Inter-chromosomal insertions into wild-type chromosomes induced by SCRaMbLE
Sijie Zhou, Junyanrui Li, Xichen Cui, Ying Wang, Ying-Jin Yuan
Inter-chromosomal insertions into wild-type chromosomes induced by SCRaMbLE
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.
genomic rearrangements / synthetic yeast genome / SCRaMbLE / inter-chromosomal insertions / synthetic biology
[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 .
CrossRef
Google scholar
|
[2] |
Alonge M , Wang X , Benoit M , Soyk S , Pereira L , Zhang L , Suresh H , Ramakrishnan S , Maumus F , Ciren D .
CrossRef
Google scholar
|
[3] |
Peter J , De Chiara M , Friedrich A , Yue J X , Pflieger D , Bergström A , Sigwalt A , Barre B , Freel K , Llored A .
CrossRef
Google scholar
|
[4] |
Yue J X , Li J , Aigrain L , Hallin J , Persson K , Oliver K , Bergström A , Coupland P , Warringer J , Lagomarsino M C .
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[17] |
Steensels J , Gorkovskiy A , Verstrepen K J . SCRaMbLEing to understand and exploit structural variation in genomes. Nature Communications, 2018, 9(1): 1937
CrossRef
Google scholar
|
[18] |
Shen Y , Gao F , Wang Y , Wang Y , Zheng J , Gong J , Zhang J , Luo Z , Schindler D , Deng Y .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[23] |
Cheng L , Zhao S , Li T , Hou S , Luo Z , Xu J , Yu W , Jiang S , Monti M , Schindler D .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[25] |
Cao H , Hastie A R , Cao D , Lam E T , Sun Y , Huang H , Liu X , Lin L , Andrews W , Chan S .
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[31] |
Mitchell L A , Wang A , Stracquadanio G , Kuang Z , Wang X , Yang K , Richardson S , Martin J A , Zhao Y , Walker R .
CrossRef
Google scholar
|
[32] |
Carbon J . Yeast centromeres: structure and function. Cell, 1984, 37(2): 351–353
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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 .
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[48] |
Biedler J L , Spengler B A . Metaphase chromosome anomaly: association with drug resistance and cell-specific products. Science, 1976, 191(4223): 185–187
CrossRef
Google scholar
|
[49] |
Rosswog C , Bartenhagen C , Welte A , Kahlert Y , Hemstedt N , Lorenz W , Cartolano M , Ackermann S , Perner S , Vogel W .
CrossRef
Google scholar
|
/
〈 | 〉 |