#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Double drives and private alleles for localised population genetic control


Autoři: Katie Willis aff001;  Austin Burt aff001
Působiště autorů: Department of Life Sciences, Imperial College London, Silwood Park, Ascot, United Kingdom aff001
Vyšlo v časopise: Double drives and private alleles for localised population genetic control. PLoS Genet 17(3): e1009333. doi:10.1371/journal.pgen.1009333
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009333

Souhrn

Synthetic gene drive constructs could, in principle, provide the basis for highly efficient interventions to control disease vectors and other pest species. This efficiency derives in part from leveraging natural processes of dispersal and gene flow to spread the construct and its impacts from one population to another. However, sometimes (for example, with invasive species) only specific populations are in need of control, and impacts on non-target populations would be undesirable. Many gene drive designs use nucleases that recognise and cleave specific genomic sequences, and one way to restrict their spread would be to exploit sequence differences between target and non-target populations. In this paper we propose and model a series of low threshold double drive designs for population suppression, each consisting of two constructs, one imposing a reproductive load on the population and the other inserted into a differentiated locus and controlling the drive of the first. Simple deterministic, discrete-generation computer simulations are used to assess the alternative designs. We find that the simplest double drive designs are significantly more robust to pre-existing cleavage resistance at the differentiated locus than single drive designs, and that more complex designs incorporating sex ratio distortion can be more efficient still, even allowing for successful control when the differentiated locus is neutral and there is up to 50% pre-existing resistance in the target population. Similar designs can also be used for population replacement, with similar benefits. A population genomic analysis of CRISPR PAM sites in island and mainland populations of the malaria mosquito Anopheles gambiae indicates that the differentiation needed for our methods to work can exist in nature. Double drives should be considered when efficient but localised population genetic control is needed and there is some genetic differentiation between target and non-target populations.

Klíčová slova:

Genetic loci – Guide RNA – Heterozygosity – Islands – Nucleases – Pest control – Population genetics – Population size


Zdroje

1. Burt A, Trivers R. Genes in conflict: the biology of selfish genetic elements. Cambridge: Belknap Press of Harvard University Press; 2006.

2. Burt A, Crisanti A. Gene drive: evolved and synthetic. ACS Chem Biol. 2018;13(2):343–6. doi: 10.1021/acschembio.7b01031 WOS:000426012800008. 29400944

3. Burt A, Coulibaly M, Crisanti A, Diabate A, Kayondo JK. Gene drive to reduce malaria transmission in sub-Saharan Africa. J Resp Innov. 2018;5:S66–S80. doi: 10.1080/23299460.2017.1419410 WOS:000434459000005.

4. Raban RR, Marshall JM, Akbari OS. Progress towards engineering gene drives for population control. J Exp Biol. 2020;223. ARTN jeb208181 doi: 10.1242/jeb.208181 WOS:000541774100005. 32034041

5. Teem JL, Alphey L, Descamps S, Edgington MP, Edwards O, Gemmell N, et al. Genetic biocontrol for invasive species. Front Bioeng Biotech. 2020;8. ARTN 452 doi: 10.3389/fbioe.2020.00452 WOS:000540500500001. 32523938

6. Hay BA, Oberhofer G, Guo M. Engineering the composition and fate of wild populations with gene drive. Ann Rev Entomol. 2021;66:407–34. Epub 2020/10/10. doi: 10.1146/annurev-ento-020117-043154 33035437

7. Beaghton A, Beaghton PJ, Burt A. Gene drive through a landscape: reaction-diffusion models of population suppression and elimination by a sex ratio distorter. Theor Pop Biol. 2016;108:51–69. doi: 10.1016/j.tpb.2015.11.005 WOS:000372560000005. 26704073

8. North AR, Burt A, Godfray HCJ. Modelling the potential of genetic control of malaria mosquitoes at national scale. BMC Biol. 2019;17. ARTN 26 doi: 10.1186/s12915-019-0645-5 WOS:000463655000001. 30922310

