Creation of Stable Heterothallic Strains of Komagataella phaffii Enables Dissection of Mating Gene Regulation

REFERENCES

• Strathern JN, Klar AJ, Hicks JB, Abraham JA, Ivy JM, Nasmyth KA, McGill C. 1982. Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell 31:183–192. https://doi.org/10.1016/0092-8674(82)90418-4.
   PubMed Web of Science ®Google Scholar
• Kostriken R, Strathern JN, Klar AJ, Hicks JB, Heffron F. 1983. A site-specific endonuclease essential for mating-type switching in Saccharomyces cerevisiae. Cell 35:167–174. https://doi.org/10.1016/0092-8674(83)90219-2.
   PubMed Web of Science ®Google Scholar
• Haber JE. 2012. Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics 191:33–64. https://doi.org/10.1534/genetics.111.134577.
   PubMed Web of Science ®Google Scholar
• Meiron H, Nahon E, Raveh D. 1995. Identification of the heterothallic mutation in HO-endonuclease of S. cerevisiae using HO/ho chimeric genes. Curr Genet 28:367–373. https://doi.org/10.1007/BF00326435.
   PubMed Web of Science ®Google Scholar
• Lin X, Heitman J. 2007. Mechanisms of homothallism in fungi and transitions between heterothallism and homothallism, p 35–57. In Heitman J, Kronstad JW, Taylor JW, Casselton LA (ed), Sex in fungi. American Society for Microbiology, Washingon, DC.
   Google Scholar
• Wilson AM, Wilken PM, van der Nest MA, Steenkamp ET, Wingfield MJ, Wingfield BD. 2015. Homothallism: an umbrella term for describing diverse sexual behaviours. IMA Fungus 6:207–214. https://doi.org/10.5598/imafungus.2015.06.01.13.
   PubMed Web of Science ®Google Scholar
• Hanson SJ, Wolfe KH. 2017. An evolutionary perspective on yeast mating-type switching. Genetics 206:9–32. https://doi.org/10.1534/genetics.117.202036.
   PubMed Web of Science ®Google Scholar
• Strathern J, Hicks J, Herskowitz I. 1981. Control of cell type in yeast by the mating type locus. The alpha 1-alpha 2 hypothesis. J Mol Biol 147:357–372.
   PubMed Web of Science ®Google Scholar
• Tatchell K, Nasmyth KA, Hall BD, Astell C, Smith M. 1981. In vitro mutation analysis of the mating-type locus in yeast. Cell 27:25–35. https://doi.org/10.1016/0092-8674(81)90357-3.
   PubMed Web of Science ®Google Scholar
• Dranginis AM. 1989. Regulation of STA1 gene expression by MAT during the life cycle of Saccharomyces cerevisiae. Mol Cell Biol 9:3992–3998. https://doi.org/10.1128/MCB.9.9.3992.
   PubMed Web of Science ®Google Scholar
• Tsong AE, Miller MG, Raisner RM, Johnson AD. 2003. Evolution of a combinatorial transcriptional circuit: a case study in yeasts. Cell 115:389–399. https://doi.org/10.1016/S0092-8674(03)00885-7.
   PubMed Web of Science ®Google Scholar
• Kelly M, Burke J, Smith M, Klar A, Beach D. 1988. Four mating-type genes control sexual differentiation in the fission yeast. EMBO J 7:1537–1547.
   PubMed Web of Science ®Google Scholar
• Baker CR, Booth LN, Sorrells TR, Johnson AD. 2012. Protein modularity, cooperative binding, and hybrid regulatory states underlie transcriptional network diversification. Cell 151:80–95. https://doi.org/10.1016/j.cell.2012.08.018.
   PubMed Web of Science ®Google Scholar
• Burkholder AC, Hartwell LH. 1985. The yeast alpha-factor receptor: structural properties deduced from the sequence of the STE2 gene. Nucleic Acids Res 13:8463–8475. https://doi.org/10.1093/nar/13.23.8463.
   PubMed Web of Science ®Google Scholar
• Hagen DC, McCaffrey G, Sprague GF. 1986. Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a factor: gene sequence and implications for the structure of the presumed receptor. Proc Natl Acad Sci U S A 83:1418–1422. https://doi.org/10.1073/pnas.83.5.1418.
   PubMed Web of Science ®Google Scholar
• Bender A, Sprague GF, Jr. 1986. Yeast peptide pheromones, a-factor and alpha-factor, activate a common response mechanism in their target cells. Cell 47:929–937. https://doi.org/10.1016/0092-8674(86)90808-1.
   PubMed Web of Science ®Google Scholar
• Maekawa H, Kaneko Y. 2014. Inversion of the chromosomal region between two mating type loci switches the mating type in Hansenula polymorpha. PLoS Genet 10:e1004796. https://doi.org/10.1371/journal.pgen.1004796.
