Inter-chromosomal insertions into wild-type chromosomes induced by SCRaMbLE
Received date: 14 Mar 2024
Accepted date: 29 Mar 2024
Copyright
Genomic rearrangements play a crucial role in shaping biological phenotypic diversity and driving species evolution. Synthetic chromosome rearrangement and modification by LoxP-mediated evolution (SCRaMbLE) has been applied to explore large-scale genomic rearrangements, yet it has been observed that these rearrangements occur exclusively in genomic regions containing loxPsym sites. Here, we found that SCRaMbLE of synthetic yeast harboring synthetic chromosome V and X can generate a variety of synthetic segment insertions into wild-type chromosomes, ranging from 1 to 300 kb. Furthermore, it was revealed that the novel insertions impacted the transcriptional level of neighboring regions and affected the production of exemplar pathway of zeaxanthin. Collectively, our results improve the understanding of the ability of SCRaMbLE to generate complex structural variations in nonsynthetic regions and provide a potential model to explore genomic transposable events.
Sijie Zhou , Junyanrui Li , Xichen Cui , Ying Wang , Ying-Jin Yuan . Inter-chromosomal insertions into wild-type chromosomes induced by SCRaMbLE[J]. Frontiers of Chemical Science and Engineering, 2024 , 18(9) : 107 . DOI: 10.1007/s11705-024-2458-5
1 |
Korbel J O , Urban A E , Affourtit J P , Godwin B , Grubert F , Simons J F , Kim P M , Palejev D , Carriero N J , Du L .
|
2 |
Alonge M , Wang X , Benoit M , Soyk S , Pereira L , Zhang L , Suresh H , Ramakrishnan S , Maumus F , Ciren D .
|
3 |
Peter J , De Chiara M , Friedrich A , Yue J X , Pflieger D , Bergström A , Sigwalt A , Barre B , Freel K , Llored A .
|
4 |
Yue J X , Li J , Aigrain L , Hallin J , Persson K , Oliver K , Bergström A , Coupland P , Warringer J , Lagomarsino M C .
|
5 |
Kreplak J , Madoui M A , Cápal P , Novák P , Labadie K , Aubert G , Bayer P E , Gali K K , Syme R A , Main D .
|
6 |
Chen H , Li C , Peng X , Zhou Z , Weinstein J N , Liang H , Caesar-Johnson S J , Demchok J A , Felau I , Kasapi M .
|
7 |
Fudenberg G , Getz G , Meyerson M , Mirny L A . High order chromatin architecture shapes the landscape of chromosomal alterations in cancer. Nature Biotechnology, 2011, 29(12): 1109–1113
|
8 |
Wu Y , Li B Z , Zhao M , Mitchell L A , Xie Z X , Lin Q H , Wang X , Xiao W H , Wang Y , Zhou X .
|
9 |
Xie Z X , Li B Z , Mitchell L A , Wu Y , Qi X , Jin Z , Jia B , Wang X , Zeng B X , Liu H M .
|
10 |
Zhou S , Wu Y , Zhao Y , Zhang Z , Jiang L , Liu L , Zhang Y , Tang J , Yuan Y J . Dynamics of synthetic yeast chromosome evolution shaped by hierarchical chromatin organization. National Science Review, 2023, 10(5): nwad073
|
11 |
Zhang H , Fu X , Gong X , Wang Y , Zhang H , Zhao Y , Shen Y . Systematic dissection of key factors governing recombination outcomes by GCE-SCRaMbLE. Nature Communications, 2022, 13(1): 5836
|
12 |
Blount B A , Lu X , Driessen M R M , Jovicevic D , Sanchez M I , Ciurkot K , Zhao Y , Lauer S , Mckiernan R M , Gowers G O F .
|
13 |
Zhou S , Wu Y , Xie Z X , Jia B , Yuan Y J . Directed genome evolution driven by structural rearrangement techniques. Chemical Society Reviews, 2021, 50(22): 12788–12807
|
14 |
Zhao Y , Coelho C , Hughes A L , Lazar-Stefanita L , Yang S , Brooks A N , Walker R S K , Zhang W , Lauer S , Hernandez C .
|
15 |
Gvozdenov Z , Barcutean Z , Struhl K . Functional analysis of a random-sequence chromosome reveals a high level and the molecular nature of transcriptional noise in yeast cells. Molecular Cell, 2023, 83(11): 1786–1797
|
16 |
Xiong Y , Zhang H , Zhou S , Ma L , Xiao W , Wu Y , Yuan Y J . Structural variations and adaptations of synthetic chromosome ends driven by SCRaMbLE in haploid and diploid yeasts. ACS Synthetic Biology, 2023, 12(3): 689–699
|
17 |
Steensels J , Gorkovskiy A , Verstrepen K J . SCRaMbLEing to understand and exploit structural variation in genomes. Nature Communications, 2018, 9(1): 1937
|
18 |
Shen Y , Gao F , Wang Y , Wang Y , Zheng J , Gong J , Zhang J , Luo Z , Schindler D , Deng Y .
|
19 |
Wang J , Xie Z X , Ma Y , Chen X R , Huang Y Q , He B , Jia B , Li B Z , Yuan Y J . Ring synthetic chromosome V SCRaMbLE. Nature Communications, 2018, 9(1): 3783
|
20 |
Wu Y , Zhu R Y , Mitchell L A , Ma L , Liu R , Zhao M , Jia B , Xu H , Li Y X , Yang Z M .
|
21 |
Zhang Y , Chiu T Y , Zhang J T , Wang S J , Wang S W , Liu L Y , Ping Z , Wang Y , Chen A , Zhang W W .
