Mating of yeast explained

The mating of yeast, also known as yeast sexual reproduction, is a fundamental biological process that promotes genetic diversity and adaptation in yeast species. Yeasts such as Saccharomyces cerevisiae (baker's yeast) are single-celled eukaryotes that can exist as either haploid cells, which contain a single set of chromosomes, or diploid cells, which contain two sets of chromosomes. Haploid yeast cells come in two mating types, a and 'α', each producing specific pheromones to identify and interact with the opposite type, thus displaying simple sexual differentiation.[1] This mating type is determined by a specific genetic locus known as MAT, which governs the mating behaviour of the cells. Haploid yeast can switch mating types through a form of genetic recombination, allowing them to change mating type as often as every cell cycle. When two haploid cells of opposite mating types encounter each other, they undergo a complex signaling process that leads to cell fusion and the formation of a diploid cell. Diploid cells can then reproduce asexually or, under nutrient-limiting conditions, undergo meiosis to produce new haploid spores.

The differences between 'a' and 'α' cells, driven by specific gene expression patterns regulated by the MAT locus, are crucial for the mating process. Additionally, the decision to mate involves a highly sensitive and complex signaling pathway that includes pheromone detection and response mechanisms. In nature, yeast mating often occurs between closely related cells, although mating type switching and pheromone signaling allow for occasional outcrossing, enhancing genetic variation. Furthermore, certain yeast species, like Schizosaccharomyces pombe and Cryptococcus neoformans, have unique mating behaviours and regulatory mechanisms, demonstrating the diversity and adaptability of yeast reproductive strategies.

Mating types

Yeasts can stably exist as either a diploid or a haploid. Both haploid and diploid yeast cells reproduce by mitosis, with daughter cells budding from mother cells. Haploid cells are capable of mating with other haploid cells of the opposite mating type (an a cell can only mate with an α cell, and vice versa) to produce a stable diploid cell. Diploid cells, usually upon facing stressful conditions such as nutrient depletion, can undergo meiosis to produce four haploid spores: two a spores and two α spores.[2] [3]

Differences between a and α cells

a cells produce a-factor', a mating pheromone which signals the presence of an a cell to neighbouring α cells.[4] a cells respond to α-factor, the α cell mating pheromone, by growing a projection (known as a shmoo, due to its distinctive shape resembling the Al Capp cartoon character Shmoo) towards the source of α-factor.[5] Similarly, α cells produce α-factor, and respond to a-factor by growing a projection towards the source of the pheromone.[6] The response of haploid cells only to the mating pheromones of the opposite mating type allows mating between a and α cells, but not between cells of the same mating type.[7]

These phenotypic differences between a and α cells are due to a different set of genes being actively transcribed and repressed in cells of the two mating types. a cells activate genes which produce a-factor and produce a cell surface receptor (Ste2) which binds to α-factor and triggers signaling within the cell.[8] [9] a cells also repress the genes associated with being an α cell. Similarly, α cells activate genes which produce α-factor and produce a cell surface receptor (Ste3) which binds and responds to a-factor, and α cells repress the genes associated with being an a cell.[10]

The MAT locus

The different sets of transcriptional repression and activation which characterize a and α cells are caused by the presence of one of two alleles of a mating-type locus called MAT: MATa or MATα located on chromosome III.[11] The MAT locus is usually divided into five regions (W, X, Y, Z1, and Z2) based on the sequences shared among the two mating types.[12] The difference lies in the Y region (Ya and Yα), which contains most of the genes and promoters.

The MATa allele of MAT encodes a gene called a1, which in haploids direct the transcription of the a-specific transcriptional program (such as expressing STE2 and repressing STE3) that defines an a cell. The MATα allele of MAT encodes the α1 and α2 genes, which in haploids direct the transcription of the α-specific transcriptional program (such as expressing STE3, repressing STE2, producing prepro-α-factor) which causes the cell to be an α cell. S. cerevisiae has an a2 gene with no apparent function that shares much of its sequence with α2; however, other yeasts like Candida albicans do have a functional and distinct MATa2 gene.

Differences between haploid and diploid cells

Haploid cells are one of two mating types (a or α), and respond to the mating pheromone produced by haploid cells of the opposite mating type, and can mate with cells of the opposite mating type. Haploid cells cannot undergo meiosis.[13] Diploid cells do not produce or respond to either mating pheromone and do not mate, but can undergo meiosis to produce four haploid cells.[14]

Like the differences between haploid a and α cells, different patterns of gene repression and activation are responsible for the phenotypic differences between haploid and diploid cells.[15] In addition to the specific a and α transcriptional patterns, haploid cells of both mating types share a haploid transcriptional pattern which activates haploid-specific genes (such as HO) and represses diploid-specific genes (such as IME1).[16] Similarly, diploid cells activate diploid-specific genes and repress haploid-specific genes.[17]

