Meiosis is a common response to nutrient deprivation in yeasts. Our goal was to determine whether the yeast Saccharomyces paradoxus performed meiosis under other abiotic stress factors, specifically salt stress. We predicted that S. paradoxus meiosis would increase in the presence of salt because osmotic stress activates the IME1 transcription factor in its model yeast relative S. cerevisiae. Contrary to our prediction, the sporulation rate of S. paradoxus decreased as salinity increased. We hypothesize that this is due to salt inhibiting mitochondrial function, but more studies are needed to determine the cause.
","acknowledgements":"This work was conducted as part of Wheaton College’s Research Experience in Biology course series. We thank the Biological, Chemical, and Environmental Sciences department at Wheaton College Massachusetts for developing and maintaining this series. We also thank class members Julianne Coyne, Matt Fais, Syan Martin, and Juliana Michelon de Caux for conversations and input during development of this project. Publication fees were provided by the Jonah Cool student research fund awarded to Wheaton College Massachusetts.
","authors":[{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","dataCuration","investigation","methodology","writing_originalDraft","writing_reviewEditing"],"email":"germain_mima@wheatoncollege.edu","firstName":"Gemima","lastName":"Germain","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","formalAnalysis","investigation","methodology","writing_originalDraft","writing_reviewEditing"],"email":"lamphere_sylvia@wheatoncollege.edu","firstName":"Sylvia","lastName":"Lamphere","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","dataCuration","investigation","methodology","writing_reviewEditing"],"email":"molinari_ella@wheatoncollege.edu","firstName":"Ella","lastName":"Molinari","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["dataCuration","formalAnalysis","fundingAcquisition","investigation","project","resources","supervision","validation","visualization","writing_originalDraft","writing_reviewEditing"],"email":"boynton_primrose@wheatoncollege.edu","firstName":"Primrose","lastName":"Boynton","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0003-0720-8966"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":null,"extendedData":[{"description":"Sporulation data","doi":null,"resourceType":"Dataset","name":"sporulation data.csv","url":"https://portal.micropublication.org/uploads/8ca9ea742921a9306878e9daed5ede44.csv"}],"funding":"Publication fees were provided by the Jonah Cool student research fund awarded to Wheaton College Massachusetts.
","image":{"url":"https://portal.micropublication.org/uploads/d6f916b52b9bfe55c40583ef17d97470.jpeg"},"imageCaption":"Sporulation efficiency decreases as the amount of salt in the environment increases. A) Photograph of vegetative cells (1) and sporulated tetrads (2). B) Relationship between percent salt and proportion of cells sporulating. Small black points are individual sporulation observations; black lines connect values for the same S. paradoxus isolate. Large red points are averages for each category of salt percentage (0, 3%, or 6% sodium chloride).
","imageTitle":"S. paradoxus sporulation in different concentrations of salt
","methods":"We grew sixteen wild S. paradoxus isolates (Table 1), previously isolated from a German forest (Boynton et al. 2021), in each of three salt concentrations: no salt (0% NaCl), low salt (3% NaCl), and high salt (6% NaCl) (Table 2). We inoculated each isolate from a colony on a petri dish into 1 mL of each medium type using a sterile stick, and included uninoculated controls of each medium type. We incubated cultures at 26°C with 180 rpm (revolutions per minute) shaking. After seven days of incubation, we mixed each culture, pipetted 5 µl onto a microscope slide, and took a photograph under a compound microscope. We scored sporulation frequencies by drawing a transect on each photograph and counting sporulated and nonsporulated cells (Figure 1A), up to 100 total cells, along each transect. Spores are observed as four haploid cells inside an ascus formed during sporulation; non-spores remain in their vegetative state as single or budding cells (Figure 1A). Sporulation proportion is equal to the number of sporulated cells divided by 100 (the total number of counted cells).
We modeled proportions of cells sporulated as a function of salt concentration using a generalized mixed-effects model, modeling variance in sporulation using the binomial family with a logit link function; we varied slopes and intercepts for each S. paradoxus isolate to account for the repeated-measures design of our experiment. Marginal R2GLMM (i.e., proportion of variance in sporulation explained by salt concentration) (Nakagawa et al. 2017) was calculated using the theoretical method of determining binomial observation errors. Statistical analyses were done using R version 4.5.2 (R Core Team, 2025) and the tidyverse, lme4, AICcmodavg, and MuMIn packages (Bartón 2025, Bates et al. 2015, Mazerolle 2023, Wickham et al., 2019).
","reagents":"Table 1: Fungal strains
Species | Strain | Reference |
S. paradoxus | 5056 | Boynton et al. 2021 |
S. paradoxus | 5057 | Boynton et al. 2021 |
S. paradoxus | 5062 | Boynton et al. 2021 |
S. paradoxus | 5069 | Boynton et al. 2021 |
S. paradoxus | 5074 | Boynton et al. 2021 |
S. paradoxus | 5078 | Boynton et al. 2021 |
S. paradoxus | 5080 | Boynton et al. 2021 |
S. paradoxus | 5081 | Boynton et al. 2021 |
S. paradoxus | 5082 | Boynton et al. 2021 |
S. paradoxus | 5093 | Boynton et al. 2021 |
S. paradoxus | 5135 | Boynton et al. 2021 |
S. paradoxus | 5144 | Boynton et al. 2021 |
S. paradoxus | 5165 | Boynton et al. 2021 |
S. paradoxus | 5167 | Boynton et al. 2021 |
S. paradoxus | 5185 | Boynton et al. 2021 |
S. paradoxus | 5202 | Boynton et al. 2021 |
Table 2: Growth media
Medium | Composition |
YPD 0% salt | 10 g/L yeast extract, 20 g/L peptone, and 20 g/L dextrose |
YPD 3% salt | 10 g/L yeast extract, 20 g/L peptone, 20 g/L dextrose, and 30 g/L sodium chloride |
YPD 6% salt | 10 g/L yeast extract, 20 g/L peptone, 20 g/L dextrose, and 60 g/L sodium chloride |
Sex, the life cycle characterized by meiosis and mating, is facultative for most eukaryotes (Nieuwenhuis and James 2016, Speijer et al. 2015). Sexual life cycles have many costs compared to asexual reproduction, including reduced growth rates, metabolic investments in meiosis and mating, and costs of finding mates, but the machinery for sex is conserved over the eukaryotic tree of life because it is the primary mechanism for eukaryotic genetic recombination (Lehtonen et al. 2012, Speijer et al. 2015). The advantages of sexual recombination, especially in the face of changing environments, can explain its ubiquity (Becks and Agrawal 2012, Lively and Morran, 2014). Sex is favored in changing environments in experimental studies (Morran et al. 2011), and stressful environments often trigger meiosis in facultatively sexual eukaryotes (Ram and Hadany 2016, Schoustra et al. 2010). For example, the facultatively sexual model yeast Saccharomyces cerevisiae undergoes meiosis and produces haploid spores (sporulation) in laboratory environments when it is nutrient starved (Mitchell 1994) (Figure 1A), but its wild sister species S. paradoxus, which has similar physiology, rarely undergoes meiosis in non-domesticated environments (Tsai et al. 2008, Vaughan-Martini and Martini 2011). We would like to understand if meiosis as a response to stress is generalizable to a non-nutrient-related stressor in S. paradoxus.
