Centromeric DNA Facilitates Nonconventional Yeast Genetic Engineering

Cao, Mingfeng; Gao, Meirong; Lopez-Garcia, Carmen Lorena; Wu, Yutong; Seetharam, Arun Somwarpet; Severin, Andrew Josef; Shao, Zengyi

doi:10.1021/acssynbio.7b00046

Cited by 58Fungal and yeast genetics researchMicrobial Metabolic Engineering and BioproductionCRISPR and Genetic Engineering

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Centromeric DNA Facilitates Nonconventional Yeast Genetic Engineering

Cao, Mingfeng, Gao, Meirong, Lopez-Garcia, Carmen Lorena, Wu, Yutong, Seetharam, Arun Somwarpet, Severin, Andrew Josef, Shao, Zengyi·2017·ACS Synthetic Biology

DOI 10.1021/acssynbio.7b00046

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Abstract

Many nonconventional yeast species have highly desirable features that are not possessed by model yeasts, despite that significant technology hurdles to effectively manipulate them lay in front. Scheffersomyces stipitis is one of the most important exemplary nonconventional yeasts in biorenewables industry, which has a high native xylose utilization capacity. Recent study suggested its much better potential than Saccharomyces cerevisiae as a well-suited microbial biomanufacturing platform for producing high-value compounds derived from shikimate pathway, many of which are associated with potent nutraceutical or pharmaceutical properties. However, the broad application of S. stipitis is hampered by the lack of stable episomal expression platforms and precise genome-editing tools. Here we report the success in pinpointing the centromeric DNA as the partitioning element to guarantee stable extra-chromosomal DNA segregation. The identified centromeric sequence not only stabilized episomal plasmid, enabled homogeneous gene expression, increased the titer of a commercially relevant compound by 3-fold, and also dramatically increased gene knockout efficiency from <1% to more than 80% with the expression of CRISPR components on the new stable plasmid. This study elucidated that establishment of a stable minichromosome-like expression platform is key to achieving functional modifications of nonconventional yeast species in order to expand the current collection of microbial factories.

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Most non-conventional yeasts lack plasmids.
“most non-conventional yeasts lack plasmids (but can be engineered to maintain foreign, extra-chromosomal DNA by designing a plasmid vector containing intrinsic autonomously replicating and centromere sequences) (Cao et al. 2017).”
From Biocontrol yeasts: mechanisms and applications (2019) · cites this paper as Cao et al. 2017