The different gene expression patterns of haploids and diploids are again due to the MAT locus. Haploid cells only contain one copy of each of the 16 chromosomes and thus can only possess one allele of MAT (either MATa or MATα), which determines their mating type.[18] Diploid cells result from the mating of an a cell and an α cell, and thus possess 32 chromosomes (in 16 pairs), including one chromosome bearing the MATa allele and another chromosome bearing the MATα allele.[19] The combination of the information encoded by the MATa allele (the a1 gene) and the MATα allele (the α1 and α2 genes) triggers the diploid transcriptional program.[20] Similarly, the presence of only a single allele of MAT, whether it is MATa or MATα, triggers the haploid transcriptional program.[21]

The alleles present at the MAT locus are sufficient to program the mating behaviour of the cell. For example, using genetic manipulations, a MATa allele can be added to a MATα haploid cell.[22] Despite having a haploid complement of chromosomes, the cell now has both the MATa and MATα alleles, and will behave like a diploid cell: it will not produce or respond to mating pheromones, and when starved will attempt to undergo meiosis, with fatal results.[23] Similarly, deletion of one copy of the MAT locus in a diploid cell, leaving only a single MATa or MATα allele, will cause a cell with a diploid complement of chromosomes to behave like a haploid cell.[24] [25]

Decision to mate

Mating in yeast is stimulated by the presence of a pheromone which binds to either the Ste2 receptor (in a-cells) or the Ste3 receptor (in α-cells).[26] [27] The binding of this pheromone then leads to the activation of a heterotrimeric G protein.[28] The dimeric portion of this G-protein recruits Ste5 (and its related MAPK cascade components) to the membrane, and ultimately results in the phosphorylation of Fus3.[29]

The switching mechanism arises as a result of competition between the Fus3 protein (a MAPK protein) and the phosphatase Ptc1.[30] These proteins both attempt to control the 4 phosphorylation sites of Ste5, a scaffold protein with Fus3 attempting to phosphorylate the phosphosites, and Ptc1 attempting to dephosphorylate them.[31]

Presence of α-factor induces recruitment of Ptc1 to Ste5 via a 4 amino acid motif located within the Ste5 phosphosites.[32] Ptc1 then dephosphorylates Ste5, ultimately resulting in the dissociation of the Fus3-Ste5 complex.[33] Fus3 dissociates in a switch-like manner, dependent on the phosphorylation state of the 4 phosphosites.[34] All 4 phosphosites must be dephosphorylated in order for Fus3 to dissociate.[35] [36] Fus3's ability to compete with Ptc1 decreases as Ptc1 is recruited, and thus the rate of dephosphorylation increases with the presence of pheromone.[37]

Kss1, a homologue of Fus3, does not affect shmooing, and does not contribute to the switch-like mating decision.[38] [39]

In yeast, mating as well as the production of shmoos occur via an all-or-none, switch-like mechanism.[40] This switch-like mechanism allows yeast cells to avoid making an unwise commitment to a highly demanding procedure.[41] However, not only does the mating decision need to be conservative (in order to avoid wasting energy), but it must also be fast to avoid losing the potential mate.[42]

The decision to mate is extremely sensitive. There are 3 ways in which this ultrasensitivity is maintained:

  1. Multi-site phosphorylation – Fus3 only dissociates from Ste5 and becomes fully active when all 4 of the phosphosites are dephosphorylated. Even one phosphorylated site will result in immunity to α-factor.[43]
  2. Two-stage binding – Fus3 and Ptc1 bind to separate docking sites on Ste5. Only after docking can they bind to, and act on, the phosphosites.[44]
  3. Steric hindrance – competition between Fus3 and Ptc1 to control the 4 phosphosites on Ste3

a and α yeast share the same mating response pathway, with the only difference being the type of receptor each mating type possesses.[45] Thus the above description, given for a-type yeast stimulated with α-factor, works equally well for α-type yeast stimulated with a-factor.[46] [47]

Mating type switching

Wild type haploid yeast are capable of switching mating type between a and α.[48] Consequently, even if a single haploid cell of a given mating type founds a colony of yeast, mating type switching will cause cells of both a and α mating types to be present in the population.[49] [50] Combined with the strong drive for haploid cells to mate with cells of the opposite mating type and form diploids, mating type switching and consequent mating will cause the majority of cells in a colony to be diploid, regardless of whether a haploid or diploid cell founded the colony.[51] The vast majority of yeast strains studied in laboratories have been altered such that they cannot perform mating type switching (by deletion of the HO gene;[52] see below); this allows the stable propagation of haploid yeast, as haploid cells of the a mating type will remain a cells (and α cells will remain α cells), and will not form diploids.

