Interplay of Chimeric Mating-Type Loci Impairs Fertility Rescue and Accounts for Intra-Strain Variability in Zygosaccharomyces rouxii Interspecies Hybrid ATCC42981

. 2019 ; 10 () : 137. [epub] 20190301

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30881382

The pre-whole genome duplication (WGD) Zygosaccharomyces clade comprises several allodiploid strain/species with industrially interesting traits. The salt-tolerant yeast ATCC42981 is a sterile and allodiploid strain which contains two subgenomes, one of them resembling the haploid parental species Z. rouxii. Recently, different mating-type-like (MTL) loci repertoires were reported for ATCC42981 and the Japanese strain JCM22060, which are considered two stocks of the same strain. MTL reconstruction by direct sequencing approach is challenging due to gene redundancy, structure complexities, and allodiploid nature of ATCC42981. Here, DBG2OLC and MaSuRCA hybrid de novo assemblies of ONT and Illumina reads were combined with in vitro long PCR to definitively solve these incongruences. ATCC42981 exhibits several chimeric MTL loci resulting from reciprocal translocation between parental haplotypes and retains two MATa/MATα expression loci, in contrast to MATα in JCM22060. Consistently to these reconstructions, JCM22060, but not ATCC42981, undergoes mating and meiosis. To ascertain whether the damage of one allele at the MAT locus regains the complete sexual cycle in ATCC42981, we removed the MATα expressed locus by gene deletion. The resulting MATa/- hemizygous mutants did not show any evidence of sporulation, as well as of self- and out-crossing fertility, probably because incomplete silencing at the chimeric HMLα cassette masks the loss of heterozygosity at the MAT locus. We also found that MATα deletion switched off a2 transcription, an activator of a-specific genes in pre-WGD species. These findings suggest that regulatory scheme of cell identity needs to be further investigated in Z. rouxii protoploid yeast.

Zobrazit více v PubMed

Albertin W., Marullo P. (2012). Polyploidy in fungi: evolution after whole-genome duplication. PubMed DOI PMC

Baker C. R., Booth L. N., Sorrells T. R., Johnson A. D. (2012). Protein modularity, cooperative binding, and hybrid regulatory states underlie transcriptional network diversification. PubMed DOI PMC

Baker C. R., Tuch B. B., Johnson A. D. (2011). Extensive DNA-binding specificity divergence of a conserved transcription regulator. PubMed DOI PMC

Bizzarri M., Cassanelli S., Pryszcz L. P., Gawor J., Gromadka R., Solieri L. (2018). Draft genome sequences of the highly halotolerant strain PubMed DOI PMC

Bizzarri M., Cassanelli S., Solieri L. (2017). Mating-type switching in CBS 732T derived subcultures unveils potential genetic and phenotypic novelties in haploid PubMed DOI

Bizzarri M., Giudici P., Cassanelli S., Solieri L. (2016). Chimeric sex-determining chromosomal regions and dysregulation of cell-type identity in a sterile PubMed DOI PMC

Boisnard S., Li Y. Z., Arnaise S., Sequeira G., Raffoux X., Enache-Angoulvant A., et al. (2015). Efficient mating-type switching in PubMed DOI PMC

Bond U., Neal C., Donnelly D., James T. C. (2004). Aneuploidy and copy number breakpoints in the genome of lager yeasts mapped by microarray hybridisation. PubMed DOI

Booth L. N., Tuch B. B., Johnson A. D. (2010). Intercalation of a new tier of transcription regulation into an ancient circuit. PubMed DOI PMC

Boynton P. J., Janzen T., Greig D. (2018). Modeling the contributions of chromosome segregation errors and aneuploidy to PubMed DOI

Braun-Galleani S., Ortiz-Merino R. A., Wu Q., Xu Y., Wolfe K. H. (2018). PubMed DOI PMC

Campbell M. A., Ganley A. R., Gabaldon T., Cox M. P. (2016). The case of the missing ancient fungal polyploids. PubMed DOI

Chien C. T., Buck S., Sternglanz R., Shore D. (1993). Targeting of SIR1 protein establishes transcriptional silencing at HM loci and telomeres in yeast. PubMed DOI

Del Angel D. V., Hjerde E., Sterck L., Capella-Gutierrez S., Notredame C., Pettersson O. V., et al. (2018). Ten steps to get started in genome assembly and annotation. PubMed DOI PMC

Dujon B. A., Louis E. J. (2017). Genome diversity and evolution in the budding yeasts (Saccharomycotina). PubMed DOI PMC

Ellahi A., Rine J. (2016). Evolution and functional trajectory of Sir1 in gene silencing. PubMed DOI PMC

Fabre E., Muller H., Therizols P., Lafontaine I., Dujon B., Fairhead C. (2005). Comparative genomics in hemiascomycete yeasts: evolution of sex, silencing, and subtelomeres. PubMed DOI