Similarly to nutrient stress, we hypothesized that salt (sodium chloride) stress might increase S. paradoxus meiosis frequency. In Saccharomyces, meiosis is induced by the transcription factor IME1 (Vershon and Pierce 2000). In S. cerevisiae, signaling proteins in the Hog1 osmotic stress response pathway, triggered by high environmental sodium chloride, bind to regulatory DNA associated with IME1, inducing transcription (Kahana-Edwin et al. 2013). Additionally, salt increases crossovers during meiosis in another model eukaryote, Arabidopsis thaliana (van Tol et al. 2018). We hypothesized that these molecular mechanisms are likely to translate to increased S. paradoxus sporulation as environmental sodium chloride concentrations increase.
Contrary to our expectation, salt decreased S. paradoxus sporulation in a laboratory experiment. We cultured sixteen S. paradoxus strains, previously isolated from a forest in Germany, in growth medium with each of three salt concentrations: 0%, 3%, and 6%. We chose these salt concentrations because they affected a different Saccharomyces phenotype, sensitivity to killer toxins, in a different study (Llorente et al. 1997). We grew cells in standard growth media supplemented with sodium chloride (Table 2) for seven days. This long incubation allowed S. paradoxus cells to deplete carbon and nitrogen in the environment and begin to undergo meiosis. We scored cultures for sporulation frequency from photographs taken under a microscope. Sporulation decreased from a mean of 90% sporulated cells with no added salt to a mean of 67% with 6% salt (Z = -8.5, p < 10-15, marginal R2GLMM = 0.46, Figure 1B).
We hypothesize that interactions among salt stress, mitochondrial function, and meiosis might explain why meiosis decreased as salt concentration increased. Mitochondrial function is necessary for activating the IME1 transcription factor, which induces meiosis (Treinin and Simchen 1992, Zhao et al. 2018). Osmotic stress has a variety of potential impacts on mitochondrial function: it is associated with changes in mitochondrial gene expression and accumulation of reactive oxygen species in mitochondria (Di Noia et al. 2023, Pastor et al. 2009). Some mutations in S. cerevisiae cells also result in decreased respiration with salt stress (Guaragnella et al. 2021), suggesting that salt can directly inhibit respiration. An alternative explanation for our observations is that salt stress increased mitosis rates while meiosis rates stayed the same, decreasing the relative number of sporulated cells we saw. We consider this unlikely because salt stress is associated with the Hog1 pathway, which halts the mitotic cell cycle (de Nadal and Posas 2022). Other impacts of salt on cell function, such as increasing glycerol accumulation or disrupting DNA replication are more likely to increase meiotic frequency relative to mitosis (Cruz-León et al. 2022, Patel and Miller 1972), so we do not consider these responsible for the pattern we observed.
Our results suggest that, while sexual life cycles may be favored with nutrient stress, they are not favored in all stressful environments. This diversity in responses to stress could be a result of molecular interactions inside the cell, for example, in the mitochondrion; it also might reflect the diversity of ecological impacts of different stressors for individual yeast cells. The identities and importances of stressors S. paradoxus encounters in natural environments could explain its population-wide infrequent rate of meiosis (Tsai et al. 2008).
","references":[{"reference":"Bartoń K. 2010. MuMIn: Multi-Model Inference. CRAN: Contributed Packages : 10.32614/cran.package.mumin.
","pubmedId":"","doi":"10.32614/CRAN.package.MuMIn"},{"reference":"Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting Linear Mixed-Effects Models Using\n lme4. Journal of Statistical Software 67: 10.18637/jss.v067.i01.
","pubmedId":"","doi":"10.18637/jss.v067.i01"},{"reference":"Becks L, Agrawal AF. 2012. The evolution of sex is favoured during adaptation to new environments. PLoS Biol 10(5): e1001317.
","pubmedId":"22563299","doi":""},{"reference":"Boynton PJ, Wloch-Salamon D, Landermann D, Stukenbrock EH. 2021. Forest Saccharomyces paradoxus are robust to seasonal biotic and abiotic changes. Ecol Evol 11(11): 6604-6619.
","pubmedId":"34141244","doi":""},{"reference":"35640616
","pubmedId":"","doi":""},{"reference":"de Nadal E, Posas F. 2022. The HOG pathway and the regulation of osmoadaptive responses in yeast. FEMS Yeast Res 22(1): 10.1093/femsyr/foac013.
","pubmedId":"35254447","doi":""},{"reference":"Di Noia MA, Scarcia P, Agrimi G, Ocheja OB, Wahid E, Pisano I, et al., Guaragnella N. 2023. Inactivation of HAP4 Accelerates RTG-Dependent Osmoadaptation in Saccharomyces cerevisiae. Int J Mol Sci 24(6): 10.3390/ijms24065320.
","pubmedId":"36982394","doi":""},{"reference":"Guaragnella N, Agrimi G, Scarcia P, Suriano C, Pisano I, Bobba A, et al., Giannattasio S. 2021. RTG Signaling Sustains Mitochondrial Respiratory Capacity in HOG1-Dependent Osmoadaptation. Microorganisms 9(9): 10.3390/microorganisms9091894.
","pubmedId":"34576788","doi":""},{"reference":"Kahana-Edwin S, Stark M, Kassir Y. 2013. Multiple MAPK cascades regulate the transcription of IME1, the master transcriptional activator of meiosis in Saccharomyces cerevisiae. PLoS One 8(11): e78920.
