دورية أكاديمية
Cortex cis -regulatory switches establish scale colour identity and pattern diversity in Heliconius .
العنوان: | Cortex cis -regulatory switches establish scale colour identity and pattern diversity in Heliconius . |
---|---|
المؤلفون: | Livraghi L; Department of Zoology, University of Cambridge, Downing St., Cambridge, United Kingdom.; Smithsonian Tropical Research Institute, Gamboa, Panama., Hanly JJ; Department of Zoology, University of Cambridge, Downing St., Cambridge, United Kingdom.; Smithsonian Tropical Research Institute, Gamboa, Panama.; The George Washington University Department of Biological Sciences, Science and Engineering Hall, Washington, United States., Van Bellghem SM; Department of Biology, Centre for Applied Tropical Ecology and Conservation, University of Puerto Rico, Rio Piedras, Puerto Rico., Montejo-Kovacevich G; Department of Zoology, University of Cambridge, Downing St., Cambridge, United Kingdom., van der Heijden ES; Department of Zoology, University of Cambridge, Downing St., Cambridge, United Kingdom.; Smithsonian Tropical Research Institute, Gamboa, Panama., Loh LS; The George Washington University Department of Biological Sciences, Science and Engineering Hall, Washington, United States., Ren A; The George Washington University Department of Biological Sciences, Science and Engineering Hall, Washington, United States., Warren IA; Department of Zoology, University of Cambridge, Downing St., Cambridge, United Kingdom., Lewis JJ; Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, United States., Concha C; Smithsonian Tropical Research Institute, Gamboa, Panama., Hebberecht L; Department of Zoology, University of Cambridge, Downing St., Cambridge, United Kingdom.; Smithsonian Tropical Research Institute, Gamboa, Panama., Wright CJ; Department of Zoology, University of Cambridge, Downing St., Cambridge, United Kingdom., Walker JM; Department of Zoology, University of Cambridge, Downing St., Cambridge, United Kingdom., Foley J; Smithsonian Tropical Research Institute, Gamboa, Panama., Goldberg ZH; Cell & Developmental Biology, Division of Biological Sciences, UC San Diego, La Jolla, United States., Arenas-Castro H; Smithsonian Tropical Research Institute, Gamboa, Panama., Salazar C; Biology Program, Faculty of Natural Sciences, Universidad del Rosario, Bogotá, Colombia., Perry MW; Cell & Developmental Biology, Division of Biological Sciences, UC San Diego, La Jolla, United States., Papa R; Department of Biology, Centre for Applied Tropical Ecology and Conservation, University of Puerto Rico, Rio Piedras, Puerto Rico., Martin A; The George Washington University Department of Biological Sciences, Science and Engineering Hall, Washington, United States., McMillan WO; Smithsonian Tropical Research Institute, Gamboa, Panama., Jiggins CD; Department of Zoology, University of Cambridge, Downing St., Cambridge, United Kingdom.; Smithsonian Tropical Research Institute, Gamboa, Panama. |
المصدر: | ELife [Elife] 2021 Jul 19; Vol. 10. Date of Electronic Publication: 2021 Jul 19. |
نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't; Research Support, U.S. Gov't, Non-P.H.S. |
اللغة: | English |
بيانات الدورية: | Publisher: eLife Sciences Publications, Ltd Country of Publication: England NLM ID: 101579614 Publication Model: Electronic Cited Medium: Internet ISSN: 2050-084X (Electronic) Linking ISSN: 2050084X NLM ISO Abbreviation: Elife Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: Cambridge, UK : eLife Sciences Publications, Ltd., 2012- |
مواضيع طبية MeSH: | Butterflies/*genetics , Pigments, Biological/*genetics , Wings, Animal/*physiology, Animals ; Clustered Regularly Interspaced Short Palindromic Repeats ; Color ; Phenotype |