9. North AR, Burt A, Godfray HCJ. Modelling the suppression of a malaria vector using a CRISPR-Cas9 gene drive to reduce female fertility. BMC Biol. 2020;18(1). ARTN 98 doi: 10.1186/s12915-020-00834-z WOS:000561855300001. 32782000

10. Thomas DD, Donnelly CA, Wood RJ, Alphey LS. Insect population control using a dominant, repressible, lethal genetic system. Science. 2000;287(5462):2474–6. doi: 10.1126/science.287.5462.2474 WOS:000086202200041. 10741964

11. Galizi R, Doyle LA, Menichelli M, Bernardini F, Deredec A, Burt A, et al. A synthetic sex ratio distortion system for the control of the human malaria mosquito. Nat Commun. 2014;5. doi: 10.1038/ncomms4977 WOS:000338834900001. 24915045

12. Burt A, Deredec A. Self-limiting population genetic control with sex-linked genome editors. Proc Roy Soc Lond B. 2018;285(1883). ARTN 20180776 doi: 10.1098/rspb.2018.0776 WOS:000439907900011. 30051868

13. Gould F, Huang YX, Legros M, Lloyd AL. A killer-rescue system for self-limiting gene drive of anti-pathogen constructs. Proc Roy Soc Lond B. 2008;275(1653):2823–9. doi: 10.1098/rspb.2008.0846 WOS:000260611200006. 18765342

14. Terradas G, Buchman AB, Bennett JB, Shriner I, Marshall JM, Akbari OS, et al. Inherently confinable split-drive systems in Drosophila. Biorxiv. 2020.

15. Oberhofer G, Ivy T, Hay BA. Split versions of Cleave and Rescue selfish genetic elements for measured self limiting gene drive. PLOS Genet. 2021;17(2):e1009385. Epub 2021/02/19. doi: 10.1371/journal.pgen.1009385 33600432.

16. Davis S, Bax N, Grewe P. Engineered underdominance allows efficient and economical introgression of traits into pest populations. J Theor Biol. 2001;212(1):83–98. doi: 10.1006/jtbi.2001.2357 WOS:000170918500007. 11527447

17. Dhole S, Lloyd AL, Gould F. Tethered homing gene drives: a new design for spatially restricted population replacement and suppression. Evol Appl. 2019;12(8):1688–702. doi: 10.1111/eva.12827 WOS:000484471100014. 31462923

18. Edgington MP, Harvey-Samuel T, Alphey L. Split drive killer-rescue provides a novel threshold-dependent gene drive. Sci Reports. 2020;10(1). ARTN 20520 doi: 10.1038/s41598-020-77544-7 WOS:000596296000007. 33239631

19. Champer J, Champer SE, Kim IK, Clark AG, Messer PW. Design and analysis of CRISPR-based underdominance toxin-antidote gene drives. Evol Appl. 2020. doi: 10.1111/eva.13180 WOS:000600504300001.

20. Dhole S, Vella MR, Lloyd AL, Gould F. Invasion and migration of spatially self-limiting gene drives: A comparative analysis. Evol Appl. 2018;11(5):794–808. doi: 10.1111/eva.12583 WOS:000433572400018. 29875820

21. Sanchez CHM, Bennett JB, Wu SL, Rasic G, Akbari OS, Marshall JM. Modeling confinement and reversibility of threshold-dependent gene drive systems in spatially-explicit Aedes aegypti populations. BMC Biology. 2020;18(1). ARTN 50 doi: 10.1186/s12915-020-0759-9 WOS:000535887600001. 32398005

22. Esvelt KM, Smidler AL, Catteruccia F, Church GM. Concerning RNA-guided gene drives for the alteration of wild populations. Elife. 2014;3. doi: 10.7554/eLife.03401 WOS:000209690800001. 25035423