The new frontier of genome engineering with CRISPR-Cas9
Doudna, J. A., & Charpentier, E. (2014) · Science · doi:10.1126/science.1258096 · Cited by 7,062
Next-generation DNA sequencing
Shendure, J., & Ji, H. (2008) · Nature Biotechnology · doi:10.1038/nbt1486 · Cited by 4,509
BEDTools: The Swiss‐Army Tool for Genome Feature Analysis
Quinlan, A. R. (2014) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1112s47 · Cited by 2,286
Genome evolution in yeasts
Dujon, B., Sherman, D., Fischer, G., Durrens, P., Casaregola, S., Lafontaine, I., de Montigny, J., Marck, C., Neuvéglise, C., Talla, E., et al. (2004) · Nature · doi:10.1038/nature02579 · Cited by 1,623
Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems
DiCarlo, J. E., Norville, J. E., Mali, P., Rios, X., Aach, J., & Church, G. M. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt135 · Cited by 1,566
The Centromere Paradox: Stable Inheritance with Rapidly Evolving DNA
Henikoff, S., Ahmad, K., & Malik, H. S. (2001) · Science · doi:10.1126/science.1062939 · Cited by 1,394
Centromeres and Kinetochores
Cleveland, D. W., Mao, Y., & Sullivan, K. F. (2003) · Cell · doi:10.1016/s0092-8674(03)00115-6 · Cited by 1,003
Complete biosynthesis of opioids in yeast
Galanie, S. S., Thodey, K., Trenchard, I. J., Interrante, M. V. F., & Smolke, C. D. (2015) · Science · doi:10.1126/science.aac9373 · Cited by 989
Establishment and Maintenance of a Heterochromatin Domain
Hall, I. M., Shankaranarayana, G. D., Noma, K.-I., Ayoub, N., Cohen, A., & Grewal, S. I. S. (2002) · Science · doi:10.1126/science.1076466 · Cited by 895
High-resolution mapping of meiotic crossovers and non-crossovers in yeast
Mancera, E., Bourgon, R., Brozzi, A., Huber, W. K., & Steinmetz, L. M. (2008) · Nature · doi:10.1038/nature07135 · Cited by 636
Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis
Jeffries, T. W., Grigoriev, I. V., Grimwood, J., Laplaza, J. M., Aerts, A. L., Salamov, A. A., Schmutz, J., Lindquist, E., Dehal, P., Shapiro, H., et al. (2007) · Nature Biotechnology · doi:10.1038/nbt1290 · Cited by 492
Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae
Gerton, J. L., DeRisi, J. L., Shroff, R., Lichten, M., Brown, P. O., & Petes, T. D. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.21.11383 · Cited by 481
GC-Content Evolution in Mammalian Genomes: The Biased Gene Conversion Hypothesis
Galtier, N., Piganeau, G., Mouchiroud, D., & Duret, L. (2001) · Genetics · doi:10.1093/genetics/159.2.907 · Cited by 474
Mitotic stability of yeast chromosomes: A colony color assay that measures nondisjunction and chromosome loss
Hieter, P. (1985) · Cell · doi:10.1016/0092-8674(85)90152-7 · Cited by 443
Eukaryotic DNA replication origins: many choices for appropriate answers
Méchali, M. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2976 · Cited by 441
A Candida albicans CRISPR system permits genetic engineering of essential genes and gene families
Vyas, V. K., Barrasa, M. I., & Fink, G. R. (2015) · Science Advances · doi:10.1126/sciadv.1500248 · Cited by 376
Major Evolutionary Transitions in Centromere Complexity
Malik, H. S., & Henikoff, S. (2009) · Cell · doi:10.1016/j.cell.2009.08.036 · Cited by 375
De novo production of the flavonoid naringenin in engineered Saccharomyces cerevisiae
Koopman, F. W., Beekwilder, J., Crimi, B., van Houwelingen, A. M. M. L., Hall, R. D., Bosch, D., van Maris, A. J. A., Pronk, J. T., & Daran, J.-M. G. (2012) · Microbial Cell Factories · doi:10.1186/1475-2859-11-155 · Cited by 367
Clustering of meiotic double-strand breaks on yeast chromosome III
Baudat, F., & Nicolas, A. G. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5213 · Cited by 320
Centromere identity is specified by a single centromeric nucleosome in budding yeast
Furuyama, S., & Biggins, S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706985104 · Cited by 271
Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins
Meraldi, P., McAinsh, A. D., Rheinbay, E., & Sorger, P. K. (2006) · Genome biology · doi:10.1186/gb-2006-7-3-r23 · Cited by 262
Metabolic engineering of the complete pathway leading to heterologous biosynthesis of various flavonoids and stilbenoids in Saccharomyces cerevisiae
Trantas, E., Panopoulos, N. J., & Ververidis, F. (2009) · Metabolic Engineering · doi:10.1016/j.ymben.2009.07.004 · Cited by 234
Advancing secondary metabolite biosynthesis in yeast with synthetic biology tools
Siddiqui, M. S., Thodey, K., Trenchard, I. J., & Smolke, C. D. (2011) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00774.x · Cited by 226
Functional selection and analysis of yeast centromeric DNA
Hieter, P., Pridmore, D., Hegemann, J. H., Thomas, M., Davis, R. W., & Philippsen, P. (1985) · Cell · doi:10.1016/0092-8674(85)90287-9 · Cited by 226
Autonomously replicating sequences in Saccharomyces cerevisiae.
Chan, C. S. M., & Tye, B. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.11.6329 · Cited by 223
Genetic Manipulation of Centromere function
Hill, A., & Bloom, K. (1987) · Molecular and Cellular Biology · doi:10.1128/mcb.7.7.2397 · Cited by 215
Rewiring yeast sugar transporter preference through modifying a conserved protein motif
Young, E. M., Tong, A., Bui, H., Spofford, C., & Alper, H. S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311970111 · Cited by 197
Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique
Sanyal, K., Baum, M. P., & Carbon, J. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404318101 · Cited by 181
Improvement of Xylose Uptake and Ethanol Production in Recombinant Saccharomyces cerevisiae through an Inverse Metabolic Engineering Approach
Jin, Y., Alper, H. S., Yang, Y.-T., & Stephanopoulos, G. N. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8249-8256.2005 · Cited by 148
A molecular transporter engineering approach to improving xylose catabolism in Saccharomyces cerevisiae
Young, E. M., Comer, A. D., Huang, H., & Alper, H. S. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.03.004 · Cited by 138
A novel epigenetic effect can alter centromere function in fission yeast
Steiner, N. C. (1994) · Cell · doi:10.1016/0092-8674(94)90075-2 · Cited by 134
Increased homologous integration frequency in Yarrowia lipolytica strains defective in non-homologous end-joining
Kretzschmar, A., Otto, C., Holz, M., Werner, S., Hübner, L., & Barth, G. (2013) · Current Genetics · doi:10.1007/s00294-013-0389-7 · Cited by 127
Investigating strain dependency in the production of aromatic compounds in Saccharomyces cerevisiae
Suástegui, M., Guo, W., Feng, X., & Shao, Z. (2016) · Biotechnology and Bioengineering · doi:10.1002/bit.26037 · Cited by 100
Self-citation
Engineering strategies for the fermentative production of plant alkaloids in yeast