   Google Scholar
• Torres-Quiroz F, Kawasaki L, Rodriguez-Gonzalez M, Patron-Soberano A, Coria R. 2007. The KlSTE2 and KlSTE3 genes encode MATalpha- and MATa-specific G-protein-coupled receptors, respectively, which are required for mating of Kluyveromyces lactis haploid cells. Yeast 24:17–25. https://doi.org/10.1002/yea.1432.
   PubMed Web of Science ®Google Scholar
• Tolstorukov I, Cregg JM. 2007. Classical genetics. Methods Mol Biol 389:189–201. https://doi.org/10.1007/978-1-59745-456-8_14.
   PubMedGoogle Scholar
• Coughlan AY, Hanson SJ, Byrne KP, Wolfe KH. 2016. Centromeres of the yeast Komagataella phaffii (Pichia pastoris) have a simple inverted-repeat structure. Genome Biol Evol 8:2482–2492. https://doi.org/10.1093/gbe/evw178.
   PubMed Web of Science ®Google Scholar
• Love KR, Shah KA, Whittaker CA, Wu J, Bartlett MC, Ma D, Leeson RL, Priest M, Borowsky J, Young SK, Love JC. 2016. Comparative genomics and transcriptomics of Pichia pastoris. BMC Genomics 17:550. https://doi.org/10.1186/s12864-016-2876-y.
   PubMed Web of Science ®Google Scholar
• Hanson SJ, Byrne KP, Wolfe KH. 2014. Mating-type switching by chromosomal inversion in methylotrophic yeasts suggests an origin for the three-locus Saccharomyces cerevisiae system. Proc Natl Acad Sci U S A 111:E4851–E4858. https://doi.org/10.1073/pnas.1416014111.
   PubMed Web of Science ®Google Scholar
• Gottschling DE, Aparicio OM, Billington BL, Zakian VA. 1990. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63:751–762. https://doi.org/10.1016/0092-8674(90)90141-Z.
   PubMed Web of Science ®Google Scholar
• Riley R, Haridas S, Wolfe KH, Lopes MR, Hittinger CT, Goker M, Salamov AA, Wisecaver JH, Long TM, Calvey CH, Aerts AL, Barry KW, Choi C, Clum A, Coughlan AY, Deshpande S, Douglass AP, Hanson SJ, Klenk HP, LaButti KM, Lapidus A, Lindquist EA, Lipzen AM, Meier-Kolthoff JP, Ohm RA, Otillar RP, Pangilinan JL, Peng Y, Rokas A, Rosa CA, Scheuner C, Sibirny AA, Slot JC, Stielow JB, Sun H, Kurtzman CP, Blackwell M, Grigoriev IV, Jeffries TW. 2016. Comparative genomics of biotechnologically important yeasts. Proc Natl Acad Sci U S A 113:9882–9887. https://doi.org/10.1073/pnas.1603941113.
   PubMed Web of Science ®Google Scholar
• Swinnen S, Thevelein JM, Nevoigt E. 2012. Genetic mapping of quantitative phenotypic traits in Saccharomyces cerevisiae. FEMS Yeast Res 12:215–227. https://doi.org/10.1111/j.1567-1364.2011.00777.x.
   PubMed Web of Science ®Google Scholar
• Weaver-Feldhaus JM, Lou J, Coleman JR, Siegel RW, Marks JD, Feldhaus MJ. 2004. Yeast mating for combinatorial Fab library generation and surface display. FEBS Lett 564:24–34. https://doi.org/10.1016/S0014-5793(04)00309-6.
   PubMed Web of Science ®Google Scholar
• Chen MT, Lin S, Shandil I, Andrews D, Stadheim TA, Choi BK. 2012. Generation of diploid Pichia pastoris strains by mating and their application for recombinant protein production. Microb Cell Fact 11:91. https://doi.org/10.1186/1475-2859-11-91.
   PubMed Web of Science ®Google Scholar
• Kurtzman C. 2005. Description of Komagataella phaffii sp. nov. and the transfer of Pichia pseudopastoris to the methylotrophic yeast genus Komagataella. Int J Syst Evol Microbiol 55:973–976. https://doi.org/10.1099/ijs.0.63491-0.
   PubMed Web of Science ®Google Scholar
• Kuberl A, Schneider J, Thallinger GG, Anderl I, Wibberg D, Hajek T, Jaenicke S, Brinkrolf K, Goesmann A, Szczepanowski R, Puhler A, Schwab H, Glieder A, Pichler H. 2011. High-quality genome sequence of Pichia pastoris CBS7435. J Biotechnol 154:312–320. https://doi.org/10.1016/j.jbiotec.2011.04.014.
   PubMed Web of Science ®Google Scholar
• Valli M, Tatto NE, Peymann A, Gruber C, Landes N, Ekker H, Thallinger GG, Mattanovich D, Gasser B, Graf AB. 2016. Curation of the genome annotation of Pichia pastoris (Komagataella phaffii) CBS7435 from gene level to protein function. FEMS Yeast Res 16:fow051. https://doi.org/10.1093/femsyr/fow051.