HML and HMR: the silent mating cassettes

Haploid yeast switch mating type by replacing the information present at the MAT locus.[53] For example, an a cell will switch to an α cell by replacing the MATa allele with the MATα allele.[54] This replacement of one allele of MAT for the other is possible because yeast cells carry an additional silenced copy of both the MATa and MATα alleles: the HML (homothallic mating left) locus typically carries a silenced copy of the MATα allele, and the HMR (homothallic mating right) locus typically carries a silenced copy of the MATa allele. The silent HML and HMR loci are often referred to as the silent mating cassettes, as the information present there is 'read into' the active MAT locus.[55]

These additional copies of the mating type information do not interfere with the function of whatever allele is present at the MAT locus because they are not expressed, so a haploid cell with the MATa allele present at the active MAT locus is still an a cell, despite also having a (silenced) copy of the MATα allele present at HML.[56] Only the allele present at the active MAT locus is transcribed, and thus only the allele present at MAT will influence cell behaviour. Hidden mating type loci are epigenetically silenced by SIR proteins, which form a heterochromatin scaffold that prevents transcription from the silent mating cassettes.[57]

Mechanics of the mating type switch

The process of mating type switching is a gene conversion event initiated by the HO gene.[58] The HO gene is a tightly regulated haploid-specific gene that is only activated in haploid cells during the G1 phase of the cell cycle.[59] The protein encoded by the HO gene is a DNA endonuclease, which physically cleaves DNA, but only at the MAT locus (due to the DNA sequence specificity of the HO endonuclease).[60]

Once HO cuts the DNA at MAT, exonucleases are attracted to the cut DNA ends and begin to degrade the DNA on both sides of the cut site.[61] This DNA degradation by exonucleases eliminates the DNA which encoded the MAT allele; however, the resulting gap in the DNA is repaired by copying in the genetic information present at either HML or HMR, filling in a new allele of either the MATa or MATα gene. Thus, the silenced alleles of MATa and MATα present at HML and HMR serve as a source of genetic information to repair the HO-induced DNA damage at the active MAT locus.

Directionality of the mating type switch

The repair of the MAT locus after cutting by the HO endonuclease almost always results in a mating type switch. When an a cell cuts the MATa allele present at the MAT locus, the cut at MAT will almost always be repaired by copying the information present at HML. This results in MAT being repaired to the MATα allele, switching the mating type of the cell from a to α.[62] Similarly, an α cell which has its MATα allele cut by the HO endonuclease will almost always repair the damage using the information present at HMR, copying the MATa gene to the MAT locus and switching the mating type of α cell to a.[63]

This is the result of the action of a recombination enhancer (RE) located on the left arm of chromosome III.[64] Deletion of this region causes a cells to incorrectly repair using HMR.[65] In a cells, Mcm1 binds to the RE and promotes recombination of the HML region.[66] In α cells, the α2 factor binds at the RE and establishes a repressive domain over RE such that recombination is unlikely to occur.[67] An innate bias means that the default behaviour is repair from HMR. The exact mechanisms of these interactions are still under investigation.[68]

Mating and inbreeding

Ruderfer et al.[69] analyzed the ancestry of natural S. cerevisiae strains and concluded that matings involving out-crossing occur only about once every 50,000 cell divisions. Thus it appears that, in nature, mating is most often between closely related yeast cells. Mating occurs when haploid cells of opposite mating type MATa and MATα come into contact. Ruderfer et al. pointed out that such contacts are frequent between closely related yeast cells for two reasons. The first is that cells of opposite mating type are present together in the same ascus, the sac that contains the cells directly produced by a single meiosis, and these cells can mate with each other. The second reason is that haploid cells of one mating type, upon cell division, often produce cells of the opposite mating type with which they can mate (see section "Mating type switching", above). The relative rarity in nature of meiotic events that result from out-crossing appears to be inconsistent with the idea that production of genetic variation is the primary selective force maintaining mating capability in this organism. However this finding is consistent with the alternative idea that the primary selective force maintaining mating capability is enhanced recombinational repair of DNA damage during meiosis,[70] since this benefit is realized during each meiosis subsequent to a mating, whether or not out-crossing occurs.

Special cases

Fission yeast

Schizosaccharomyces pombe is a facultative sexual yeast that can undergo mating when nutrients are limiting.[71] Exposure of S. pombe to hydrogen peroxide, an agent that causes oxidative stress leading to oxidative DNA damage, strongly induces mating, meiosis, and formation of meiotic spores.[72] This finding suggests that meiosis, and particularly meiotic recombination, may be an adaptation for repairing DNA damage.[73] The overall structure of the MAT locus is similar to that in S. cerevisiae. The mating-type switching system is similar, but has evolved independently.

Self-mating in Cryptococcus neoformans

Cryptococcus neoformans is a basidiomycetous fungus that grows as a budding yeast in culture and in an infected host. C. neoformans causes life-threatening meningoencephalitis in immune compromised patients. It undergoes a filamentous transition during the sexual cycle to produce spores, the suspected infectious agent. The vast majority of environmental and clinical isolates of C. neoformans are mating type α. Filaments ordinarily have haploid nuclei, but these can undergo a process of diploidization (perhaps by endoduplication or stimulated nuclear fusion) to form diploid cells termed blastospores.[74] The diploid nuclei of blastospores can then undergo meiosis, including recombination, to form haploid basidiospores that can then be dispersed. This process is referred to as monokaryotic fruiting. Required for this process is a gene designated dmc1, a conserved homologue of genes RecA in bacteria, and RAD51 in eukaryotes. Dmc1 mediates homologous chromosome pairing during meiosis and repair of double-strand breaks in DNA (see Meiosis; also Michod et al.[75]). Lin et al. suggested that one benefit of meiosis in C. neoformans could be to promote DNA repair in a DNA damaging environment that could include the defensive responses of the infected host.