Trenchard, I. J., & Smolke, C. D. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.05.001 · Cited by 96
Rapid evolution of Cse4p-rich centromeric DNA sequences in closely related pathogenic yeasts, Candida albicans and Candida dubliniensis
Padmanabhan, S., Thakur, J., Siddharthan, R., & Sanyal, K. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809770105 · Cited by 87
High expression of XYL2 coding for xylitol dehydrogenase is necessary for efficient xylose fermentation by engineered Saccharomyces cerevisiae
Kim, S. R., Ha, S.-J., Kong, I. I., & Jin, Y. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.04.001 · Cited by 86
Centromeric Chromatin and Epigenetic Effects in Kinetochore Assembly
Wiens, G. R., & Sorger, P. K. (1998) · Cell · doi:10.1016/s0092-8674(00)81157-5 · Cited by 82
Yeast factories for the production of aromatic compounds: from building blocks to plant secondary metabolites
Suástegui, M., & Shao, Z. (2016) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-016-1824-9 · Cited by 78
Self-citation
A yeast acts in (Cis) to inhibit meiotic gene conversion of adjacent sequences
Lambie, E. J., & Roeder, G. S. (1988) · Cell · doi:10.1016/0092-8674(88)90428-x · Cited by 74
Optimization of yeast-based production of medicinal protoberberine alkaloids
Galanie, S. S., & Smolke, C. D. (2015) · Microbial Cell Factories · doi:10.1186/s12934-015-0332-3 · Cited by 73
Diversity in the organization of centromeric chromatin
Steiner, F. A., & Henikoff, S. (2015) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2015.03.010 · Cited by 68
Evolutionary Genomics and Systems Biology
Caetano‐Anollés, G. (2010) · Wiley eBooks · doi:10.1002/9780470570418 · Cited by 68
Chromosomal G + C Content Evolution in Yeasts: Systematic Interspecies Differences, and GC-Poor Troughs at Centromeres
Lynch, D. B., Logue, M. E., Butler, G., & Wolfe, K. H. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq042 · Cited by 65
High-efficiency transformation of Pichia stipitis based on its URA3 gene and a homologous autonomous replication sequence, ARS2
Yang, V. W., Marks, J. A., Davis, B. P., & Jeffries, T. W. (1994) · Applied and Environmental Microbiology · doi:10.1128/aem.60.12.4245-4254.1994 · Cited by 62
Cloning and disruption of the b-isopropylmalate dehydrogenase gene ( LEU2 ) of Pichia stipitis with URA3 and recovery of the double auxotroph
Lu, P. Z., Davis, B. P., Hendrick, J., & Jeffries, T. W. (1998) · Applied Microbiology and Biotechnology · doi:10.1007/s002530051150 · Cited by 58
Innovating a Nonconventional Yeast Platform for Producing Shikimate as the Building Block of High-Value Aromatics
Gao, M., Cao, M., Suástegui, M., Walker, J., Quiroz, N. R., Wu, Y., Tribby, D., Okerlund, A. L., Stanley, L. M., Shanks, J. V., et al. (2016) · ACS Synthetic Biology · doi:10.1021/acssynbio.6b00132 · Cited by 57
Self-citation
Feasibility of xylose fermentation by engineeredSaccharomyces cerevisiaeoverexpressing endogenous aldose reductase (GRE3), xylitol dehydrogenase (XYL2), and xylulokinase (XYL3) fromScheffersomyces stipitis
Kim, S. R., Kwee, N. R., Kim, H., & Jin, Y. (2013) · FEMS Yeast Research · doi:10.1111/1567-1364.12036 · Cited by 54
A Comprehensive Genome-Wide Map of Autonomously Replicating Sequences in a Naive Genome
Liachko, I., Bhaskar, A., Lee, C., Chung, S. C. C., Tye, B., & Keich, U. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000946 · Cited by 53
Sh ble and Cre adapted for functional genomics and metabolic engineering of Pichia stipitis
Laplaza, J. M., Torres, B. R., Jin, Y., & Jeffries, T. W. (2005) · Enzyme and Microbial Technology · doi:10.1016/j.enzmictec.2005.07.024 · Cited by 50
Discovery of an Unconventional Centromere in Budding Yeast Redefines Evolution of Point Centromeres
Kobayashi, N., Suzuki, Y., Schoenfeld, L. W., Müller, C. A., Nieduszynski, C. A., Wolfe, K. H., & Tanaka, T. U. (2015) · Current Biology · doi:10.1016/j.cub.2015.06.023 · Cited by 49
Increasing expression level and copy number of aYarrowia lipolyticaplasmid through regulated centromere function
Liu, L., Otoupal, P. B., Pan, A., & Alper, H. S. (2014) · FEMS Yeast Research · doi:10.1111/1567-1364.12201 · Cited by 44
Faithful segregation of the multicopy yeast plasmid through cohesin-mediated recognition of sisters
Ghosh, S., Hajra, S., & Jayaram, M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702996104 · Cited by 44
Only Centromeres Can Supply the Partition System Required for ARS Function in the Yeast Yarrowia lipolytica
Vernis, L., Poljak, L. G., Chasles, M., Uchida, K., Casarégola, S., Käs, E., Matsuoka, M., Gaillardin, C. M., & Fournier, P. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4300 · Cited by 43
Complete DNA Sequence of Kuraishia capsulata Illustrates Novel Genomic Features among Budding Yeasts (Saccharomycotina)
Morales, L., Noël, B., Porcel, B. M., Marcet‐Houben, M., Hullo, M.-F., Sacerdot, C., Tekaia, F., Leh, V., Despons, L., Khanna, V., et al. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt201 · Cited by 42
Construction and Engineering of Large Biochemical Pathways via DNA Assembler
Shao, Z., & Zhao, H. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-625-2_9 · Cited by 34
Self-citation
Time to Be Versatile: Regulation of the Replication Timing Program in Budding Yeast
Yoshida, K., Poveda, A., & Pasero, P. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.09.020 · Cited by 33
Manipulating Natural Product Biosynthetic Pathways via DNA Assembler
Shao, Z., & Zhao, H. (2014) · Current Protocols in Chemical Biology · doi:10.1002/9780470559277.ch130191 · Cited by 33
Self-citation
DNA Assembler
Shao, Z., & Zhao, H. (2012) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-404634-4.00010-3 · Cited by 33
Self-citation
The Partitioning and Copy Number Control Systems of the Selfish Yeast Plasmid: An Optimized Molecular Design for Stable Persistence in Host Cells
Liu, Y., Sau, S., Ma, C.-H., Kachroo, A. H., Rowley, P. A., Chang, K.-M., Fan, H., & Jayaram, M. (2014) · Microbiology Spectrum · doi:10.1128/microbiolspec.plas-0003-2013 · Cited by 30
Efficient gene targeting in a Candida guilliermondii non-homologous end-joining pathway-deficient strain
Foureau, E., Courdavault, V., Rojas, L. F., Dutilleul, C., Simkin, A. J., Crèche, J., Atehortúa, L., Giglioli‐Guivarc’h, N., Clastre, M., & Papon, N. (2013) · Biotechnology Letters · doi:10.1007/s10529-013-1169-7 · Cited by 25
Genetic Dissection of Centromere Function
Schulman, I. G., & Bloom, K. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.6.3156-3166.1993 · Cited by 16
A DNA Polymerase Mutation That Suppresses the Segregation Bias of an ARS Plasmid in Saccharomyces cerevisiae
Houtteman, S. W., & Elder, R. T. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.3.1489-1496.1993 · Cited by 5

