 Jan;42(Database issue):D7-17

pubmed: 24259429

Genome Biol Evol. 2018 Nov 1;10(11):3038-3057

pubmed: 30252073

J Mol Evol. 1980 Dec;16(2):111-20

pubmed: 7463489

Genome Biol Evol. 2012;4(5):687-702

pubmed: 22534163

Sci Rep. 2018 Sep 6;8(1):13332

pubmed: 30190506

Nature. 2006 Oct 5;443(7111):521-4

pubmed: 17024082

Nucleic Acids Res. 2016 Jan 4;44(D1):D81-9

pubmed: 26612867

Nature. 2006 May 4;441(7089):87-90

pubmed: 16625209

Genome Biol. 2018 Nov 19;19(1):199

pubmed: 30454069

Nat Rev Genet. 2011 Aug 18;12(9):615-27

pubmed: 21850042

Nat Genet. 2007 Dec;39(12):1461-8

pubmed: 17987029

Annu Rev Genomics Hum Genet. 2007;8:241-59

pubmed: 17506661

Genome Biol Evol. 2019 Aug 1;11(8):2162-2177

pubmed: 31214686

Elife. 2019 Jan 08;8:

pubmed: 30620335

Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):196-201

pubmed: 8990185

Genome Res. 2018 Jun;28(6):824-835

pubmed: 29712752

Bioinformatics. 2017 Oct 1;33(19):3088-3090

pubmed: 28575171

Mol Biol Evol. 2013 Apr;30(4):772-80

pubmed: 23329690

Bioinformatics. 2014 Nov 15;30(22):3276-8

pubmed: 25095880

Genome Biol Evol. 2016 Jan 21;8(2):403-10

pubmed: 26802115

Nature. 2010 Apr 29;464(7293):1347-50

pubmed: 20428170

Biol Lett. 2021 Sep;17(9):20210342

pubmed: 34464541

Nature. 2016 Jun 01;534(7605):102-5

pubmed: 27251284

Nat Rev Genet. 2001 Apr;2(4):256-67

pubmed: 11283698

Mol Biol Evol. 2012 Dec;29(12):3685-702

pubmed: 22826456

DNA Res. 2012;19(1):11-21

pubmed: 22086996

PLoS Comput Biol. 2016 Jun 16;12(6):e1004956

pubmed: 27309962

Bioinformatics. 2013 Oct 1;29(19):2487-9

pubmed: 23842809

Mol Ecol. 2019 Mar;28(6):1537-1549

pubmed: 30003608

Cytogenet Genome Res. 2005;110(1-4):462-7

pubmed: 16093699

Biotechniques. 2005 Apr;38(4):561-5

pubmed: 15884674

Nat Rev Genet. 2017 May;18(5):292-308

pubmed: 28286338

Trends Genet. 2000 Jun;16(6):276-7

pubmed: 10827456

Bioinformatics. 2005 Jun;21 Suppl 1:i351-8

pubmed: 15961478

Heredity (Edinb). 2016 May;116(5):466-76

pubmed: 26860199

Nat Rev Genet. 2008 May;9(5):397-405

pubmed: 18368054

Genome Biol Evol. 2017 Oct 1;9(10):2491-2505

pubmed: 28981642

Bioessays. 2006 Sep;28(9):913-22

pubmed: 16937363

Cell Mol Life Sci. 2015 Nov;72(21):4063-76

pubmed: 26223268

Cytogenet Genome Res. 2005;110(1-4):510-21

pubmed: 16093704

Cytogenet Genome Res. 2005;110(1-4):25-34

pubmed: 16093655

Gene. 2016 Dec 5;594(1):151-159

pubmed: 27614292

Int Immunol. 2000 Jun;12(6):757-65

pubmed: 10837403

Mol Ecol. 2013 Mar;22(6):1503-17

pubmed: 23293987

Nat Rev Genet. 2012 Mar 06;13(4):233-45

pubmed: 22392219

Curr Opin Genet Dev. 2016 Apr;37:90-100

pubmed: 26855260

Curr Biol. 2018 Mar 5;28(5):770-778.e5

pubmed: 29456146

Gene. 2012 Nov 1;509(1):7-15

pubmed: 22921893

Gene. 2007 Oct 15;401(1-2):165-71

pubmed: 17716834

PLoS Genet. 2007 Nov;3(11):e210

pubmed: 18081425

Nature. 2014 Oct 16;514(7522):317-21

pubmed: 25274300

Genes Dev. 2019 Sep 1;33(17-18):1098-1116

pubmed: 31481535

Insect Biochem Mol Biol. 2008 Dec;38(12):1046-57

pubmed: 19280695

Cell. 2002 May 3;109(3):371-81

pubmed: 12015986

