Genome editing in the mushroom-forming basidiomycete Coprinopsis cinerea, optimized by a high-throughput transformation system

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Sugano, Shigeo S ^a   Suzuki, Hiroko ^a   Shimokita, Eisuke ^a,b   Chiba, Hirofumi ^a   Noji, Sumihare ^a   Osakabe, Yuriko ^a   Osakabe, Keishi ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b Forestry and Fisheries Technology Support Center   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

AGARICALES; CRISPR CAS SYSTEM; FUNGAL GENOME; GENE EDITING; GENE EXPRESSION; GENETIC RECOMBINATION; GENETIC TRANSFORMATION; GENETICS; PROCEDURES; PROMOTER REGION; PROTOPLAST; REPORTER GENE; STAINING;

AGARICALES; CRISPR-CAS SYSTEMS; GENE EDITING; GENE EXPRESSION; GENES, REPORTER; GENOME, FUNGAL; GREEN FLUORESCENT PROTEINS; PROMOTER REGIONS, GENETIC; PROTOPLASTS; RECOMBINATION, GENETIC; STAINING AND LABELING; TRANSFORMATION, GENETIC;

EID: 85018942459     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-00883-5     Document Type: Article

References (34)

1. Burns, C. et al. Analysis of the Basidiomycete Coprinopsis cinerea reveals conservation of the core meiotic expression program over half a billion years of evolution. PLoS Genet 6, e1001135, doi: 10.1371/journal.pgen.1001135 (2010).
2. Stajich, J. E. et al. Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc Natl Acad Sci USA 107, 11889-11894, doi: 10.1073/pnas.1003391107 (2010).
3. Murata, Y., Fujii, M., Zolan, M. E. & Kamada, T. Molecular analysis of pcc1, a gene that leads to A-regulated sexual morphogenesis in Coprinus cinereus. Genetics 149, 1753-1761 (1998).
4. Cheng, C. K. et al. 5′-Serial Analysis of Gene Expression studies reveal a transcriptomic switch during fruiting body development in Coprinopsis cinerea. BMC Genomics 14, 195, doi: 10.1186/1471-2164-14-195 (2013).
5. Muraguchi, H. et al. Strand-Specific RNA-Seq Analyses of Fruiting Body Development in Coprinopsis cinerea. Plos One 10, doi:ARTN e014158610.1371/journal.pone. 0141586 (2015).
6. Nakazawa, T., Ando, Y., Kitaaki, K., Nakahori, K. & Kamada, T. Efficient gene targeting in ΔCc.ku70 or ΔCc.lig4 mutants of the agaricomycete Coprinopsis cinerea. Fungal Genetics and Biology 48, 939-946, doi: 10.1016/j.fgb.2011.06.003 (2011).
7. Collins, C. M., Heneghan, M. N., Kilaru, S., Bailey, A. M. & Foster, G. D. Improvement of the Coprinopsis cinerea molecular toolkit using new construct design and additional marker genes. Journal of Microbiological Methods 82, 156-162, doi: 10.1016/j.mimet.2010.05.007 (2010).
8. Binninger, D. M., Skrzynia, C., Pukkila, P. J. & Casselton, L. A. DNA-mediated transformation of the basidiomycete Coprinus cinereus. EMBO J 6, 835-840 (1987).
9. Lastra, C. C. L., Hajek, A. E. & Humber, R. A. Effects of two cryopreservation techniques on viability and pathogenicity of entomophthoralean fungi. Can J Bot 79, 861-864 (2001).
10. Specht, C. A., Munozrivas, A., Novotny, C. P. & Ullrich, R. C. Transformation of Schizophyllum-Commune - an Analysis of Parameters for Improving Transformation Frequencies. Exp Mycol 12, 357-366, doi: 10.1016/0147-5975(88)90027-8 (1988).
11. Dörnte, B. & Kües, U. Reliability in Transformation of the Basidiomycete Coprinopsis cinerea. Current Trends in Biotechnology and Pharmacy 6, 340-355, doi: 10.1007/s00253-016-7693-3 (2012).
12. Osakabe, Y. & Osakabe, K. Genome Editing with Engineered Nucleases in Plants. Plant Cell Physiol 56, 389-400, doi: 10.1093/pcp/pcu170 (2015).
13. Doudna, J. A. & Charpentier, E. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346, 1258096-1258096, doi: 10.1126/science.12580966 (2014).
14. Matsu-ura, T., Baek, M., Kwon, J. & Hong, C. Efficient gene editing in Neurospora crassa with CRISPR technology. Fungal Biology and Biotechnology 2, doi: 10.1186/s40694-015-0015-1 (2015).
15. Vyas, V. K., Barrasa, M. I. & Fink, G. R. A CRISPR system permits genetic engineering of essential genes and gene families. Sci Adv 1, e1500248-e1500248, doi: 10.1126/sciadv.1500248 (2015).