Further reading

External links

study shows that there are great similarities between the parts of DNA that determine the sex of plants and animals and the parts of DNA that determine mating types in certain fungi. Accessed 5 April 2008.

Notes and References

  1. For the sake of clarity, this article bolds the Latin letter "a" and uses regular font weight for the Greek α. The usual convention is to print both in the same weight, but doing so would make the two letters hard to tell apart in italicized text.
  2. Book: Bergman LW . Two-Hybrid Systems . Growth and maintenance of yeast . Methods in Molecular Biology (Clifton, N.J.) . 177 . 9–14 . 2001 . 11530618 . 10.1385/1-59259-210-4:009 . 1-59259-210-4 .
  3. Börner GV, Hochwagen A, MacQueen AJ . Meiosis in budding yeast . Genetics . 225 . 2 . October 2023 . 37616582 . 10550323 . 10.1093/genetics/iyad125 .
  4. Michaelis S, Barrowman J . Biogenesis of the Saccharomyces cerevisiae pheromone a-factor, from yeast mating to human disease . Microbiology and Molecular Biology Reviews . 76 . 3 . 626–651 . September 2012 . 22933563 . 3429625 . 10.1128/MMBR.00010-12 .
  5. Merlini L, Dudin O, Martin SG . Mate and fuse: how yeast cells do it . Open Biology . 3 . 3 . 130008 . March 2013 . 23466674 . 3718343 . 10.1098/rsob.130008 .
  6. Chen W, Nie Q, Yi TM, Chou CS . Modelling of Yeast Mating Reveals Robustness Strategies for Cell-Cell Interactions . PLOS Computational Biology . 12 . 7 . e1004988 . July 2016 . 27404800 . 4942089 . 10.1371/journal.pcbi.1004988 . 2016PLSCB..12E4988C . free . Edelstein-Keshet L .
  7. Hanson SJ, Wolfe KH . An Evolutionary Perspective on Yeast Mating-Type Switching . Genetics . 206 . 1 . 9–32 . May 2017 . 28476860 . 5419495 . 10.1534/genetics.117.202036 .
  8. Haber JE . Mating-type genes and MAT switching in Saccharomyces cerevisiae . Genetics . 191 . 1 . 33–64 . May 2012 . 22555442 . 3338269 . 10.1534/genetics.111.134577 .
  9. Gastaldi S, Zamboni M, Bolasco G, Di Segni G, Tocchini-Valentini GP . Analysis of random PCR-originated mutants of the yeast Ste2 and Ste3 receptors . MicrobiologyOpen . 5 . 4 . 670–686 . August 2016 . 27150158 . 4985600 . 10.1002/mbo3.361 .
  10. Book: Brenner S, Miller JH . Encyclopedia of Genetics . . 2001 . 978-0-12-227080-2 . 275–278 . en . Cassette Model . 10.1006/rwgn.2001.0162 . 2024-05-09 . https://www.sciencedirect.com/science/article/abs/pii/B0122270800001622.
  11. Tsong AE, Miller MG, Raisner RM, Johnson AD . Evolution of a combinatorial transcriptional circuit: a case study in yeasts . Cell . 115 . 4 . 389–399 . November 2003 . 14622594 . 10.1016/S0092-8674(03)00885-7 . free .
  12. Lee CS, Haber JE . Mating-type Gene Switching in Saccharomyces cerevisiae . Microbiology Spectrum . 3 . 2 . April 2015 . MDNA3–0013–2014 . 26104712 . 10.1128/microbiolspec.MDNA3-0013-2014 . Gellert M, Craig N .
  13. Wagstaff JE, Klapholz S, Esposito RE . Meiosis in haploid yeast . Proceedings of the National Academy of Sciences of the United States of America . 79 . 9 . 2986–2990 . May 1982 . 7045878 . 10.1073/pnas.79.9.2986 . free . 346333 . 1982PNAS...79.2986W .
  14. Yeager R, Bushkin GG, Singer E, Fu R, Cooperman B, McMurray M . Post-Transcriptional Control of Mating-Type Gene Expression during Gametogenesis in Saccharomyces cerevisiae . Biomolecules . 11 . 8 . 1223 . August 2021 . 34439889 . 8394074 . 10.3390/biom11081223 . free .
  15. Solieri L, Cassanelli S, Huff F, Barroso L, Branduardi P, Louis EJ, Morrissey JP . Insights on life cycle and cell identity regulatory circuits for unlocking genetic improvement in Zygosaccharomyces and Kluyveromyces yeasts . FEMS Yeast Research . 21 . 8 . December 2021 . 34791177 . 8673824 . 10.1093/femsyr/foab058 .
  16. Nagaraj VH, O'Flanagan RA, Bruning AR, Mathias JR, Vershon AK, Sengupta AM . Combined analysis of expression data and transcription factor binding sites in the yeast genome . BMC Genomics . 5 . 1 . 59 . August 2004 . 15331021 . 517709 . 10.1186/1471-2164-5-59 . free .