Gabaldón T., Martin T., Marcet-Houben M., Durrens P., Bolotin-Fukuhara M., Lespinet O., et al. (2013). Comparative genomics of emerging pathogens in the PubMed DOI PMC

Gallagher J. E. G., Babiarz J. E., Teytelman L., Wolfe K. H., Rine J. (2009). Elaboration, diversification and regulation of the Sir1 family of silencing proteins in PubMed DOI PMC

Gordon J. L., Armisén D., Proux-Wéra E., ÓhÉigeartaigh S. S., Byrne K. P., Wolfe K. H. (2011). Evolutionary erosion of yeast sex chromosomes by mating-type switching accidents. PubMed DOI PMC

Gordon J. L., Wolfe K. H. (2008). Recent allopolyploid origin of PubMed DOI

Greig D., Borts R. H., Louis E. J., Travisano M. (2002). Epistasis and hybrid sterility in PubMed DOI PMC

Güldener U., Heck S., Fiedler T., Beinhauer J., Hegemann J. H. (1996). A new efficient gene disruption cassette for repeated use in budding yeast. PubMed DOI PMC

Haber J. E. (2012). Mating-type genes and PubMed DOI PMC

Hewitt S. K., Donaldson I. J., Lovell S. C., Delneri D. (2014). Sequencing and characterisation of rearrangements in three PubMed DOI PMC

Hickman M. A., Froyd C. A., Rusche L. N. (2011). Reinventing heterochromatin in budding yeasts: Sir2 and the origin recognition complex take center stage. PubMed DOI PMC

Hoffman C. S., Winston F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of PubMed DOI

Istace B., Friedrich A., d’Agata L., Faye S., Payen E., Beluche O., et al. (2017). De novo assembly and population genomic survey of natural yeast isolates with the oxford nanopore MinION sequencer. PubMed DOI PMC

Jain M., Koren S., Miga K. H., Quick J., Rand A. C., Sasani T. A. (2018). Nanopore sequencing and assembly of a human genome with ultra-long reads. PubMed DOI PMC

Jain M., Olsen H. E., Paten B., Akeson M. (2016). The oxford nanopore MinION: delivery of nanopore sequencing to the genomics community. PubMed DOI PMC

James S. A., Stratford M. (2011). “

Jansen H. J., Liem M., Jong-Raadsen S. A., Dufour S., Weltzien F. A., Swinkels W., et al. (2017). Rapid de novo assembly of the European eel genome from nanopore sequencing reads. PubMed DOI PMC

Karanyicz E., Antunovics Z., Kallai Z., Sipiczki M. (2017). Non-introgressive genome chimerisation by malsegregation in autodiploidised allotetraploids during meiosis of PubMed DOI

Lee H., Chou J., Cheong L., Chang N. H., Yang S. Y., Leu J. Y. (2008). Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. PubMed DOI

Liti G., Barton D. B. H., Louis E. J. (2006). Sequence diversity, reproductive isolation and species concepts in PubMed DOI PMC

Lõoke M., Kristjuhan K., Kristjuhan A. (2011). Extraction of genomic dna from yeasts for pcr-based applications. PubMed DOI PMC

Marcet-Houben M., Gabaldón T. (2015). Beyond the whole-genome duplication: phylogenetic evidence for an ancient interspecies hybridization in the baker’s yeast lineage. PubMed DOI PMC

Monerawela C., Bond U. (2017). Recombination sites on hybrid chromosomes in PubMed DOI

Mori H., Onishi H. (1967). Diploid hybridization in a heterothallic haploid yeast, PubMed PMC

Muller H., Hennequin C., Gallaud J., Dujon B., Fairhead C. (2008). The asexual yeast PubMed DOI PMC

Ner S. S., Smith M. (1989). Role of intron splicing in the function of the MATa1 gene of PubMed DOI PMC

Ohno S. (1970). DOI

Ortiz-Merino R. A., Kuanyshev N., Braun-Galleani S., Byrne K. P., Porro D., Branduardi P. (2017). Evolutionary restoration of fertility in an interspecies hybrid yeast, by whole-genome duplication after a failed mating-type switch. PubMed DOI PMC

Pfliegler P. W., Antunovics Z., Sipiczki M. (2012). Double sterility barrier between Saccharomyces species and its breakdown in allopolyploid hybrids by chromosome loss. PubMed DOI

Pribylova L., Sychrova H. (2003). Efficient transformation of the osmotolerant yeast PubMed DOI

Priyam A., Woodcroft B. J., Rai V., Munagala A., Moghul I., Ter F., et al. (2015). Sequenceserver: a modern graphical user interface for custom BLAST databases. PubMed DOI PMC

Proux-Wéra E., Armisén D., Byrne K. P., Wolfe K. H. (2012). A pipeline for automated annotation of yeast genome sequences by a conserved-synteny approach. PubMed DOI PMC

Pryszcz L., Gabaldón T. (2016). Redundans: an assembly pipeline for highly heterozygous genomes. PubMed DOI PMC

Rajeh A., Lv J., Lin Z. (2018). Heterogeneous rates of genome rearrangement contributed to the disparity of species richness in Ascomycota. PubMed DOI PMC

Roberts C., Van der Walt J. P. (1959). The life cycle of PubMed

Sambrook J., Maniatis T., Fritsch E. (1989).