|
22 |
Jia B , Jin J , Han M , Li B , Yuan Y . Directed yeast genome evolution by controlled introduction of trans-chromosomic structural variations. Science China: Life Sciences, 2022, 65(9): 1703–1717
|
23 |
Cheng L , Zhao S , Li T , Hou S , Luo Z , Xu J , Yu W , Jiang S , Monti M , Schindler D .
|
24 |
Voigt K , Gogol-Döring A , Miskey C , Chen W , Cathomen T , Izsvák Z , Ivics Z . Retargeting sleeping beauty transposon insertions by engineered zinc finger DNA-binding domains. Molecular Therapy, 2012, 20(10): 1852–1862
|
25 |
Cao H , Hastie A R , Cao D , Lam E T , Sun Y , Huang H , Liu X , Lin L , Andrews W , Chan S .
|
26 |
Xie Z X , Mitchell L A , Liu H M , Li B Z , Liu D , Agmon N , Wu Y , Li X , Zhou X , Li B .
|
27 |
Liti G , Carter D M , Moses A M , Warringer J , Parts L , James S A , Davey R P , Roberts I N , Burt A , Koufopanou V .
|
28 |
Asker D . Isolation and characterization of a novel, highly selective astaxanthin-producing marine bacterium. Journal of Agricultural and Food Chemistry, 2017, 65(41): 9101–9109
|
29 |
Wang P , Xu H , Li H , Chen H , Zhou S , Tian F , Li B Z , Bo X , Wu Y , Yuan Y J . SCRaMbLEing of a synthetic yeast chromosome with clustered essential genes reveals synthetic lethal interactions. ACS Synthetic Biology, 2020, 9(5): 1181–1189
|
30 |
Dymond J S , Richardson S M , Coombes C E , Babatz T , Muller H , Annaluru N , Blake W J , Schwerzmann J W , Dai J , Lindstrom D L .
|
31 |
Mitchell L A , Wang A , Stracquadanio G , Kuang Z , Wang X , Yang K , Richardson S , Martin J A , Zhao Y , Walker R .
|
32 |
Carbon J . Yeast centromeres: structure and function. Cell, 1984, 37(2): 351–353
|
33 |
Xu H , Han M , Zhou S , Li B Z , Wu Y , Yuan Y J . Chromosome drives via CRISPR-Cas9 in yeast. Nature Communications, 2020, 11(1): 4344
|
34 |
Li Y X , Wu Y , Ma L , Guo Z , Xiao W H , Yuan Y J . Loss of heterozygosity by SCRaMbLEing. Science China. Life Sciences, 2019, 62(3): 381–393
|
35 |
Ko N , Nishihama R , Pringle J R . Control of 5-FOA and 5-FU resistance by Saccharomyces cerevisiae YJL055W. Yeast, 2008, 25(2): 155–160
|
36 |
Wood A J , Lo T W , Zeitler B , Pickle C S , Ralston E J , Lee A H , Amora R , Miller J C , Leung E , Meng X .
|
37 |
Gaj T , Gersbach C A , Barbas C F . ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends in Biotechnology, 2013, 31(7): 397–405
|
38 |
Fleiss A , O’donnell S , Fournier T , Lu W , Agier N , Delmas S , Schacherer J , Fischer G . Reshuffling yeast chromosomes with CRISPR/Cas9. PLOS Genetics, 2019, 15(8): e1008332
|
39 |
Sultana T , Zamborlini A , Cristofari G , Lesage P . Integration site selection by retroviruses and transposable elements in eukaryotes. Nature Reviews. Genetics, 2017, 18(5): 292–308
|
40 |
Domínguez M , Dugas E , Benchouaia M , Leduque B , Jiménez-Gómez J M , Colot V , Quadrana L . The impact of transposable elements on tomato diversity. Nature Communications, 2020, 11(1): 4058
|
41 |
Brooks A N , Hughes A L , Clauder-Münster S , Mitchell L A , Boeke J D , Steinmetz L M . Transcriptional neighborhoods regulate transcript isoform lengths and expression levels. Science, 2022, 375(6584): 1000–1005
|
42 |
Studer A , Zhao Q , Ross-Ibarra J , Doebley J . Identification of a functional transposon insertion in the maize domestication gene tb1. Nature Genetics, 2011, 43(11): 1160–1163
|
43 |
Soyk S , Lemmon Z H , Oved M , Fisher J , Liberatore K L , Park S J , Goren A , Jiang K , Ramos A , Van Der Knaap E .
|
44 |
Fueyo R , Judd J , Feschotte C , Wysocka J . Roles of transposable elements in the regulation of mammalian transcription. Nature Reviews: Molecular Cell Biology, 2022, 23(7): 481–497
|
45 |
Wang Y , Wang M , Djekidel M N , Chen H , Liu D , Alt F W , Zhang Y . eccDNAs are apoptotic products with high innate immunostimulatory activity. Nature, 2021, 599(7884): 308–314
|
46 |
Yang F , Su W , Chung O W , Tracy L , Wang L , Ramsden D A , Zhang Z Z Z . Retrotransposons hijack alt-EJ for DNA replication and eccDNA biogenesis. Nature, 2023, 620(7972): 218–225
|
47 |
Guo F , Gopaul D N , Van Duyne G D . Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature, 1997, 389(6646): 40–46
|
48 |
Biedler J L , Spengler B A . Metaphase chromosome anomaly: association with drug resistance and cell-specific products. Science, 1976, 191(4223): 185–187
|
49 |
Rosswog C , Bartenhagen C , Welte A , Kahlert Y , Hemstedt N , Lorenz W , Cartolano M , Ackermann S , Perner S , Vogel W .
|
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