23. Sudweeks J, Hollingsworth B, Blondel DV, Campbell KJ, Dhole S, Eisemann JD, et al. Locally fixed alleles: a method to localize gene drive to island populations. Sci Reports. 2019;9. ARTN 15821 doi: 10.1038/s41598-019-51994-0 WOS:000493716000022. 31676762

24. Burt A. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc Roy Soc Lond B. 2003;270(1518):921–8. doi: 10.1098/rspb.2002.2319 WOS:000182969000005. 12803906

25. Kyrou K, Hammond AM, Galizi R, Kranjc N, Burt A, Beaghton AK, et al. A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat Biotechnol. 2018;36(11):1062–+. doi: 10.1038/nbt.4245 WOS:000450374000019. 30247490

26. Oberhofer G, Ivy T, Hay BA. Cleave and Rescue, a novel selfish genetic element and general strategy for gene drive. Proc Natl Acad Sci USA. 2019;116(13):6250–9. doi: 10.1073/pnas.1816928116 WOS:000462382800067. 30760597

27. Champer J, Yang E, Lee E, Liu JX, Clark AG, Messer PW. A CRISPR homing gene drive targeting a haplolethal gene removes resistance alleles and successfully spreads through a cage population. Proc Natl Acad Sci USA. 2020;117(39):24377–83. doi: 10.1073/pnas.2004373117 WOS:000576672700020. 32929034

28. Courchamp F, Berek L, Gascoigne J. Allee effects in ecology and conservation. Oxford: Oxford University Press; 2008.

29. Champer J, Lee E, Yang E, Liu C, Clark AG, Messer PW. A toxin-antidote CRISPR gene drive system for regional population modification. Nat Commun. 2020;11(1). ARTN 1082 doi: 10.1038/s41467-020-14960-3 WOS:000518590600001. 32109227

30. Nash A, Urdaneta GM, Beaghton AK, Hoermann A, Papathanos PA, Christophides GK, et al. Integral gene drives for population replacement. Biol Open. 2019;8(1). ARTN bio037762 doi: 10.1242/bio.037762 WOS:000457406100012. 30498016

31. Champer J, Kim IK, Champer SE, Clark AG, Messer PW. Performance analysis of novel toxin-antidote CRISPR gene drive systems. BMC Biol. 2020;18(1):27. Epub 2020/03/14. doi: 10.1186/s12915-020-0761-2 32164660; PubMed Central PMCID: PMC7068947.

32. Simoni A, Hammond AM, Beaghton AK, Galizi R, Taxiarchi C, Kyrou K, et al. A male-biased sex-distorter gene drive for the human malaria vector Anopheles gambiae. Nat Biotechnol. 2020;38(9):1097–. doi: 10.1038/s41587-020-0658-1 WOS:000556636100002. 32764730

33. Hicks WM, Kim M, Haber JE. Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science. 2010;329(5987):82–5. doi: 10.1126/science.1191125 WOS:000279402700037. 20595613

34. Simoni A, Siniscalchi C, Chan Y-S, Huen DS, Russell S, Windbichler N, et al. Development of synthetic selfish elements based on modular nucleases in Drosophila melanogaster. Nucl Acids Res. 2014;42(11):7461–72. doi: 10.1093/nar/gku387 WOS:000338769400062. 24803674

35. Rodgers K, McVey M. Error-prone repair of DNA double-strand breaks. J Cell Physiol. 2016;231(1):15–24. doi: 10.1002/jcp.25053 WOS:000362217800004. 26033759

36. Pollegioni P, North AR, Persampieri T, Bucci A, Minuz RL, Groneberg DA, et al. Detecting the population dynamics of an autosomal sex ratio distorter transgene in malaria vector mosquitoes. J Appl Ecol. 2020;57(10):2086–96. doi: 10.1111/1365-2664.13702 WOS:000550495400001. 33149368

37. Marshall JM, Akbari OS. Gene drive strategies for population replacement. In: Adelman ZN, editor. Genetic control of malaria and dengue. London: Academic Press; 2016. p. 169–200.