","pubmedId":"24236068","doi":""},{"reference":"Lehtonen J, Jennions MD, Kokko H. 2012. The many costs of sex. Trends Ecol Evol 27(3): 172-8.
","pubmedId":"22019414","doi":""},{"reference":"Lively CM, Morran LT. 2014. The ecology of sexual reproduction. J Evol Biol 27(7): 1292-303.
","pubmedId":"24617324","doi":""},{"reference":"Llorente P, Marquina D, Santos A, Peinado JM, Spencer-Martins I. 1997. Effect of salt on the killer phenotype of yeasts from olive brines. Appl Environ Microbiol 63(3): 1165-7.
","pubmedId":"9055432","doi":""},{"reference":"Bartoń K. 2010. MuMIn: Multi-Model Inference. CRAN: Contributed Packages : 10.32614/cran.package.mumin.
","pubmedId":"","doi":"10.32614/CRAN.package.MuMIn "},{"reference":"Mitchell AP. 1994. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev 58(1): 56-70.
","pubmedId":"8177171","doi":""},{"reference":"Morran LT, Schmidt OG, Gelarden IA, Parrish RC 2nd, Lively CM. 2011. Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333(6039): 216-8.
","pubmedId":"21737739","doi":""},{"reference":"Nakagawa S, Johnson PCD, Schielzeth H. 2017. The coefficient of determination R(2) and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. J R Soc Interface 14(134): 10.1098/rsif.2017.0213.
","pubmedId":"28904005","doi":""},{"reference":"Nieuwenhuis BP, James TY. 2016. The frequency of sex in fungi. Philos Trans R Soc Lond B Biol Sci 371(1706): 10.1098/rstb.2015.0540.
","pubmedId":"27619703","doi":""},{"reference":"Pastor MM, Proft M, Pascual-Ahuir A. 2009. Mitochondrial function is an inducible determinant of osmotic stress adaptation in yeast. J Biol Chem 284(44): 30307-17.
","pubmedId":"19720830","doi":""},{"reference":"Patel PV, Miller JJ. 1972. Stimulation of yeast sporulation by glycerol. J Appl Bacteriol 35(1): 63-9.
","pubmedId":"4554448","doi":""},{"reference":"R Core Team. 2025. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
","pubmedId":"","doi":""},{"reference":"Ram Y, Hadany L. 2016. Condition-dependent sex: who does it, when and why? Philos Trans R Soc Lond B Biol Sci 371(1706): 10.1098/rstb.2015.0539.
","pubmedId":"27619702","doi":""},{"reference":"Schoustra S, Rundle HD, Dali R, Kassen R. 2010. Fitness-associated sexual reproduction in a filamentous fungus. Curr Biol 20(15): 1350-5.
","pubmedId":"20598542","doi":""},{"reference":"Speijer D, Lukeš J, Eliáš M. 2015. Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc Natl Acad Sci U S A 112(29): 8827-34.
","pubmedId":"26195746","doi":""},{"reference":"Treinin M, Simchen G. 1993. Mitochondrial activity is required for the expression of IME1, a regulator of meiosis in yeast. Curr Genet 23(3): 223-7.
","pubmedId":"8435851","doi":""},{"reference":"Tsai IJ, Bensasson D, Burt A, Koufopanou V. 2008. Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle. Proc Natl Acad Sci U S A 105(12): 4957-62.
","pubmedId":"18344325","doi":""},{"reference":"Vaughan-Martini A, Martini A. 2011. Saccharomyces Meyen ex Reess (1870). The Yeasts : 733-746.
","pubmedId":"","doi":"10.1016/B978-0-444-52149-1.00061-6"},{"reference":"van Tol N, Rolloos M, van Loon P, van der Zaal BJ. 2018. MeioSeed: a CellProfiler-based program to count fluorescent seeds for crossover frequency analysis in Arabidopsis thaliana. Plant Methods 14: 32.
","pubmedId":"29692862","doi":""},{"reference":"Vershon AK, Pierce M. 2000. Transcriptional regulation of meiosis in yeast. Curr Opin Cell Biol 12(3): 334-9.
","pubmedId":"10801467","doi":""},{"reference":"Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, et al., Yutani. 2019. Welcome to the Tidyverse. Journal of Open Source Software 4: 1686.
","pubmedId":"","doi":"10.21105/joss.01686"},{"reference":"Zhao H, Wang Q, Liu C, Shang Y, Wen F, Wang F, et al., Li W. 2018. A Role for the Respiratory Chain in Regulating Meiosis Initiation in Saccharomyces cerevisiae. Genetics 208(3): 1181-1194.
","pubmedId":"29301906","doi":""}],"title":"Sodium chloride stress inhibits Saccharomyces paradoxus meiosis
","reviews":[{"reviewer":{"displayName":"Catherine Gehring"},"openAcknowledgement":false,"status":{"submitted":true}}],"curatorReviews":[]},{"id":"bae01b98-ea86-41a0-ad85-3645180bf917","decision":"edit","abstract":"Meiosis is a common response to nutrient deprivation in yeasts. Our goal was to determine whether the yeast Saccharomyces paradoxus performed meiosis under other abiotic stress factors, specifically salt stress. We predicted that S. paradoxus meiosis would increase in the presence of salt because osmotic stress activates the IME1 transcription factor in its model yeast relative S. cerevisiae. Contrary to our prediction, the sporulation rate of S. paradoxus decreased as salinity increased. We hypothesize that this is due to salt inhibiting mitochondrial function, but more studies are needed to determine the cause.
","acknowledgements":"This work was conducted as part of Wheaton College’s Research Experience in Biology course series. We thank the Biological, Chemical, and Environmental Sciences department at Wheaton College, Massachusetts, for developing and maintaining this series. We also thank class members Julianne Coyne, Matt Fais, Syan Martin, and Juliana Michelon de Caux for conversations and input during development of this project.