  17. Voth WP, Stillman DJ . Changes in developmental state: demolish the old to construct the new . Genes & Development . 17 . 18 . 2201–2204 . September 2003 . 12975315 . 10.1101/gad.1142103 . free .
  18. Book: Watkinson SC, Boddy L, Money NP . The Fungi . . 2016 . 978-0-12-382034-1 . 3rd . 99–139 . en . Chapter 4 - Genetics – Variation, Sexuality, and Evolution . 10.1016/B978-0-12-382034-1.00004-9 . https://www.sciencedirect.com/science/article/abs/pii/B9780123820341000049.
  19. Bizzarri M, Giudici P, Cassanelli S, Solieri L . Chimeric Sex-Determining Chromosomal Regions and Dysregulation of Cell-Type Identity in a Sterile Zygosaccharomyces Allodiploid Yeast . PLOS ONE . 11 . 4 . e0152558 . 2016-04-11 . 27065237 . 4827841 . 10.1371/journal.pone.0152558 . 2016PLoSO..1152558B . free . Fairhead C .
  20. Zill OA, Rine J . Interspecies variation reveals a conserved repressor of alpha-specific genes in Saccharomyces yeasts . Genes & Development . 22 . 12 . 1704–1716 . June 2008 . 18559484 . 2428066 . 10.1101/gad.1640008 .
  21. Leupold U . Transposable mating-type genes in yeasts . Nature . 283 . 5750 . 811–812 . February 1980 . 6987523 . 10.1038/283811a0 . 1980Natur.283..811L .
  22. Book: Lennarz WJ, Lane MD . Encyclopedia of Biological Chemistry . . 2004 . 978-0-12-443710-4 . 200–203 . en . Transcriptional Silencing . 10.1016/B0-12-443710-9/00723-7 . 2024-05-09 . https://www.sciencedirect.com/science/article/abs/pii/B0124437109007237.
  23. Lengeler KB, Davidson RC, D'souza C, Harashima T, Shen WC, Wang P, Pan X, Waugh M, Heitman J . Signal transduction cascades regulating fungal development and virulence . Microbiology and Molecular Biology Reviews . 64 . 4 . 746–785 . December 2000 . 11104818 . 99013 . 10.1128/MMBR.64.4.746-785.2000 .
  24. Lee K, Neigeborn L, Kaufman RJ . The unfolded protein response is required for haploid tolerance in yeast . The Journal of Biological Chemistry . 278 . 14 . 11818–11827 . April 2003 . 12560331 . 10.1074/jbc.M210475200 . free .
  25. Book: Conn PM . Handbook of Models for Human Aging . . 2006 . 978-0-12-369391-4 . en . 17 - Telomeres and Aging in the Yeast Model System . 191–205 . 10.1016/B978-0-12-369391-4.X5000-0 . https://www.sciencedirect.com/science/article/abs/pii/B9780123693914500187.
  26. Versele M, Lemaire K, Thevelein JM . Sex and sugar in yeast: two distinct GPCR systems . EMBO Reports . 2 . 7 . 574–579 . July 2001 . 11463740 . 1083946 . 10.1093/embo-reports/kve132 .
  27. Emmerstorfer-Augustin A, Augustin CM, Shams S, Thorner J . Tracking yeast pheromone receptor Ste2 endocytosis using fluorogen-activating protein tagging . Molecular Biology of the Cell . 29 . 22 . 2720–2736 . November 2018 . 30207829 . 6249837 . 10.1091/mbc.E18-07-0424 . Glick BS .
  28. Navarro-Olmos R, Kawasaki L, Domínguez-Ramírez L, Ongay-Larios L, Pérez-Molina R, Coria R . The beta subunit of the heterotrimeric G protein triggers the Kluyveromyces lactis pheromone response pathway in the absence of the gamma subunit . Molecular Biology of the Cell . 21 . 3 . 489–498 . February 2010 . 20016006 . 2814793 . 10.1091/mbc.e09-06-0472 . Boone C .
  29. Winters MJ, Pryciak PM . MAPK modulation of yeast pheromone signaling output and the role of phosphorylation sites in the scaffold protein Ste5 . Molecular Biology of the Cell . 30 . 8 . 1037–1049 . April 2019 . 30726174 . 6589907 . 10.1091/mbc.E18-12-0793 . Boone C .
  30. Malleshaiah MK, Shahrezaei V, Swain PS, Michnick SW . The scaffold protein Ste5 directly controls a switch-like mating decision in yeast . Nature . 465 . 7294 . 101–105 . May 2010 . 20400943 . 10.1038/nature08946 . 2010Natur.465..101M .