38. Adelman ZN, Basu S, Myles KM. Engineering pathogen resistance in mosquitoes. In: Adelman ZN, editor. Genetic control of malaria and dengue. London: Academic Press; 2016. p. 277–304.

39. Anopheles gambiae Genomes Consortium. Genome variation and population structure among 1142 mosquitoes of the African malaria vector species Anopheles gambiae and Anopheles coluzzii. Genome Res. 2020;30(10):1533–46. Epub 2020/09/30. doi: 10.1101/gr.262790.120 32989001; PubMed Central PMCID: PMC7605271.

40. Magori K, Gould F. Genetically engineered underdominance for manipulation of pest populations: a deterministic model. Genetics. 2006;172(4):2613–20. doi: 10.1534/genetics.105.051789 WOS:000237225800048. 16415364

41. Khamis D, El Mouden C, Kura K, Bonsall MB. Ecological effects on underdominance threshold drives for vector control. J Theor Biol. 2018;456:1–15. doi: 10.1016/j.jtbi.2018.07.024 WOS:000445321400001. 30040965

42. Marshall JM, Hay BA. Medusa: a novel gene drive system for confined suppression of insect populations. PLOS One. 2014;9(7). ARTN e102694 doi: 10.1371/journal.pone.0102694 WOS:000339614100049. 25054803

43. Del Amo VL, Bishop AL, Sanchez CHM, Bennett JB, Feng XC, Marshall JM, et al. A transcomplementing gene drive provides a flexible platform for laboratory investigation and potential field deployment. Nat Commun. 2020;11(1). ARTN 352 doi: 10.1038/s41467-019-13977-7 WOS:000514637800004. 31953404

44. DiCarlo JE, Chavez A, Dietz SL, Esvelt KM, Church GM. Safeguarding CRISPR-Cas9 gene drives in yeast. Nat Biotechnol. 2015;33(12):1250–+. doi: 10.1038/nbt.3412 WOS:000366387700016. 26571100

45. Champer J, Chung J, Lee YL, Liu C, Yang E, Wen ZX, et al. Molecular safeguarding of CRISPR gene drive experiments. Elife. 2019;8. ARTN e41439 doi: 10.7554/eLife.41439 WOS:000457468900001. 30666960

46. Li M, Yang T, Kandul NP, Bui M, Gamez S, Raban R, et al. Development of a confinable gene drive system in the human disease vector Aedes aegypti. Elife. 2020;9. ARTN e51701 doi: 10.7554/eLife.51701 WOS:000508594700001. 31960794

47. Webster SH, Vella MR, Scott MJ. Development and testing of a novel killer-rescue self-limiting gene drive system in Drosophila melanogaster. Proc Roy Soc Lond B. 2020;287(1925). ARTN 20192994 doi: 10.1098/rspb.2019.2994 WOS:000526900400001. 32292114

48. Zapletal J, Najmitabrizi N, Erraguntla M, Lawley MA, Myles KM, Adelman ZN. Making gene drive biodegradable. Phil Trans Roy Soc Lond B. 2021;376(1818). ARTN 20190804 doi: 10.1098/rstb.2019.0804 WOS:000603646400003. 33357058

49. Pombi M, Stump AD, Della Torre A, Besansky NJ. Variation in recombination rate across the X chromosome of Anopheles gambiae. Am J Trop Med Hyg. 2006;75(5):901–3. doi: 10.4269/ajtmh.2006.75.901 WOS:000242189100022. 17123984

50. Galizi R, Hammond A, Kyrou K, Taxiarchi C, Bernardini F, O’Loughlin SM, et al. A CRISPR-Cas9 sex-ratio distortion system for genetic control. Sci Reports. 2016;6. doi: 10.1038/srep31139 WOS:000380652300001. 27484623

51. Fasulo B, Meccariello A, Morgan M, Borufka C, Papathanos PA, Windbichler N. A fly model establishes distinct mechanisms for synthetic CRISPR/Cas9 sex distorters. PLOS Genet. 2020;16(3). ARTN e1008647 doi: 10.1371/journal.pgen.1008647 WOS:000524758200018. 32168334