","authors":[{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","dataCuration","investigation","methodology","writing_originalDraft","writing_reviewEditing"],"email":"germain_mima@wheatoncollege.edu","firstName":"Gemima","lastName":"Germain","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","formalAnalysis","investigation","methodology","writing_originalDraft","writing_reviewEditing"],"email":"lamphere_sylvia@wheatoncollege.edu","firstName":"Sylvia","lastName":"Lamphere","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","dataCuration","investigation","methodology","writing_reviewEditing"],"email":"molinari_ella@wheatoncollege.edu","firstName":"Ella","lastName":"Molinari","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["dataCuration","formalAnalysis","fundingAcquisition","investigation","project","resources","supervision","validation","visualization","writing_originalDraft","writing_reviewEditing"],"email":"boynton_primrose@wheatoncollege.edu","firstName":"Primrose","lastName":"Boynton","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0003-0720-8966"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[{"description":"Sporulation data","doi":null,"resourceType":"Dataset","name":"sporulation data.csv","url":"https://portal.micropublication.org/uploads/8ca9ea742921a9306878e9daed5ede44.csv"}],"funding":"This work was funded by the Biological, Chemical, and Environmental Sciences department at Wheaton College, Massachusetts. Publication fees were provided by Wheaton College’s Library, Technology, and Learning Committee.
","image":{"url":"https://portal.micropublication.org/uploads/d6f916b52b9bfe55c40583ef17d97470.jpeg"},"imageCaption":"Sporulation efficiency decreases as the amount of salt in the environment increases. A) Photograph of vegetative cells (1) and sporulated tetrads (2). B) Relationship between percent salt and proportion of cells sporulating. Small black points are individual sporulation observations; black lines connect values for the same S. paradoxus isolate. Large red points are averages for each category of salt percentage (0, 3%, or 6% sodium chloride).
","imageTitle":"S. paradoxus sporulation in different concentrations of salt
","methods":"We grew sixteen wild S. paradoxus isolates (Table 1) in each of three salt concentrations: no salt (0% NaCl), low salt (3% NaCl), and high salt (6% NaCl) (Table 2). All isolates had been isolated in 2017 or 2018 from soil or leaf litter next to oak trees in Nehmtener Forst, a mixed temperate forest in Nehmten, Schleswig-Holstein, Germany (Boynton et al. 2021). We inoculated each isolate from a colony on a petri dish into a single replicate of 1 mL of each medium type using a sterile stick and included uninoculated controls of each medium type to control for culture contamination. We incubated cultures at 26°C with 180 rpm (revolutions per minute) shaking. After seven days of incubation, we mixed each culture, pipetted 5 µl onto a microscope slide, and took a photograph under a compound microscope. We scored sporulation frequencies by drawing a transect on each photograph and counting sporulated and nonsporulated cells (Figure 1A), up to 100 total cells, along each transect. Spores are observed as four haploid cells inside an ascus formed during sporulation; non-spores remain in their vegetative state as single or budding cells (Figure 1A). Sporulation proportion is equal to the number of sporulated cells divided by 100 (the total number of counted cells).
We modeled proportions of cells sporulated as a function of salt concentration using a generalized mixed-effects model, modeling variance in sporulation using the binomial family with a logit link function; we varied slopes and intercepts for each S. paradoxus isolate to account for the repeated-measures design of our experiment. Marginal R2GLMM (i.e., proportion of variance in sporulation explained by salt concentration) (Nakagawa et al. 2017) was calculated using the theoretical method of determining binomial observation errors. Statistical analyses were done using R version 4.5.2 (R Core Team, 2025) and the tidyverse, lme4, AICcmodavg, and MuMIn packages (Bartón 2025, Bates et al. 2015, Mazerolle 2023, Wickham et al., 2019).
","reagents":"Table 1: Fungal strains
Species | Strain | Reference |
S. paradoxus | 5056 | Boynton et al. 2021 |
S. paradoxus | 5057 | Boynton et al. 2021 |
S. paradoxus | 5062 | Boynton et al. 2021 |
S. paradoxus | 5069 | Boynton et al. 2021 |
S. paradoxus | 5074 | Boynton et al. 2021 |
S. paradoxus | 5078 | Boynton et al. 2021 |
S. paradoxus | 5080 | Boynton et al. 2021 |
S. paradoxus | 5081 | Boynton et al. 2021 |
S. paradoxus | 5082 | Boynton et al. 2021 |
S. paradoxus | 5093 | Boynton et al. 2021 |
S. paradoxus | 5135 | Boynton et al. 2021 |
S. paradoxus | 5144 | Boynton et al. 2021 |
S. paradoxus | 5165 | Boynton et al. 2021 |
S. paradoxus | 5167 | Boynton et al. 2021 |
S. paradoxus | 5185 | Boynton et al. 2021 |
S. paradoxus | 5202 | Boynton et al. 2021 |
Table 2: Growth media
Medium | Composition |
YPD 0% salt | 10 g/L yeast extract, 20 g/L peptone, and 20 g/L dextrose |
YPD 3% salt | 10 g/L yeast extract, 20 g/L peptone, 20 g/L dextrose, and 30 g/L sodium chloride |
YPD 6% salt | 10 g/L yeast extract, 20 g/L peptone, 20 g/L dextrose, and 60 g/L sodium chloride |
Sex, the life cycle characterized by meiosis and mating, is facultative for most eukaryotes (Nieuwenhuis and James 2016, Speijer et al. 2015). Sexual life cycles have many costs compared to asexual reproduction, including reduced growth rates, metabolic investments in meiosis and mating, and costs of finding mates, but the machinery for sex is conserved over the eukaryotic tree of life because it is the primary mechanism for eukaryotic genetic recombination (Lehtonen et al. 2012, Speijer et al. 2015). The advantages of sexual recombination, especially in the face of changing environments, can explain its ubiquity (Becks and Agrawal 2012, Lively and Morran, 2014). Sex is favored in changing environments in experimental studies (Morran et al. 2011), and stressful environments often trigger meiosis in facultatively sexual eukaryotes (Ram and Hadany 2016, Schoustra et al. 2010). For example, the facultatively sexual model yeast Saccharomyces cerevisiae undergoes meiosis and produces haploid spores (sporulation) in laboratory environments when it is nutrient-starved (Mitchell 1994) (Figure 1A), but its wild sister species S. paradoxus, which has similar physiology, rarely undergoes meiosis in non-domesticated environments (Tsai et al. 2008, Vaughan-Martini and Martini 2011). We would like to understand if meiosis as a response to stress is generalizable to a non-nutrient-related stressor in S. paradoxus.
Similarly to nutrient stress, we hypothesized that salt (sodium chloride) stress might increase S. paradoxus meiosis frequency. In Saccharomyces, meiosis is induced by the transcription factor IME1 (Vershon and Pierce 2000). In S. cerevisiae, signaling proteins in the Hog1 osmotic stress response pathway, triggered by high environmental sodium chloride, bind to regulatory DNA associated with IME1, inducing transcription (Kahana-Edwin et al. 2013). Additionally, salt increases crossovers during meiosis in another model eukaryote, Arabidopsis thaliana (van Tol et al. 2018). We hypothesized that these molecular mechanisms are likely to translate to increased S. paradoxus sporulation as environmental sodium chloride concentrations increase. In this project, we tested whether increased sodium chloride concentrations increase rates of S. paradoxus meiosis.