Sato A., Matsushima K., Oshima K., Hattori M., Koyama Y. (2017). Draft genome sequencing of the highly halotolerant and allopolyploid yeast PubMed DOI PMC

Sievers F., Higgins D. G. (2014). “Clustal omega, accurate alignment of very large numbers of sequences,” in PubMed DOI

Simão F. A., Waterhouse R. M., Ioannidis P., Kriventseva E. V., Zdobnov E. M. (2015). BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. PubMed DOI

Sipiczki M. (2008). Interspecies hybridization and recombination in PubMed DOI

Slater G. S. C., Birney E. (2005). Automated generation of heuristics for biological sequence comparison. PubMed DOI PMC

Solieri L., Cassanelli S., Croce M. A., Giudici P. (2008). Genome size and ploidy level: new insights for elucidating relationships in PubMed DOI

Solieri L., Dakal T. C., Giudici P., Cassanelli S. (2014). Sex-determination system in the diploid yeast PubMed DOI PMC

Solieri L., Vezzani V., Cassanelli S., Dakal T. C., Pazzini J., Giudici P. (2016). Differential hypersaline stress response in PubMed DOI

Souciet J. L., Dujon B., Gaillardin C. (2009). Comparative genomics of protoploid PubMed DOI PMC

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. PubMed DOI PMC

Treangen T. J., Salzberg S. L. (2012). Repetitive DNA and next-generation sequencing: computational challenges and solutions. PubMed DOI PMC

Tsong A. E., Miller M. G., Raisner R. M., Johnson A. D. (2003). Evolution of a combinatorial transcriptional circuit: a case study in yeasts. PubMed DOI

Tsong A. E., Tuch B. B., Li H., Johnson A. D. (2006). Evolution of alternative transcriptional circuits with identical logic. PubMed DOI

Vaser R., Sovic′ I., Nagarajan N., Šikic′ M. (2017). Fast and accurate de novo genome assembly from long uncorrected reads. PubMed DOI PMC

Walker B. J., Abeel T., Shea T., Priest M., Abouelliel A., Sakthikumar S., et al. (2014). Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PubMed DOI PMC

Wang Z., Ye S., Li J., Zheng B., Bao M., Ning G. (2011). Fusion primer and nested integrated PCR (FPNI-PCR): a new high-efficiency strategy for rapid chromosome walking or flanking sequence cloning. PubMed DOI PMC

Watanabe J., Uehara K., Mogi Y. (2013). Diversity of mating-type chromosome structures in the yeast PubMed DOI PMC

Watanabe J., Uehara K., Mogi Y., Tsukioka Y. (2017). Mechanism for restoration of fertility in hybrid PubMed DOI PMC

Waterhouse A. M., Procter J. B., Martin D. M., Clamp M., Barton G. J. (2009). Jalview version 2–a multiple sequence alignment editor and analysis workbench. PubMed DOI PMC

Wolfe K. H. (2015). Origin of the yeast whole-genome duplication. PubMed DOI PMC

Wolfe K. H., Armisen D., Proux-Wera E., OhEigeartaigh S. S., Azam H., Gordon J. L., et al. (2015). Clade- and species-specific features of genome evolution in the PubMed DOI PMC

Ye C., Hill C. M., Wu S., Ruan J., Ma Z. S. (2016). DBG2OLC: efficient assembly of large genomes using long erroneous reads of the third generation sequencing technologies. PubMed DOI PMC

Yue J. X., Li J., Aigrain L., Hallin J., Persson K., Oliver K., et al. (2017). Contrasting evolutionary genome dynamics between domesticated and wild yeasts. PubMed DOI PMC

Zill O. A., Scannell D., Teytelman L., Rine J. (2010). Co-evolution of transcriptional silencing proteins and the DNA elements specifying their assembly. PubMed DOI PMC

Zill O. A., Scannell D. R., Kuei J., Sadhu M., Rine J. (2012). Evolutionary analysis of heterochromatin protein compatibility by interspecies complementation in PubMed DOI PMC

Zimin A. V., Puiu D., Luo M. C., Zhu T., Koren S., Marcais G., et al. (2017). Hybrid assembly of the large and highly repetitive genome of PubMed DOI PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...