52. Hammond A, Karlsson X, Morianou I, Kyrou K, Beaghton A, Gribble M, et al. Regulating the expression of gene drives is key to increasing their invasive potential and the mitigation of resistance. PLOS Genet. 2021;17(1):e1009321. doi: 10.1371/journal.pgen.1009321 33513149

53. Pane A, Salvemini M, Bovi PD, Polito C, Saccone G. The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development. 2002;129(15):3715–25. WOS:000177570800017. 12117820

54. Meccariello A, Salvemini M, Primo P, Hall B, Koskiniot P, Dalikova M, et al. Maleness-on-the-Y (MoY) orchestrates male sex determination in major agricultural fruit fly pests. Science. 2019;365(6460):1457–+. doi: 10.1126/science.aax1318 WOS:000488838600049. 31467189

55. Aryan A, Anderson MAE, Biedler JK, Qi YM, Overcash JM, Naumenko AN, et al. Nix alone is sufficient to convert female Aedes aegypti into fertile males and myo-sex is needed for male flight. Proc Natl Acad Sci USA. 2020;117(30):17702–9. doi: 10.1073/pnas.2001132117 WOS:000555848400016. 32661163

56. Deredec A, Godfray HCJ, Burt A. Requirements for effective malaria control with homing endonuclease genes. Proc Natl Acad Sci USA. 2011;108(43):E874–E80. doi: 10.1073/pnas.1110717108 WOS:000296378100004. 21976487

57. Hatanaka K, Okada M. Retarded nuclear migration in Drosophila embryos with aberrant F-actin reorganization caused by maternal mutations and by cytochalasin treatment. Development. 1991;111(4):909–20. WOS:A1991FK57600007. 1879360

58. O’Leary S, Adelman ZN. Disrupting female flight in the vector Aedes aegypti. Biorxiv. 2019.

59. Basrur NS, De Obaldia ME, Morita T, Herre M, von Heynitz RK, Tsitohay YN, et al. fruitless mutant male mosquitoes gain attraction to human odor. Elife. 2020;9. ARTN e63982 doi: 10.7554/eLife.63982 WOS:000610890200001. 33284111

60. Krzywinska E, Ferretti L, Li J, Li JC, Chen CH, Krzywinski J. femaleless controls sex determination and dosage compensation pathways in females of Anopheles mosquitoes. Curr Biol. 2021. Epub 2021/01/09. doi: 10.1016/j.cub.2020.12.014 33417880.

61. Oh KP, Shiels AB, Shiels L, Blondel DV, Campbell KJ, Saah JR, et al. Population genomics of invasive rodents on islands: genetic consequences of colonization and prospects for localized synthetic gene drive. Evol Appl. 2021. https://doi.org/10.1111/eva.13210.

62. Presgraves DC. Evaluating genomic signatures of "the large X-effect" during complex speciation. Mol Ecol. 2018;27(19):3822–30. doi: 10.1111/mec.14777 WOS:000446838400008. 29940087

63. Beaghton A, Hammond A, Nolan T, Crisanti A, Godfray HCJ, Burt A. Requirements for driving antipathogen effector genes into populations of disease vectors by homing. Genetics. 2017;205(4):1587–96. doi: 10.1534/genetics.116.197632 WOS:000401126600017. 28159753

64. Beaghton AK, Hammond A, Nolan T, Crisanti A, Burt A. Gene drive for population genetic control: non-functional resistance and parental effects. Proc Roy Soc Lond B. 2019;286(1914). ARTN 20191586 doi: 10.1098/rspb.2019.1586 WOS:000504858100006. 31662083

65. Met Office. Cartopy: a cartographic python library with a matplotlib interface. 2010–2015. http://scitools.org.uk/cartopy.


Článek vyšel v časopise

PLOS Genetics


2021 Číslo 3
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková, Ph.D.

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#