Contrary to our expectation, salt decreased S. paradoxus sporulation in a laboratory experiment. We cultured sixteen S. paradoxus strains, previously isolated from a forest in Germany, in growth medium with each of three salt concentrations: 0%, 3%, and 6%. We chose these salt concentrations because they affected a different Saccharomyces phenotype, sensitivity to killer toxins, in a different study (Llorente et al. 1997). We grew cells in standard growth media supplemented with sodium chloride (Table 2) for seven days. This long incubation allowed S. paradoxus cells to deplete carbon and nitrogen in the environment and begin to undergo meiosis. We scored cultures for sporulation frequency from photographs taken under a microscope. Sporulation decreased from a mean of 90% sporulated cells with no added salt to a mean of 67% with 6% salt (Z = -8.5, p < 10-15, marginal R2GLMM = 0.46, Figure 1B).
We hypothesize that interactions among salt stress, mitochondrial function, and meiosis might explain why meiosis decreased as salt concentration increased. Mitochondrial function is necessary for activating the IME1 transcription factor, which induces meiosis (Treinin and Simchen 1992, Zhao et al. 2018). Osmotic stress has a variety of potential impacts on mitochondrial function: it is associated with changes in mitochondrial gene expression and accumulation of reactive oxygen species in mitochondria (Di Noia et al. 2023, Pastor et al. 2009). Some mutations in S. cerevisiae cells also result in decreased respiration with salt stress (Guaragnella et al. 2021), suggesting that salt can directly inhibit respiration. An alternative explanation for our observations is that salt stress increased mitosis rates while meiosis rates stayed the same, decreasing the relative number of sporulated cells we saw. We consider this unlikely because salt stress is associated with the Hog1 pathway, which halts the mitotic cell cycle (de Nadal and Posas 2022). Other impacts of salt on cell function, such as increasing glycerol accumulation or disrupting DNA replication, are more likely to increase meiotic frequency relative to mitosis (Cruz-León et al. 2022, Patel and Miller 1972), so we do not consider these responsible for the pattern we observed.
Our results suggest that, while sexual life cycles may be favored with nutrient stress, they are not favored in all stressful environments. This diversity in responses to stress could be a result of molecular interactions inside the cell, for example, in the mitochondrion; it also might reflect the diversity of ecological impacts of different stressors for individual yeast cells. The identities and importances of stressors S. paradoxus encounters in natural environments could explain its population-wide infrequent rate of meiosis (Tsai et al. 2008).
","references":[{"reference":"Bartoń K. 2010. MuMIn: Multi-Model Inference. CRAN: Contributed Packages : 10.32614/cran.package.mumin.
","pubmedId":"","doi":"10.32614/CRAN.package.MuMIn"},{"reference":"Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting Linear Mixed-Effects Models Using\n lme4. Journal of Statistical Software 67: 10.18637/jss.v067.i01.
","pubmedId":"","doi":"10.18637/jss.v067.i01"},{"reference":"Becks L, Agrawal AF. 2012. The evolution of sex is favoured during adaptation to new environments. PLoS Biol 10(5): e1001317.
","pubmedId":"22563299","doi":""},{"reference":"Boynton PJ, Wloch-Salamon D, Landermann D, Stukenbrock EH. 2021. Forest Saccharomyces paradoxus are robust to seasonal biotic and abiotic changes. Ecol Evol 11(11): 6604-6619.
","pubmedId":"34141244","doi":""},{"reference":"35640616
","pubmedId":"","doi":""},{"reference":"de Nadal E, Posas F. 2022. The HOG pathway and the regulation of osmoadaptive responses in yeast. FEMS Yeast Res 22(1): 10.1093/femsyr/foac013.
","pubmedId":"35254447","doi":""},{"reference":"Di Noia MA, Scarcia P, Agrimi G, Ocheja OB, Wahid E, Pisano I, et al., Guaragnella N. 2023. Inactivation of HAP4 Accelerates RTG-Dependent Osmoadaptation in Saccharomyces cerevisiae. Int J Mol Sci 24(6): 10.3390/ijms24065320.
","pubmedId":"36982394","doi":""},{"reference":"Guaragnella N, Agrimi G, Scarcia P, Suriano C, Pisano I, Bobba A, et al., Giannattasio S. 2021. RTG Signaling Sustains Mitochondrial Respiratory Capacity in HOG1-Dependent Osmoadaptation. Microorganisms 9(9): 10.3390/microorganisms9091894.
","pubmedId":"34576788","doi":""},{"reference":"Kahana-Edwin S, Stark M, Kassir Y. 2013. Multiple MAPK cascades regulate the transcription of IME1, the master transcriptional activator of meiosis in Saccharomyces cerevisiae. PLoS One 8(11): e78920.
","pubmedId":"24236068","doi":""},{"reference":"Lehtonen J, Jennions MD, Kokko H. 2012. The many costs of sex. Trends Ecol Evol 27(3): 172-8.
","pubmedId":"22019414","doi":""},{"reference":"Lively CM, Morran LT. 2014. The ecology of sexual reproduction. J Evol Biol 27(7): 1292-303.
","pubmedId":"24617324","doi":""},{"reference":"Llorente P, Marquina D, Santos A, Peinado JM, Spencer-Martins I. 1997. Effect of salt on the killer phenotype of yeasts from olive brines. Appl Environ Microbiol 63(3): 1165-7.
","pubmedId":"9055432","doi":""},{"reference":"Bartoń K. 2010. MuMIn: Multi-Model Inference. CRAN: Contributed Packages : 10.32614/cran.package.mumin.
","pubmedId":"","doi":"10.32614/CRAN.package.MuMIn "},{"reference":"Mitchell AP. 1994. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev 58(1): 56-70.
","pubmedId":"8177171","doi":""},{"reference":"Morran LT, Schmidt OG, Gelarden IA, Parrish RC 2nd, Lively CM. 2011. Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333(6039): 216-8.