Nat Commun. 2012 Jan 10;3:621

pubmed: 22233631

PLoS Genet. 2019 Feb 1;15(2):e1007965

pubmed: 30707693

Genome Biol Evol. 2012;4(8):689-99

pubmed: 22798449

Mob DNA. 2012 Sep 26;3(1):14

pubmed: 23013939

Bioinformatics. 2019 Mar 15;35(6):1051-1052

pubmed: 30165587

Dev Dyn. 2009 Sep;238(9):2202-10

pubmed: 19347955

Curr Opin Genet Dev. 2018 Apr;49:15-24

pubmed: 29505963

Mol Biol Evol. 2000 May;17(5):804-12

pubmed: 10779541

Nat Rev Genet. 2017 Feb;18(2):71-86

pubmed: 27867194

Annu Rev Genet. 2007;41:331-68

pubmed: 18076328

Hum Genet. 2010 Feb;127(2):135-54

pubmed: 19823873

Biochem Soc Trans. 2008 Aug;36(Pt 4):641-7

pubmed: 18631133

Dev Biol. 2017 Jun 15;426(2):393-400

pubmed: 27297884

Zookeys. 2020 Jun 04;938:97-124

pubmed: 32550787

Mob DNA. 2016 Aug 11;7:16

pubmed: 27525044

Mol Biol Evol. 2019 Jul 1;36(7):1405-1417

pubmed: 30865231

Mol Biol Evol. 2015 Jan;32(1):268-74

pubmed: 25371430

Genome Biol Evol. 2016 Dec 14;8(11):3301-3322

pubmed: 27702814

Mob DNA. 2019 Dec 12;10:48

pubmed: 31857828

Dev Biol. 2005 Jul 15;283(2):446-58

pubmed: 15936749

Genes Dev. 2011 Sep 15;25(18):1982-96

pubmed: 21937715

Bioinformatics. 2009 Aug 1;25(15):1972-3

pubmed: 19505945

Genome Biol. 2018 Jul 9;19(1):85

pubmed: 29983116

Genetica. 2011 Jan;139(1):149-54

pubmed: 21210187

Nucleic Acids Res. 2017 Jan 4;45(D1):D200-D203

pubmed: 27899674

Mob DNA. 2019 Nov 3;10:42

pubmed: 31700550

J Hered. 2017 Mar 1;108(2):163-175

pubmed: 28003372

Gene. 2009 Dec 15;448(2):207-13

pubmed: 19651192

Genetics. 2005 Feb;169(2):1033-43

pubmed: 15731520

Nucleic Acids Res. 2013 Jan;41(Database issue):D758-63

pubmed: 23143105

Trends Genet. 2017 Nov;33(11):817-831

pubmed: 28844698

Nucleic Acids Res. 2007 Jul;35(Web Server issue):W265-8

pubmed: 17485477

Mol Biol Evol. 2003 May;20(5):674-85

pubmed: 12679549

Nat Commun. 2019 Dec 17;10(1):5757

pubmed: 31848330

Curr Opin Genet Dev. 2009 Dec;19(6):607-12

pubmed: 19914058

Nat Methods. 2017 Jun;14(6):587-589

pubmed: 28481363

Mol Biol Evol. 2007 Aug;24(8):1872-88

pubmed: 17556756

Chromosome Res. 2018 Mar;26(1-2):5-23

pubmed: 29332159

Mob DNA. 2013 Oct 02;4(1):21

pubmed: 24088337

Nature. 2016 Oct 27;538(7626):533-536

pubmed: 27760113

Philos Trans R Soc Lond B Biol Sci. 2017 Dec 19;372(1736):

pubmed: 29109221

J Evol Biol. 2014 Dec;27(12):2573-84

pubmed: 25290698

Bioinformatics. 2010 Mar 15;26(6):841-2

pubmed: 20110278

Genes Dev. 2002 Sep 15;16(18):2415-27

pubmed: 12231630

Mol Biol Evol. 2008 Apr;25(4):787-94

pubmed: 18258610

Mob DNA. 2015 Jan 17;6(1):3

pubmed: 25606061

Nat Rev Genet. 2007 Dec;8(12):973-82

pubmed: 17984973

Nature. 2012 Jul 5;487(7405):94-8

pubmed: 22722851

BMC Bioinformatics. 2009 Dec 15;10:421

pubmed: 20003500

Nucleic Acids Res. 2004 Mar 19;32(5):1792-7

pubmed: 15034147

Annu Rev Genet. 2012;46:21-42

pubmed: 22905872

Cell. 2011 Nov 23;147(5):1171-85

pubmed: 22118469

Bioessays. 2009 Jul;31(7):703-14

pubmed: 19415638

Proc Natl Acad Sci U S A. 2017 Feb 21;114(8):E1460-E1469

pubmed: 28179571

Genetica. 2002 May;115(1):49-63

pubmed: 12188048