  31. Choudhury S, Baradaran-Mashinchi P, Torres MP . Negative Feedback Phosphorylation of Gγ Subunit Ste18 and the Ste5 Scaffold Synergistically Regulates MAPK Activation in Yeast . Cell Reports . 23 . 5 . 1504–1515 . May 2018 . 29719261 . 5987779 . 10.1016/j.celrep.2018.03.135 .
  32. Chen RE, Thorner J . Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae . Biochimica et Biophysica Acta (BBA) - Molecular Cell Research . 1773 . 8 . 1311–1340 . August 2007 . 17604854 . 2031910 . 10.1016/j.bbamcr.2007.05.003 .
  33. Ariño J, Casamayor A, González A . Type 2C protein phosphatases in fungi . Eukaryotic Cell . 10 . 1 . 21–33 . January 2011 . 21076010 . 3019798 . 10.1128/EC.00249-10 .
  34. Nagiec MJ, McCarter PC, Kelley JB, Dixit G, Elston TC, Dohlman HG . Signal inhibition by a dynamically regulated pool of monophosphorylated MAPK . Molecular Biology of the Cell . 26 . 18 . 3359–3371 . September 2015 . 26179917 . 4569323 . 10.1091/mbc.e15-01-0037 . Boone C .
  35. Gartner A, Nasmyth K, Ammerer G . Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phosphorylation of FUS3 and KSS1 . Genes & Development . 6 . 7 . 1280–1292 . July 1992 . 1628831 . 10.1101/gad.6.7.1280 . free .
  36. Martins BM, Swain PS . Ultrasensitivity in phosphorylation-dephosphorylation cycles with little substrate . PLOS Computational Biology . 9 . 8 . e1003175 . 2013-08-08 . 23950701 . 3738489 . 10.1371/journal.pcbi.1003175 . free . 2013PLSCB...9E3175M . Mac Gabhann F .
  37. Ariño J, Velázquez D, Casamayor A . Ser/Thr protein phosphatases in fungi: structure, regulation and function . Microbial Cell . 6 . 5 . 217–256 . April 2019 . 31114794 . 6506691 . 10.15698/mic2019.05.677 .
  38. Li Y, Roberts J, AkhavanAghdam Z, Hao N . Mitogen-activated protein kinase (MAPK) dynamics determine cell fate in the yeast mating response . The Journal of Biological Chemistry . 292 . 50 . 20354–20361 . December 2017 . 29123025 . 5733576 . 10.1074/jbc.AC117.000548 . free .
  39. Errede B, Vered L, Ford E, Pena MI, Elston TC . Pheromone-induced morphogenesis and gradient tracking are dependent on the MAPK Fus3 binding to Gα . Molecular Biology of the Cell . 26 . 18 . 3343–3358 . September 2015 . 26179918 . 4569322 . 10.1091/mbc.e15-03-0176 . Boone C .
  40. Wang X, Tian W, Banh BT, Statler BM, Liang J, Stone DE . Mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine . The Journal of Cell Biology . 218 . 11 . 3730–3752 . November 2019 . 31570500 . 6829655 . 10.1083/jcb.201901155 .
  41. Marini G, Nüske E, Leng W, Alberti S, Pigino G . Reorganization of budding yeast cytoplasm upon energy depletion . Molecular Biology of the Cell . 31 . 12 . 1232–1245 . June 2020 . 32293990 . 7353153 . 10.1091/mbc.E20-02-0125 . Bloom K .
  42. Malek H, Long T . 2019-01-01 . Adventures in Time and Space: What Shapes Behavioural Decisions in Drosophila melanogaster? . Theses and Dissertations (Comprehensive).
  43. Liu X, Bardwell L, Nie Q . A combination of multisite phosphorylation and substrate sequestration produces switchlike responses . Biophysical Journal . 98 . 8 . 1396–1407 . April 2010 . 20409458 . 2856190 . 10.1016/j.bpj.2009.12.4307 . 2010BpJ....98.1396L .
  44. Bhaduri S, Pryciak PM . Cyclin-specific docking motifs promote phosphorylation of yeast signaling proteins by G1/S Cdk complexes . Current Biology . 21 . 19 . 1615–1623 . October 2011 . 21945277 . 3196376 . 10.1016/j.cub.2011.08.033 . 2011CBio...21.1615B .
  45. Gonçalves-Sá J, Murray A . Asymmetry in sexual pheromones is not required for ascomycete mating . Current Biology . 21 . 16 . 1337–1346 . August 2011 . 21835624 . 3159855 . 10.1016/j.cub.2011.06.054 . 2011CBio...21.1337G .
  46. Banderas A, Koltai M, Anders A, Sourjik V . Sensory input attenuation allows predictive sexual response in yeast . Nature Communications . 7 . 1 . 12590 . August 2016 . 27557894 . 5007329 . 10.1038/ncomms12590 . 2016NatCo...712590B .