","pubmedId":"21737739","doi":""},{"reference":"Nakagawa S, Johnson PCD, Schielzeth H. 2017. The coefficient of determination R(2) and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. J R Soc Interface 14(134): 10.1098/rsif.2017.0213.
","pubmedId":"28904005","doi":""},{"reference":"Nieuwenhuis BP, James TY. 2016. The frequency of sex in fungi. Philos Trans R Soc Lond B Biol Sci 371(1706): 10.1098/rstb.2015.0540.
","pubmedId":"27619703","doi":""},{"reference":"Pastor MM, Proft M, Pascual-Ahuir A. 2009. Mitochondrial function is an inducible determinant of osmotic stress adaptation in yeast. J Biol Chem 284(44): 30307-17.
","pubmedId":"19720830","doi":""},{"reference":"Patel PV, Miller JJ. 1972. Stimulation of yeast sporulation by glycerol. J Appl Bacteriol 35(1): 63-9.
","pubmedId":"4554448","doi":""},{"reference":"R Core Team. 2025. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
","pubmedId":"","doi":""},{"reference":"Ram Y, Hadany L. 2016. Condition-dependent sex: who does it, when and why? Philos Trans R Soc Lond B Biol Sci 371(1706): 10.1098/rstb.2015.0539.
","pubmedId":"27619702","doi":""},{"reference":"Schoustra S, Rundle HD, Dali R, Kassen R. 2010. Fitness-associated sexual reproduction in a filamentous fungus. Curr Biol 20(15): 1350-5.
","pubmedId":"20598542","doi":""},{"reference":"Speijer D, Lukeš J, Eliáš M. 2015. Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc Natl Acad Sci U S A 112(29): 8827-34.
","pubmedId":"26195746","doi":""},{"reference":"Treinin M, Simchen G. 1993. Mitochondrial activity is required for the expression of IME1, a regulator of meiosis in yeast. Curr Genet 23(3): 223-7.
","pubmedId":"8435851","doi":""},{"reference":"Tsai IJ, Bensasson D, Burt A, Koufopanou V. 2008. Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle. Proc Natl Acad Sci U S A 105(12): 4957-62.
","pubmedId":"18344325","doi":""},{"reference":"Vaughan-Martini A, Martini A. 2011. Saccharomyces Meyen ex Reess (1870). The Yeasts : 733-746.
","pubmedId":"","doi":"10.1016/B978-0-444-52149-1.00061-6"},{"reference":"van Tol N, Rolloos M, van Loon P, van der Zaal BJ. 2018. MeioSeed: a CellProfiler-based program to count fluorescent seeds for crossover frequency analysis in Arabidopsis thaliana. Plant Methods 14: 32.
","pubmedId":"29692862","doi":""},{"reference":"Vershon AK, Pierce M. 2000. Transcriptional regulation of meiosis in yeast. Curr Opin Cell Biol 12(3): 334-9.
","pubmedId":"10801467","doi":""},{"reference":"Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, et al., Yutani. 2019. Welcome to the Tidyverse. Journal of Open Source Software 4: 1686.
","pubmedId":"","doi":"10.21105/joss.01686"},{"reference":"Zhao H, Wang Q, Liu C, Shang Y, Wen F, Wang F, et al., Li W. 2018. A Role for the Respiratory Chain in Regulating Meiosis Initiation in Saccharomyces cerevisiae. Genetics 208(3): 1181-1194.
","pubmedId":"29301906","doi":""}],"title":"Sodium chloride stress inhibits Saccharomyces paradoxus meiosis
","reviews":[],"curatorReviews":[]},{"id":"72dbbbe7-1c7e-4f67-a037-a914d4548700","decision":"accept","abstract":"Meiosis is a common response to nutrient deprivation in yeasts. Our goal was to determine whether the yeast Saccharomyces paradoxus performed meiosis under other abiotic stress factors, specifically salt stress. We predicted that S. paradoxus meiosis would increase in the presence of salt because osmotic stress activates the IME1 transcription factor in its model yeast relative S. cerevisiae. Contrary to our prediction, the sporulation rate of S. paradoxus decreased as salinity increased. We hypothesize that this is due to salt inhibiting mitochondrial function, but more studies are needed to determine the cause.
","acknowledgements":"This work was conducted as part of Wheaton College’s Research Experience in Biology course series. We thank the Biological, Chemical, and Environmental Sciences department at Wheaton College, Massachusetts, for developing and maintaining this series. We also thank class members Julianne Coyne, Matt Fais, Syan Martin, and Juliana Michelon de Caux for conversations and input during development of this project.
","authors":[{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","dataCuration","investigation","methodology","writing_originalDraft","writing_reviewEditing"],"email":"germain_mima@wheatoncollege.edu","firstName":"Gemima","lastName":"Germain","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","formalAnalysis","investigation","methodology","writing_originalDraft","writing_reviewEditing"],"email":"lamphere_sylvia@wheatoncollege.edu","firstName":"Sylvia","lastName":"Lamphere","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","dataCuration","investigation","methodology","writing_reviewEditing"],"email":"molinari_ella@wheatoncollege.edu","firstName":"Ella","lastName":"Molinari","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["dataCuration","formalAnalysis","fundingAcquisition","investigation","project","resources","supervision","validation","visualization","writing_originalDraft","writing_reviewEditing"],"email":"boynton_primrose@wheatoncollege.edu","firstName":"Primrose","lastName":"Boynton","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0003-0720-8966"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[{"description":"Sporulation data","doi":"10.22002/b0mff-2ex45","resourceType":"Dataset","name":"sporulation data.csv","url":"https://portal.micropublication.org/uploads/8ca9ea742921a9306878e9daed5ede44.csv"}],"funding":"This work was funded by the Biological, Chemical, and Environmental Sciences department at Wheaton College, Massachusetts. Publication fees were provided by Wheaton College’s Library, Technology, and Learning Committee.
","image":{"url":"https://portal.micropublication.org/uploads/d6f916b52b9bfe55c40583ef17d97470.jpeg"},"imageCaption":"Sporulation efficiency decreases as the amount of salt in the environment increases. A) Photograph of vegetative cells (1) and sporulated tetrads (2). B) Relationship between percent salt and proportion of cells sporulating. Small black points are individual sporulation observations; black lines connect values for the same S. paradoxus isolate. Large red points are averages for each category of salt percentage (0, 3%, or 6% sodium chloride).