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Authors: Cao, M., Gao, M., Lopez-Garcia, C. L., Wu, Y., Seetharam, A. S., Severin, A. J., & Shao, Z.
Affiliations: Iowa State University (US)
Corresponding author: Shao, Zengyi
ORCID: Cao, Mingfeng
Wu, Yutong
Seetharam, Arun Somwarpet
Severin, Andrew Josef
Shao, Zengyi
Venue: ACS Synthetic Biology
Publisher: American Chemical Society (ACS)
Published: 2017-04-25
Volume: 6
Issue: 8
Pages: 1545-1553
ISSN: 2161-5063 (ISSN-L)
DOI: 10.1021/acssynbio.7b00046
OpenAlex: W2607465103
Cited by: 57
References: 62
Citations by year: 2026: 3 · 2025: 7 · 2024: 3 · 2023: 4 · 2022: 3 · 2021: 10 · 2020: 11 · 2019: 5 · 2018: 8 · 2017: 3
FWCI: 3.02
Type: journal article
Language: en
Open access: closed
Locations: ACS Synthetic Biology (publishedVersion)
PubMed (publishedVersion)
Funders: Office of Experimental Program to Stimulate Competitive Research (EPS-1101284)
Division of Engineering Education and Centers (EEC-0813570)
Iowa Energy Center (4782024)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
Keywords: centromeric DNA, non-conventional yeasts, Scheffersomyces stipitis, shikimate pathway, xylose utilization
MeSH terms: Ascomycota, Centromere, DNA, Fungal Proteins, Genetic Engineering, Gene Expression Regulation, Fungal, Epigenesis, Genetic, Clustered Regularly Interspaced Short Palindromic Repeats

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Centromeric DNA Facilitates Nonconventional Yeast Genetic Engineering

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