The joy of balancers
Autoři:
Danny E. Miller aff001; Kevin R. Cook aff003; R. Scott Hawley aff004
Působiště autorů:
Department of Medicine, Division of Medical Genetics, University of Washington, Seattle, Washington, United States of America
aff001; Department of Pediatrics, Division of Genetic Medicine, University of Washington, Seattle, Washington and Seattle Children's Hospital, Seattle, Washington, United States of America
aff002; Department of Biology, Indiana University, Bloomington, Indiana, United States of America
aff003; Stowers Institute for Medical Research, Kansas City, Missouri, United States of America
aff004; Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas, United States of America
aff005
Vyšlo v časopise:
The joy of balancers. PLoS Genet 15(11): e32767. doi:10.1371/journal.pgen.1008421
Kategorie:
Review
doi:
https://doi.org/10.1371/journal.pgen.1008421
Souhrn
Balancer chromosomes are multiply inverted and rearranged chromosomes that are widely used in Drosophila genetics. First described nearly 100 years ago, balancers are used extensively in stock maintenance and complex crosses. Recently, the complete molecular structures of several commonly used balancers were determined by whole-genome sequencing. This revealed a surprising amount of variation among balancers derived from a common progenitor, identified genes directly affected by inversion breakpoints, and cataloged mutations shared by balancers. These studies emphasized that it is important to choose the optimal balancer, because different inversions suppress meiotic recombination in different chromosomal regions. In this review, we provide a brief history of balancers in Drosophila, discuss how they are used today, and provide examples of unexpected recombination events involving balancers that can lead to stock breakdown.
Klíčová slova:
Centromeres – Deletion mutation – Drosophila melanogaster – Heterochromatin – Chromosomal inversions – Chromosome structure and function – X chromosomes – Homologous recombination
Zdroje
1. Crown NK, Miller DE, Sekelsky J, Hawley SR. Local inversion heterozygosity alters recombination throughout the genome. Curr Biol. 2018;28: 1 19. doi: 10.1016/j.cub.2017.11.007
2. Stone W, Thomas I. Crossover and disjunctional properties of X chromosome inversions in Drosophila melanogaster. Genetica. 1935;17: 170 184. doi: 10.1007/bf01984187
3. Sturtevant A, Beadle G. The relations of inversions in the X chromosome of Drosophila melanogaster to crossing over and disjunction. Genetics. 1936;21: 554 604. 17246812
4. Sturtevant A. A Case of rearrangement of genes in Drosophila. Proc National Acad Sci. 1921;7: 235–237. doi: 10.1073/pnas.7.8.235 16576597
5. Sturtevant A. A third group of linked genes in Drosophila ampelophila. Science. 1913;37: 990 992. doi: 10.1126/science.37.965.990 17833164
6. Sturtevant A. A crossover reducer in Drosophila melanogaster due to inversion of a section of the third chromosome. Biologisches Zentralblatt. 1926; 697 702. doi: 10.1111/j.1365-2818.1930.tb01489.x/abstract
7. Muller H. Genetic variability, twin hybrids and constant hybrids, in a case of balanced lethal factors. Genetics. 1918;3: 422 499. 17245914
8. Muller HJ. An Oenothera-like case in Drosophila. Proc National Acad Sci. 1917;3: 619–626. doi: 10.1073/pnas.3.10.619 16586762
9. Muller H. The measurement of gene mutation rate in Drosophila, its high variability, and its dependence upon temperature. Genetics. 1928;13: 279 357. 17246553
10. Muller H, Prokofyeva A. The individual gene in relation to the chromomere and the chromosome. Proc National Acad Sci. 1935;21: 16–26. doi: 10.1073/pnas.21.1.16 16577650
11. Lewis E, Mislove R. New mutants report. Drosophila Information Service. 1953;27: 57 58.
12. Schultz J, Redfield H. Interchromosomal effects on crossing over in Drosophila. Cold Spring Harbor symposia on quantitative biology. 1951;16: 175 197. doi: 10.1101/sqb.1951.016.01.015 14942738
13. Grell R, Lewis E. New mutants report. Drosophila Information Service. 1956;30: 71.
14. Mislove R, Lewis E. New Mutants Report. Drosophila Information Service. 1954;28: 77.
15. Merriam J. FM7: first multiple seven. Drosophila Information Service. 1968;43: 64.
16. Ward L. The genetics of curly wing in Drosophila. Another case of balanced lethal factors. Genetics. 1923;8: 276 300. 17246014
17. Mislove R, Lewis E. SM5: Second Multiple 5. Drosophila Information Service. 1955;29: 75.
18. Oster I. A new crossing-over suppressor in chromosome 2 effective in the presence of heterologous inversions. Drosophila Information Service. 1956;30: 145.