","imageTitle":"S. paradoxus sporulation in different concentrations of salt
","methods":"We grew sixteen wild S. paradoxus isolates (Table 1) in each of three salt concentrations: no salt (0% NaCl), low salt (3% NaCl), and high salt (6% NaCl) (Table 2). All isolates had been isolated in 2017 or 2018 from soil or leaf litter next to oak trees in Nehmtener Forst, a mixed temperate forest in Nehmten, Schleswig-Holstein, Germany (Boynton et al. 2021). We inoculated each isolate from a colony on a petri dish into a single replicate of 1 mL of each medium type using a sterile stick and included uninoculated controls of each medium type to control for culture contamination. We incubated cultures at 26°C with 180 rpm (revolutions per minute) shaking. After seven days of incubation, we mixed each culture, pipetted 5 µl onto a microscope slide, and took a photograph under a compound microscope. We scored sporulation frequencies by drawing a transect on each photograph and counting sporulated and nonsporulated cells (Figure 1A), up to 100 total cells, along each transect. Spores are observed as four haploid cells inside an ascus formed during sporulation; non-spores remain in their vegetative state as single or budding cells (Figure 1A). Sporulation proportion is equal to the number of sporulated cells divided by 100 (the total number of counted cells).
We modeled proportions of cells sporulated as a function of salt concentration using a generalized mixed-effects model, modeling variance in sporulation using the binomial family with a logit link function; we varied slopes and intercepts for each S. paradoxus isolate to account for the repeated-measures design of our experiment. Marginal R2GLMM (i.e., proportion of variance in sporulation explained by salt concentration) (Nakagawa et al. 2017) was calculated using the theoretical method of determining binomial observation errors. Statistical analyses were done using R version 4.5.2 (R Core Team, 2025) and the tidyverse, lme4, AICcmodavg, and MuMIn packages (Bartón 2025, Bates et al. 2015, Mazerolle 2023, Wickham et al., 2019).
","reagents":"Table 1: Fungal strains
Species | Strain | Reference |
S. paradoxus | 5056 | Boynton et al. 2021 |
S. paradoxus | 5057 | Boynton et al. 2021 |
S. paradoxus | 5062 | Boynton et al. 2021 |
S. paradoxus | 5069 | Boynton et al. 2021 |
S. paradoxus | 5074 | Boynton et al. 2021 |
S. paradoxus | 5078 | Boynton et al. 2021 |
S. paradoxus | 5080 | Boynton et al. 2021 |
S. paradoxus | 5081 | Boynton et al. 2021 |
S. paradoxus | 5082 | Boynton et al. 2021 |
S. paradoxus | 5093 | Boynton et al. 2021 |
S. paradoxus | 5135 | Boynton et al. 2021 |
S. paradoxus | 5144 | Boynton et al. 2021 |
S. paradoxus | 5165 | Boynton et al. 2021 |
S. paradoxus | 5167 | Boynton et al. 2021 |
S. paradoxus | 5185 | Boynton et al. 2021 |
S. paradoxus | 5202 | Boynton et al. 2021 |
Table 2: Growth media
Medium | Composition |
YPD 0% salt | 10 g/L yeast extract, 20 g/L peptone, and 20 g/L dextrose |
YPD 3% salt | 10 g/L yeast extract, 20 g/L peptone, 20 g/L dextrose, and 30 g/L sodium chloride |
YPD 6% salt | 10 g/L yeast extract, 20 g/L peptone, 20 g/L dextrose, and 60 g/L sodium chloride |
Sex, the life cycle characterized by meiosis and mating, is facultative for most eukaryotes (Nieuwenhuis and James 2016, Speijer et al. 2015). Sexual life cycles have many costs compared to asexual reproduction, including reduced growth rates, metabolic investments in meiosis and mating, and costs of finding mates, but the machinery for sex is conserved over the eukaryotic tree of life because it is the primary mechanism for eukaryotic genetic recombination (Lehtonen et al. 2012, Speijer et al. 2015). The advantages of sexual recombination, especially in the face of changing environments, can explain its ubiquity (Becks and Agrawal 2012, Lively and Morran, 2014). Sex is favored in changing environments in experimental studies (Morran et al. 2011), and stressful environments often trigger meiosis in facultatively sexual eukaryotes (Ram and Hadany 2016, Schoustra et al. 2010). For example, the facultatively sexual model yeast Saccharomyces cerevisiae undergoes meiosis and produces haploid spores (sporulation) in laboratory environments when it is nutrient-starved (Mitchell 1994) (Figure 1A), but its wild sister species S. paradoxus, which has similar physiology, rarely undergoes meiosis in non-domesticated environments (Tsai et al. 2008, Vaughan-Martini and Martini 2011). We would like to understand if meiosis as a response to stress is generalizable to a non-nutrient-related stressor in S. paradoxus.
Similarly to nutrient stress, we hypothesized that salt (sodium chloride) stress might increase S. paradoxus meiosis frequency. In Saccharomyces, meiosis is induced by the transcription factor IME1 (Vershon and Pierce 2000). In S. cerevisiae, signaling proteins in the Hog1 osmotic stress response pathway, triggered by high environmental sodium chloride, bind to regulatory DNA associated with IME1, inducing transcription (Kahana-Edwin et al. 2013). Additionally, salt increases crossovers during meiosis in another model eukaryote, Arabidopsis thaliana (van Tol et al. 2018). We hypothesized that these molecular mechanisms are likely to translate to increased S. paradoxus sporulation as environmental sodium chloride concentrations increase. In this project, we tested whether increased sodium chloride concentrations increase rates of S. paradoxus meiosis.
Contrary to our expectation, salt decreased S. paradoxus sporulation in a laboratory experiment. We cultured sixteen S. paradoxus strains, previously isolated from a forest in Germany, in growth medium with each of three salt concentrations: 0%, 3%, and 6%. We chose these salt concentrations because they affected a different Saccharomyces phenotype, sensitivity to killer toxins, in a different study (Llorente et al. 1997). We grew cells in standard growth media supplemented with sodium chloride (Table 2) for seven days. This long incubation allowed S. paradoxus cells to deplete carbon and nitrogen in the environment and begin to undergo meiosis. We scored cultures for sporulation frequency from photographs taken under a microscope. Sporulation decreased from a mean of 90% sporulated cells with no added salt to a mean of 67% with 6% salt (Z = -8.5, p < 10-15, marginal R2GLMM = 0.46, Figure 1B).