   PubMed Web of Science ®Google Scholar
• Hartig A, Holly J, Saari G, MacKay VL. 1986. Multiple regulation of STE2, a mating-type-specific gene of Saccharomyces cerevisiae. Mol Cell Biol 6:2106–2114. https://doi.org/10.1128/MCB.6.6.2106.
   PubMed Web of Science ®Google Scholar
• Sprague GF, Jr, Jensen R, Herskowitz I. 1983. Control of yeast cell type by the mating type locus: positive regulation of the alpha-specific STE3 gene by the MATalpha 1 product. Cell 32:409–415. https://doi.org/10.1016/0092-8674(83)90460-9.
   PubMed Web of Science ®Google Scholar
• Bender A, Sprague GF, Jr. 1989. Pheromones and pheromone receptors are the primary determinants of mating specificity in the yeast Saccharomyces cerevisiae. Genetics 121:463–476.
   PubMed Web of Science ®Google Scholar
• Reedy JL, Floyd AM, Heitman J. 2009. Mechanistic plasticity of sexual reproduction and meiosis in the Candida pathogenic species complex. Curr Biol 19:891–899. https://doi.org/10.1016/j.cub.2009.04.058.
   PubMed Web of Science ®Google Scholar
• Kitamura K, Shimoda C. 1991. The Schizosaccharomyces pombe mam2 gene encodes a putative pheromone receptor which has a significant homology with the Saccharomyces cerevisiae Ste2 protein. EMBO J 10:3743–3751.
   PubMed Web of Science ®Google Scholar
• Tanaka K, Davey J, Imai Y, Yamamoto M. 1993. Schizosaccharomyces pombe map3+ encodes the putative M-factor receptor. Mol Cell Biol 13:80–88. https://doi.org/10.1128/MCB.13.1.80.
   PubMed Web of Science ®Google Scholar
• Otsubo Y, Yamamoto M. 2012. Signaling pathways for fission yeast sexual differentiation at a glance. J Cell Sci 125:2789–2793. https://doi.org/10.1242/jcs.094771.
   PubMed Web of Science ®Google Scholar
• Goutte C, Johnson AD. 1988. a1 protein alters the DNA binding specificity of alpha 2 repressor. Cell 52:875–882. https://doi.org/10.1016/0092-8674(88)90429-1.
   PubMed Web of Science ®Google Scholar
• Fairhead C, Llorente B, Denis F, Soler M, Dujon B. 1996. New vectors for combinatorial deletions in yeast chromosomes and for gap-repair cloning using ‘split-marker’ recombination. Yeast 12:1439–1457. https://doi.org/10.1002/(SICI)1097-0061(199611)12:14<1439::AID-YEA37>3.0.CO;2-O.
   PubMed Web of Science ®Google Scholar
• Gasser B, Prielhofer R, Marx H, Maurer M, Nocon J, Steiger M, Puxbaum V, Sauer M, Mattanovich D. 2013. Pichia pastoris: protein production host and model organism for biomedical research. Future Microbiol 8:191–208. https://doi.org/10.2217/fmb.12.133.
   PubMed Web of Science ®Google Scholar
• Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S. 2011. A modular cloning system for standardized assembly of multigene constructs. PLoS One 6:e16765. https://doi.org/10.1371/journal.pone.0016765.
   PubMed Web of Science ®Google Scholar
• Sarkari P, Marx H, Blumhoff ML, Mattanovich D, Sauer M, Steiger MG. 2017. An efficient tool for metabolic pathway construction and gene integration for Aspergillus niger. Bioresour Technol 245:1327–1333. https://doi.org/10.1016/j.biortech.2017.05.004.
   PubMed Web of Science ®Google Scholar
• Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. 2013. RNA-guided human genome engineering via Cas9. Science 339:823–826. https://doi.org/10.1126/science.1232033.
   PubMed Web of Science ®Google Scholar
• Gao Y, Zhao Y. 2014. Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J Integr Plant Biol 56:343–349. https://doi.org/10.1111/jipb.12152.
   PubMed Web of Science ®Google Scholar
• Marx H, Mattanovich D, Sauer M. 2008. Overexpression of the riboflavin biosynthetic pathway in Pichia pastoris. Microb Cell Fact 7:23. https://doi.org/10.1186/1475-2859-7-23.
   PubMed Web of Science ®Google Scholar
• Stadlmayr G, Mecklenbrauker A, Rothmuller M, Maurer M, Sauer M, Mattanovich D, Gasser B. 2010. Identification and characterisation of novel Pichia pastoris promoters for heterologous protein production. J Biotechnol 150:519–529. https://doi.org/10.1016/j.jbiotec.2010.09.957.
   PubMed Web of Science ®Google Scholar
• Prielhofer R, Barrero JJ, Steuer S, Gassler T, Zahrl R, Baumann K, Sauer M, Mattanovich D, Gasser B, Marx H. 2017. GoldenPiCS: a golden gate-derived modular cloning system for applied synthetic biology in the yeast Pichia pastoris. BMC Syst Biol, in press.
   PubMed Web of Science ®Google Scholar