  47. Muller N, Piel M, Calvez V, Voituriez R, Gonçalves-Sá J, Guo CL, Jiang X, Murray A, Meunier N . A Predictive Model for Yeast Cell Polarization in Pheromone Gradients . PLOS Computational Biology . 12 . 4 . e1004795 . April 2016 . 27077831 . 4831791 . 10.1371/journal.pcbi.1004795 . free . 2016PLSCB..12E4795M . Rao CV .
  48. Book: Brenner S, Miller JH . Encyclopedia of Genetics . . 2001 . 978-0-12-227080-2 . 798–800 . en . Gene Rearrangement in Eukaryotic Organisms . 10.1006/rwgn.2001.0518 . https://www.sciencedirect.com/science/article/abs/pii/B0122270800005188.
  49. Coughlan AY, Lombardi L, Braun-Galleani S, Martos AA, Galeote V, Bigey F, Dequin S, Byrne KP, Wolfe KH . The yeast mating-type switching endonuclease HO is a domesticated member of an unorthodox homing genetic element family . eLife . 9 . April 2020 . 32338594 . 7282813 . 10.7554/eLife.55336 . free .
  50. Laney JD, Hochstrasser M . Ubiquitin-dependent degradation of the yeast Mat(alpha)2 repressor enables a switch in developmental state . Genes & Development . 17 . 18 . 2259–2270 . September 2003 . 12952895 . 196463 . 10.1101/gad.1115703 .
  51. Wang Y, Lo WC, Chou CS . A modeling study of budding yeast colony formation and its relationship to budding pattern and aging . PLOS Computational Biology . 13 . 11 . e1005843 . November 2017 . 29121651 . 5697893 . 10.1371/journal.pcbi.1005843 . free . 2017PLSCB..13E5843W . Komarova NL .
  52. Book: Handbook of nucleic acid purification. 2009. CRC Press. Liu D . 9781420070972. Boca Raton. 614294429. 174.
  53. Shore D . Genetic recombination: sex-change operations in yeast . Current Biology . 7 . 1 . R24–R27 . January 1997 . 9072164 . 10.1016/S0960-9822(06)00012-1 . 1997CBio....7..R24S . free .
  54. Klar AJ . The yeast mating-type switching mechanism: a memoir . Genetics . 186 . 2 . 443–449 . October 2010 . 20940334 . 2942867 . 10.1534/genetics.110.122531 .
  55. Weber JM, Ehrenhofer-Murray AE . Design of a minimal silencer for the silent mating-type locus HML of Saccharomyces cerevisiae . Nucleic Acids Research . 38 . 22 . 7991–8000 . December 2010 . 20699276 . 3001064 . 10.1093/nar/gkq689 .
  56. Maroc L, Zhou-Li Y, Boisnard S, Fairhead C . A single Ho-induced double-strand break at the MAT locus is lethal in Candida glabrata . PLOS Genetics . 16 . 10 . e1008627 . October 2020 . 33057400 . 7591073 . 10.1371/journal.pgen.1008627 . free . Heitman J .
  57. Faure G, Jézéquel K, Roisné-Hamelin F, Bitard-Feildel T, Lamiable A, Marcand S, Callebaut I . Discovery and Evolution of New Domains in Yeast Heterochromatin Factor Sir4 and Its Partner Esc1 . Genome Biology and Evolution . 11 . 2 . 572–585 . February 2019 . 30668669 . 6394760 . 10.1093/gbe/evz010 . Wolfe K .
  58. Thon G, Maki T, Haber JE, Iwasaki H . Mating-type switching by homology-directed recombinational repair: a matter of choice . Current Genetics . 65 . 2 . 351–362 . April 2019 . 30382337 . 6420890 . 10.1007/s00294-018-0900-2 .
  59. Krebs JE, Kuo MH, Allis CD, Peterson CL . Cell cycle-regulated histone acetylation required for expression of the yeast HO gene . Genes & Development . 13 . 11 . 1412–1421 . June 1999 . 10364158 . 316758 . 10.1101/gad.13.11.1412 .
  60. Butler G, Kenny C, Fagan A, Kurischko C, Gaillardin C, Wolfe KH . Evolution of the MAT locus and its Ho endonuclease in yeast species . Proceedings of the National Academy of Sciences of the United States of America . 101 . 6 . 1632–1637 . February 2004 . 14745027 . 341799 . 10.1073/pnas.0304170101 . free . 2004PNAS..101.1632B .
  61. Pâques F, Haber JE . Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae . Microbiology and Molecular Biology Reviews . 63 . 2 . 349–404 . June 1999 . 10357855 . 98970 . 10.1128/MMBR.63.2.349-404.1999 .
  62. Belton JM, Lajoie BR, Audibert S, Cantaloube S, Lassadi I, Goiffon I, Baù D, Marti-Renom MA, Bystricky K, Dekker J . The Conformation of Yeast Chromosome III Is Mating Type Dependent and Controlled by the Recombination Enhancer . Cell Reports . 13 . 9 . 1855–1867 . December 2015 . 26655901 . 4681004 . 10.1016/j.celrep.2015.10.063 .