مستخلص: | In Heliconius butterflies, wing colour pattern diversity and scale types are controlled by a few genes of large effect that regulate colour pattern switches between morphs and species across a large mimetic radiation. One of these genes, cortex , has been repeatedly associated with colour pattern evolution in butterflies. Here we carried out CRISPR knockouts in multiple Heliconius species and show that cortex is a major determinant of scale cell identity. Chromatin accessibility profiling and introgression scans identified cis -regulatory regions associated with discrete phenotypic switches. CRISPR perturbation of these regions in black hindwing genotypes recreated a yellow bar, revealing their spatially limited activity. In the H. melpomene/timareta lineage, the candidate CRE from yellow-barred phenotype morphs is interrupted by a transposable element, suggesting that cis -regulatory structural variation underlies these mimetic adaptations. Our work shows that cortex functionally controls scale colour fate and that its cis -regulatory regions control a phenotypic switch in a modular and pattern-specific fashion. Competing Interests: LL, JH, SV, GM, Ev, LL, AR, IW, JL, CC, LH, CW, JW, JF, ZG, HA, CS, MP, RP, AM, WM, CJ No competing interests declared (© 2021, Livraghi et al.) |
References: | Bioinformatics. 2009 Jul 15;25(14):1754-60. (PMID: 19451168) Genome Biol. 2014;15(12):550. (PMID: 25516281) Bioinformatics. 2018 Mar 1;34(5):867-868. (PMID: 29096012) Nat Methods. 2013 Dec;10(12):1213-8. (PMID: 24097267) Curr Biol. 2019 Dec 2;29(23):3996-4009.e4. (PMID: 31735676) Biol Lett. 2019 Oct 31;15(10):20190582. (PMID: 31615373) Mol Ecol. 2017 Oct;26(19):5160-5172. (PMID: 28777894) G3 (Bethesda). 2016 Jan 15;6(3):695-708. (PMID: 26772750) Proc Natl Acad Sci U S A. 2017 Oct 3;114(40):10701-10706. (PMID: 28923954) Genesis. 2001 Mar;29(3):141-52. (PMID: 11252055) PLoS Genet. 2009 Feb;5(2):e1000366. (PMID: 19197358) Nature. 2016 Jun 01;534(7605):102-5. (PMID: 27251284) Science. 2010 Jan 15;327(5963):302-5. (PMID: 20007865) Curr Opin Insect Sci. 2016 Oct;17:24-31. (PMID: 27720070) Proc Natl Acad Sci U S A. 2019 Sep 24;116(39):19431-19439. (PMID: 31506350) Curr Biol. 2004 Apr 6;14(7):630-6. (PMID: 15062106) Methods. 2014 Sep;69(2):128-36. (PMID: 24576617) Proc Biol Sci. 2008 Jan 7;275(1630):37-45. (PMID: 17956848) Nat Ecol Evol. 2017;1(3):52. (PMID: 28523290) Nat Biotechnol. 2019 Aug;37(8):907-915. (PMID: 31375807) Curr Biol. 2018 Nov 5;28(21):3450-3457.e13. (PMID: 30344115) Elife. 2021 Jul 19;10:. (PMID: 34280087) Mol Biol Evol. 2019 Dec 1;36(12):2842-2853. (PMID: 31504750) Nature. 2016 Jun 01;534(7605):106-10. (PMID: 27251285) J Exp Biol. 2017 Apr 01;220(Pt 7):1267-1276. (PMID: 28108668) Heredity (Edinb). 2015 May;114(5):515-24. (PMID: 25806542) Nucleic Acids Res. 2015 Jul 1;43(W1):W7-14. (PMID: 25883146) Dev Biol. 2014 Nov 15;395(2):367-78. (PMID: 25196151) PLoS Biol. 2019 Feb 7;17(2):e2006288. (PMID: 30730876) Science. 2020 Nov 6;370(6517):721-725. (PMID: 33154142) Science. 2009 Feb 6;323(5915):746-51. (PMID: 19197055) Genetics. 2015 May;200(1):1-19. (PMID: 25953905) Interface Focus. 2019 Feb 6;9(1):20180047. (PMID: 30603067) Sci Adv. 2020 Sep 25;6(39):. (PMID: 32978147) Nat Methods. 2012 Jun 28;9(7):676-82. (PMID: 22743772) Dev Dyn. 2019 Aug;248(8):657-670. (PMID: 31107575) Pigment Cell Res. 1993 Mar;6(2):85-90. (PMID: 8321868) PLoS Biol. 2016 Jan 15;14(1):e1002353. (PMID: 26771987) Development. 2007 Mar;134(5):891-9. (PMID: 17251266) Evol Dev. 2001 Nov-Dec;3(6):415-23. (PMID: 11806637) J R Soc Interface. 2018 Apr;15(141):. (PMID: 29669892) Gigascience. 2018 Dec 1;7(12):. (PMID: 30476205) Bioinformatics. 2012 Jun 15;28(12):1647-9. (PMID: 22543367) Curr Top Dev Biol. 2016;119:27-61. (PMID: 27282023) J Cell Biol. 2002 Jun 24;157(7):1139-49. (PMID: 12082076) Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8605-12. (PMID: 17494759) PLoS Biol. 2020 Feb 6;18(2):e3000597. (PMID: 32027643) Nat Rev Genet. 2020 Aug;21(8):461-475. (PMID: 32382123) Nucleic Acids Res. 2019 Jul 2;47(W1):W636-W641. (PMID: 30976793) Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):12632-7. (PMID: 22802635) Proc Natl Acad Sci U S A. 2019 Nov 26;116(48):24174-24183. (PMID: 31712408) Proc Natl Acad Sci U S A. 2017 Oct 3;114(40):10707-10712. (PMID: 28923944) Genetics. 2017 May;206(1):429-438. (PMID: 28341652) Heredity (Edinb). 2016 Jan;116(1):52-9. (PMID: 26219230) Mol Biol Evol. 2019 Jan 1;36(1):159-173. (PMID: 30452724) Mol Ecol. 2021 May;30(9):1946-1961. (PMID: 33464655) Methods. 2001 Dec;25(4):402-8. (PMID: 11846609) PLoS Genet. 2007 Nov;3(11):e202. (PMID: 18020708) Heredity (Edinb). 2019 Aug;123(2):138-152. (PMID: 30670842) Development. 