19. Craymer L. New Mutants Report. Drosophila Information Service. 1984;60: 234 236.
20. Lewis E. New Mutants Report. Drosophila Information Service. 1960;34: 51.
21. Lindsley D, Zimm G. The Genome of Drosophila melanogaster. San Diego: Academic Press; 1992.
22. Hazelrigg T, Kaufman T. Revertants of dominant mutations associated with the antennapedia gene complex of Drosophila melanogaster: Cytology and Genetics. Genetics. 1983;105: 581 600. 17246168
23. Ashburner M. New Mutants Report. Drosophila Information Service. 1972;49: 34.
24. Schaeffer SW, Goetting-Minesky PM, Kovacevic M, Peoples JR, Graybill JL, Miller JM, et al. Evolutionary genomics of inversions in Drosophila pseudoobscura: Evidence for epistasis. Proc National Acad Sci. 2003;100: 8319–8324. doi: 10.1073/pnas.1432900100 12824467
25. Edgely M. Genetic balancers. Wormbook. 2006; doi: 10.1895/wormbook.1.89.1
26. Merritt BB, Cheung LS. GRIBCG: a software for selection of sgRNAs in the design of balancer chromosomes. Bmc Bioinformatics. 2019;20: 122. doi: 10.1186/s12859-019-2712-x 30866794
27. Schwartz HT, Sternberg PW. A toolkit of engineered recombinational balancers in C. elegans. Trends Genet. 2018;34: 253–255. doi: 10.1016/j.tig.2018.01.009 29395380
28. Dejima K, Hori S, Iwata S, Suehiro Y, Yoshina S, Motohashi T, et al. An aneuploidy-free and structurally defined balancer chromosome toolkit for Caenorhabditis elegans. Cell Reports. 2018;22: 232–241. doi: 10.1016/j.celrep.2017.12.024 29298424
29. Iwata S, Yoshina S, Suehiro Y, Hori S, Mitani S. Engineering new balancer chromosomes in C. elegans via CRISPR/Cas9. Sci Rep-uk. 2016;6: 33840. doi: 10.1038/srep33840 27650892
30. Chen X, Liao S, Huang X, Xu T, Feng X, Guang S. Targeted chromosomal rearrangements via a combinatorial use of CRISPR/Cas9 and Cre/LoxP technologies in Caenorhabditis elegans. G3 Genes Genomes Genetics. 2018;8: g3.200473.2018. doi: 10.1534/g3.118.200473 29950430
31. Hentges KE, Justice MJ. Checks and balancers: balancer chromosomes to facilitate genome annotation. Trends Genet. 2004;20: 252 259. doi: 10.1016/j.tig.2004.04.004 15145578
32. Ye Z, Sun L, Li R, Han M, Zhuang Y, Wu X, et al. Generation of a mouse full-length balancer with versatile cassette-shuttling selection strategy. Int J Biol Sci. 2016;12: 911–916. doi: 10.7150/ijbs.15172 27489495
33. Miller DE, Smith CB, Kazemi N, Cockrell AJ, Arvanitakis AV, Blumenstiel JP, et al. Whole-genome analysis of individual meiotic events in Drosophila melanogaster reveals that noncrossover gene conversions are insensitive to interference and the centromere effect. Genetics. 2016;203: 159–171. doi: 10.1534/genetics.115.186486 26944917
34. Ghavi-Helm Y, Jankowski A, Meiers S, Viales RR, Korbel JO, Furlong EE. Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression. Nat Genet. 2019; 1–11. doi: 10.1038/s41588-018-0328-0
35. Miller DE, Cook KR, Arvanitakis AV, Hawley SR. Third chromosome balancer inversions disrupt protein-coding genes and influence distal recombination events in Drosophila melanogaster. G3 Genes Genomes Genetics. 2016;6: 1959 1967. doi: 10.1534/g3.116.029330 27172211
36. Miller DE, Cook KR, Hemenway EA, Fang V, Miller AL, Hales KG, et al. The molecular and genetic characterization of second chromosome balancers in Drosophila melanogaster. G3 Genes Genomes Genetics. 2018;8: g3.200021.2018. doi: 10.1534/g3.118.200021 29420191
37. Miller DE, Cook KR, Kazemi N, Smith CB, Cockrell AJ, Hawley SR, et al. Rare recombination events generate sequence diversity among balancer chromosomes in Drosophila melanogaster. Proc National Acad Sci. 2016;113: E1352–E1361. doi: 10.1073/pnas.1601232113 26903656
38. Vef O, Cleppien D, Löffler T, Altenhein B, Technau GM. A new strategy for efficient in vivo screening of mutagenized Drosophila embryos. Dev Genes Evol. 2006;216: 105–108. doi: 10.1007/s00427-005-0036-5 16328480
39. Halfon MS, Gisselbrecht S, Lu J, Estrada B, Keshishian H, Michelson AM. New fluorescent protein reporters for use with the Drosophila gal4 expression system and for vital detection of balancer chromosomes. Genesis. 2002;34: 135–138. doi: 10.1002/gene.10136 12324968
40. Casso D, Ramírez-Weber F-A, Kornberg TB. GFP-tagged balancer chromosomes for Drosophila melanogaster. Mech Develop. 2000;91: 451–454. doi: 10.1016/s0925-4773(00)00248-3
Štítky
Genetika Reprodukční medicínaČlánek vyšel v časopise
PLOS Genetics
2019 Číslo 11
Nejčtenější v tomto čísle
- The genetic architecture of helminth-specific immune responses in a wild population of Soay sheep (Ovis aries)
- A circadian output center controlling feeding:Fasting rhythms in Drosophila
- AMPK regulates ESCRT-dependent microautophagy of proteasomes concomitant with proteasome storage granule assembly during glucose starvation
- Chromatin dynamics enable transcriptional rhythms in the cnidarian Nematostella vectensis