  63. Kaplun L, Ivantsiv Y, Bakhrat A, Raveh D . DNA damage response-mediated degradation of Ho endonuclease via the ubiquitin system involves its nuclear export . The Journal of Biological Chemistry . 278 . 49 . 48727–48734 . December 2003 . 14506225 . 10.1074/jbc.M308671200 . free .
  64. Houston P, Simon PJ, Broach JR . The Saccharomyces cerevisiae recombination enhancer biases recombination during interchromosomal mating-type switching but not in interchromosomal homologous recombination . Genetics . 166 . 3 . 1187–1197 . March 2004 . 15082540 . 1470794 . 10.1534/genetics.166.3.1187 .
  65. Ruan C, Workman JL, Simpson RT . The DNA repair protein yKu80 regulates the function of recombination enhancer during yeast mating type switching . Molecular and Cellular Biology . 25 . 19 . 8476–8485 . October 2005 . 16166630 . 1265738 . 10.1128/MCB.25.19.8476-8485.2005 .
  66. Wu C, Weiss K, Yang C, Harris MA, Tye BK, Newlon CS, Simpson RT, Haber JE . Mcm1 regulates donor preference controlled by the recombination enhancer in Saccharomyces mating-type switching . Genes & Development . 12 . 11 . 1726–1737 . June 1998 . 9620858 . 316872 . 10.1101/gad.12.11.1726 .
  67. Dodson AE, Rine J . Donor Preference Meets Heterochromatin: Moonlighting Activities of a Recombinational Enhancer in Saccharomyces cerevisiae . Genetics . 204 . 3 . 1065–1074 . November 2016 . 27655944 . 5105842 . 10.1534/genetics.116.194696 .
  68. Catalani E, Fanelli G, Silvestri F, Cherubini A, Del Quondam S, Bongiorni S, Taddei AR, Ceci M, De Palma C, Perrotta C, Rinalducci S, Prantera G, Cervia D . Nutraceutical Strategy to Counteract Eye Neurodegeneration and Oxidative Stress in Drosophila melanogaster Fed with High-Sugar Diet . Antioxidants . 10 . 8 . 1197 . July 2021 . 34439445 . 8388935 . 10.3390/antiox10081197 . free .
  69. Ruderfer DM, Pratt SC, Seidel HS, Kruglyak L . Population genomic analysis of outcrossing and recombination in yeast . Nature Genetics . 38 . 9 . 1077–1081 . September 2006 . 16892060 . 10.1038/ng1859 . 783720 .
  70. Book: Birdsell JA, Wills C . 2003 . The evolutionary origin and maintenance of sexual recombination: A review of contemporary models. . Evolutionary Biology Series . Evolutionary Biology . 33 . 27–137 . MacIntyre RJ, Clegg MT . Springer . 978-0306472619 .
  71. Davey J . Fusion of a fission yeast . Yeast . 14 . 16 . 1529–1566 . December 1998 . 9885154 . 10.1002/(SICI)1097-0061(199812)14:16<1529::AID-YEA357>3.0.CO;2-0 . 44652765 . free .
  72. Bernstein C, Johns V . Sexual reproduction as a response to H2O2 damage in Schizosaccharomyces pombe . Journal of Bacteriology . 171 . 4 . 1893–1897 . April 1989 . 2703462 . 209837 . 10.1128/jb.171.4.1893-1897.1989 .
  73. Staleva L, Hall A, Orlow SJ . Oxidative stress activates FUS1 and RLM1 transcription in the yeast Saccharomyces cerevisiae in an oxidant-dependent Manner . Molecular Biology of the Cell . 15 . 12 . 5574–5582 . December 2004 . 15385622 . 532035 . 10.1091/mbc.e04-02-0142 .
  74. Lin X, Hull CM, Heitman J . Sexual reproduction between partners of the same mating type in Cryptococcus neoformans . Nature . 434 . 7036 . 1017–1021 . April 2005 . 15846346 . 10.1038/nature03448 . 3195603 . 2005Natur.434.1017L .
  75. Michod RE, Bernstein H, Nedelcu AM . Adaptive value of sex in microbial pathogens . Infection, Genetics and Evolution . 8 . 3 . 267–285 . May 2008 . 18295550 . 10.1016/j.meegid.2008.01.002 . 2008InfGE...8..267M .

This article is licensed under the GNU Free Documentation License. It uses material from the Wikipedia article "Mating of yeast".

Except where otherwise indicated, Everything.Explained.Today is © Copyright 2009-2024, A B Cryer, All Rights Reserved. Cookie policy.