2004 Jul;131(13):3169-81. (PMID: 15175253) Genome Biol Evol. 2021 Jul 6;13(7):. (PMID: 33944917) J Insect Sci. 2016 Jun 07;16(1):. (PMID: 27271971) Curr Biol. 2018 Nov 5;28(21):3469-3474.e4. (PMID: 30415702) J Insect Physiol. 2016 Feb;85:32-45. (PMID: 26654884) Evodevo. 2019 Jul 16;10:15. (PMID: 31341608) Science. 2011 Aug 26;333(6046):1137-41. (PMID: 21778360) Arthropod Struct Dev. 2013 Jan;42(1):37-46. (PMID: 23017249) Ecol Entomol. 2019 Jun;44(3):397-405. (PMID: 31217661) Arthropod Struct Dev. 2013 Sep;42(5):349-59. (PMID: 23792046) Evodevo. 2019 Aug 08;10:16. (PMID: 31406559) Nature. 2012 Jul 5;487(7405):94-8. (PMID: 22722851) Proc Natl Acad Sci U S A. 2022 Feb 22;119(8):. (PMID: 35169073) PLoS Biol. 2006 Oct;4(10):e303. (PMID: 17002517) Curr Biol. 2019 Jul 8;29(13):2157-2166.e6. (PMID: 31257142) Syst Biol. 2010 May;59(3):307-21. (PMID: 20525638) Annu Rev Genomics Hum Genet. 2015;16:103-31. (PMID: 26079281) |
معلومات مُعتمدة: | R00 EY027016 United States EY NEI NIH HHS; T32 GM007240 United States GM NIGMS NIH HHS; T32 GM133351 United States GM NIGMS NIH HHS; BB/R007500/1 United Kingdom BB_ Biotechnology and Biological Sciences Research Council |
فهرسة مساهمة: | Keywords: ATAC-Seq; cis-regulation; crisppr; developmental biology; evolution; evolutionary biology; heliconius; wing patterning Local Abstract: [plain-language-summary] Heliconius butterflies have bright patterns on their wings that tell potential predators that they are toxic. As a result, predators learn to avoid eating them. Over time, unrelated species of butterflies have evolved similar patterns to avoid predation through a process known as Müllerian mimicry. Worldwide, there are over 180,000 species of butterflies and moths, most of which have different wing patterns. How do genes create this pattern diversity? And do butterflies use similar genes to create similar wing patterns? One of the genes involved in creating wing patterns is called cortex . This gene has a large region of DNA around it that does not code for proteins, but instead, controls whether cortex is on or off in different parts of the wing. Changes in this non-coding region can act like switches, turning regions of the wing into different colours and creating complex patterns, but it is unclear how these switches have evolved. Butterfly wings get their colour from tiny structures called scales, which each have their own unique set of pigments. In Heliconius butterflies, there are three types of scales: yellow/white scales, black scales, and red/orange/brown scales. Livraghi et al. used a DNA editing technique called CRISPR to find out whether the cortex gene affects scale type. First, Livraghi et al. confirmed that deleting cortex turned black and red scales yellow. Next, they used the same technique to manipulate the non-coding DNA around the cortex gene to see the effect on the wing pattern. This manipulation turned a black-winged butterfly into a butterfly with a yellow wing band, a pattern that occurs naturally in Heliconius butterflies. The next step was to find the mutation responsible for the appearance of yellow wing bands in nature. It turns out that a bit of extra genetic code, derived from so-called ‘jumping genes’, had inserted itself into the non-coding DNA around the cortex gene, ‘flipping’ the switch and leading to the appearance of the yellow scales. Genetic information contains the instructions to generate shape and form in most organisms. These instructions evolve over millions of years, creating everything from bacteria to blue whales. Butterfly wings are visual evidence of evolution, but the way their genes create new patterns isn't specific to butterflies. Understanding wing patterns can help researchers to learn how genetic switches control diversity across other species too. |
سلسلة جزيئية: | Dryad 10.5061/dryad.8gtht76m0 |
المشرفين على المادة: | 0 (Pigments, Biological) |
تواريخ الأحداث: | Date Created: 20210719 Date Completed: 20211019 Latest Revision: 20231107 |
رمز التحديث: | 20240628 |
مُعرف محوري في PubMed: | PMC8289415 |
DOI: | 10.7554/eLife.68549 |
PMID: | 34280087 |
قاعدة البيانات: | MEDLINE |
تدمد: | 2050-084X |
---|---|
DOI: | 10.7554/eLife.68549 |