16. Arazoe, T. et al. Tailor-made CRISPR/Cas system for highly efficient targeted gene replacement in the rice blast fungus. Biotechnol Bioeng 112, 2543-2549, doi: 10.1002/bit.25662 (2015).
17. Liu, R., Chen, L., Jiang, Y., Zhou, Z. & Zou, G. Efficient genome editing in filamentous fungus Trichoderma reesei using the CRISPR/Cas9 system. Cell. Discovery 1, 15007, doi: 10.1038/celldisc.2015.7 (2015).
18. Fuller, K. K., Chen, S., Loros, J. J. & Dunlap, J. C. Development of the CRISPR/Cas9 System for Targeted Gene Disruption in Aspergillus fumigatus. Eukaryotic Cell 14, 1073-1080, doi: 10.1128/ec.00107-15 (2015).
19. Schuster, M., Schweizer, G., Reissmann, S. & Kahmann, R. Genome editing in Ustilago maydis using the CRISPR-Cas system. Fungal Genetics and Biology 89, 3-9, doi: 10.1016/j.fgb.2015.09.001 (2015).
20. Castanera, R., Lopez-Varas, L., Pisabarro, A. G. & Ramirez, L. Validation of Reference Genes for Transcriptional Analyses in Pleurotus ostreatus by Using Reverse Transcription-Quantitative PCR. Appl Environ Microb 81, 4120-4129, doi: 10.1128/Aem.00402-15 (2015).
21. Kim, S., Ha, B. S. & Ro, H. S. Current Technologies and Related Issues for Mushroom Transformation. Mycobiology 43, 1-8, doi: 10.5941/MYCO.2015.43.1.1 (2015).
22. Hall, M. P. et al. Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate. Acs Chem Biol 7, 1848-1857, doi: 10.1021/cb3002478 (2012).
23. Burns, C. et al. Efficient GFP expression in the mushrooms Agaricus bisporus and Coprinus cinereus requires introns. Fungal Genetics and Biology 42, 191-199, doi: 10.1016/j.fgb.2004.11.005 (2005).
24. Auer, T. O., Duroure, K., De Cian, A., Concordet, J. P. & Del Bene, F. Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair. Genome Res 24, 142-153, doi: 10.1101/gr.161638.113 (2014).
25. Yu, L., Mishra, D. S. & Rigsbee, D. R. Determination of the glass properties of D-mannitol using sorbitol as an impurity. J Pharm Sci 87, 774-777, doi: 10.1021/js970224o (1998).
26. Scholtmeijer, K., Wosten, H. A. B., Springer, J. & Wessels, J. G. H. Effect of introns and AT-rich sequences on expression of the bacterial hygromycin B resistance gene in the basidiomycete Schizophyllum commune. Appl Environ Microb 67, 481-483, doi: 10.1128/AEM.67.1.481-483.2001 (2001).
27. Kamada, T. Molecular genetics of sexual development in the mushroom Coprinus cinereus. Bioessays 24, 449-459, doi: 10.1002/bies.10083 (2002).
28. Ohm, R. A., de Jong, J. F., de Bekker, C., Wosten, H. A. B. & Lugones, L. G. Transcription factor genes of Schizophyllum commune involved in regulation of mushroom formation. Mol Microbiol 81, 1433-1445, doi: 10.1111/j.1365-2958.2011.07776.x (2011).
29. Ishizaki, T., Kanno, T., Kajiwara, S. & Shishido, K. Increased heavy metal sensitivity of Escherichia coli producing the expression product of priA gene derived from the basidiomycete Lentinus edodes. Fems Microbiol Lett 171, 141-146, doi: 10.1111/j.1574-6968.1999.tb13424.x (1999).
30. Yamazaki, T., Hasebe, T., Kajiwara, S. & Shishido, K. Structure and function of a pyrimidine/purine-biased sequence from the 5 '-flanking region of the basidiomycete Lentinus edodes gene priA. Mol Gen Genet 263, 262-270, doi: 10.1007/s004380051167 (2000).
31. Rao, P. S. & Niederpruem, D. J. Carbohydrate metabolism during morphogenesis of Coprinus lagopus (sensu Buller). Journal of Bacteriology 100, 1222-1228 (1969).
32. Wälti, M. A. et al. Targeted gene silencing in the model mushroom Coprinopsis cinerea (Coprinus cinereus) by expression of homologous hairpin RNAs. Eukaryotic Cell 5, 732-744, doi: 10.1128/EC.5.4.732-744.2006 (2006).
33. Cummings, W. J., Celerin, M., Crodian, J., Brunick, L. K. & Zolan, M. E. Insertional mutagenesis in Coprinus cinereus: use of a dominant selectable marker to generate tagged, sporulation-defective mutants. Current Genetics 36, 371-382, doi: 10.1007/s002940050512 (1999).
34. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675, doi: 10.1038/nmeth.2089 (2012).