We hypothesize that interactions among salt stress, mitochondrial function, and meiosis might explain why meiosis decreased as salt concentration increased. Mitochondrial function is necessary for activating the IME1 transcription factor, which induces meiosis (Treinin and Simchen 1992, Zhao et al. 2018). Osmotic stress has a variety of potential impacts on mitochondrial function: it is associated with changes in mitochondrial gene expression and accumulation of reactive oxygen species in mitochondria (Di Noia et al. 2023, Pastor et al. 2009). Some mutations in S. cerevisiae cells also result in decreased respiration with salt stress (Guaragnella et al. 2021), suggesting that salt can directly inhibit respiration. An alternative explanation for our observations is that salt stress increased mitosis rates while meiosis rates stayed the same, decreasing the relative number of sporulated cells we saw. We consider this unlikely because salt stress is associated with the Hog1 pathway, which halts the mitotic cell cycle (de Nadal and Posas 2022). Other impacts of salt on cell function, such as increasing glycerol accumulation or disrupting DNA replication, are more likely to increase meiotic frequency relative to mitosis (Cruz-León et al. 2022, Patel and Miller 1972), so we do not consider these responsible for the pattern we observed.
Our results suggest that, while sexual life cycles may be favored with nutrient stress, they are not favored in all stressful environments. This diversity in responses to stress could be a result of molecular interactions inside the cell, for example, in the mitochondrion; it also might reflect the diversity of ecological impacts of different stressors for individual yeast cells. The identities and importances of stressors S. paradoxus encounters in natural environments could explain its population-wide infrequent rate of meiosis (Tsai et al. 2008).
","references":[{"reference":"Bartoń K. 2010. MuMIn: Multi-Model Inference. CRAN: Contributed Packages : 10.32614/cran.package.mumin.
","pubmedId":"","doi":"10.32614/CRAN.package.MuMIn"},{"reference":"Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting Linear Mixed-Effects Models Using\n lme4. Journal of Statistical Software 67: 10.18637/jss.v067.i01.
","pubmedId":"","doi":"10.18637/jss.v067.i01"},{"reference":"Becks L, Agrawal AF. 2012. The evolution of sex is favoured during adaptation to new environments. PLoS Biol 10(5): e1001317.
","pubmedId":"22563299","doi":""},{"reference":"Boynton PJ, Wloch-Salamon D, Landermann D, Stukenbrock EH. 2021. Forest Saccharomyces paradoxus are robust to seasonal biotic and abiotic changes. Ecol Evol 11(11): 6604-6619.
","pubmedId":"34141244","doi":""},{"reference":"Cruz-León S, Vanderlinden W, Müller P, Forster T, Staudt G, Lin YY, Lipfert J, Schwierz N. 2022. Twisting DNA by salt. Nucleic Acids Res 50(10): 5726-5738.
","pubmedId":"35640616","doi":""},{"reference":"de Nadal E, Posas F. 2022. The HOG pathway and the regulation of osmoadaptive responses in yeast. FEMS Yeast Res 22(1): 10.1093/femsyr/foac013.
","pubmedId":"35254447","doi":""},{"reference":"Di Noia MA, Scarcia P, Agrimi G, Ocheja OB, Wahid E, Pisano I, et al., Guaragnella N. 2023. Inactivation of HAP4 Accelerates RTG-Dependent Osmoadaptation in Saccharomyces cerevisiae. Int J Mol Sci 24(6): 10.3390/ijms24065320.
","pubmedId":"36982394","doi":""},{"reference":"Guaragnella N, Agrimi G, Scarcia P, Suriano C, Pisano I, Bobba A, et al., Giannattasio S. 2021. RTG Signaling Sustains Mitochondrial Respiratory Capacity in HOG1-Dependent Osmoadaptation. Microorganisms 9(9): 10.3390/microorganisms9091894.
","pubmedId":"34576788","doi":""},{"reference":"Kahana-Edwin S, Stark M, Kassir Y. 2013. Multiple MAPK cascades regulate the transcription of IME1, the master transcriptional activator of meiosis in Saccharomyces cerevisiae. PLoS One 8(11): e78920.
","pubmedId":"24236068","doi":""},{"reference":"Lehtonen J, Jennions MD, Kokko H. 2012. The many costs of sex. Trends Ecol Evol 27(3): 172-8.
","pubmedId":"22019414","doi":""},{"reference":"Lively CM, Morran LT. 2014. The ecology of sexual reproduction. J Evol Biol 27(7): 1292-303.
","pubmedId":"24617324","doi":""},{"reference":"Llorente P, Marquina D, Santos A, Peinado JM, Spencer-Martins I. 1997. Effect of salt on the killer phenotype of yeasts from olive brines. Appl Environ Microbiol 63(3): 1165-7.
","pubmedId":"9055432","doi":""},{"reference":"Bartoń K. 2010. MuMIn: Multi-Model Inference. CRAN: Contributed Packages : 10.32614/cran.package.mumin.
","pubmedId":"","doi":"10.32614/CRAN.package.MuMIn "},{"reference":"Mitchell AP. 1994. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev 58(1): 56-70.
","pubmedId":"8177171","doi":""},{"reference":"Morran LT, Schmidt OG, Gelarden IA, Parrish RC 2nd, Lively CM. 2011. Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333(6039): 216-8.
","pubmedId":"21737739","doi":""},{"reference":"Nakagawa S, Johnson PCD, Schielzeth H. 2017. The coefficient of determination R(2) and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. J R Soc Interface 14(134): 10.1098/rsif.2017.0213.
","pubmedId":"28904005","doi":""},{"reference":"Nieuwenhuis BP, James TY. 2016. The frequency of sex in fungi. Philos Trans R Soc Lond B Biol Sci 371(1706): 10.1098/rstb.2015.0540.
","pubmedId":"27619703","doi":""},{"reference":"Pastor MM, Proft M, Pascual-Ahuir A. 2009. Mitochondrial function is an inducible determinant of osmotic stress adaptation in yeast. J Biol Chem 284(44): 30307-17.
","pubmedId":"19720830","doi":""},{"reference":"Patel PV, Miller JJ. 1972. Stimulation of yeast sporulation by glycerol. J Appl Bacteriol 35(1): 63-9.
","pubmedId":"4554448","doi":""},{"reference":"R Core Team. 2025. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
","pubmedId":"","doi":""},{"reference":"Ram Y, Hadany L. 2016. Condition-dependent sex: who does it, when and why? Philos Trans R Soc Lond B Biol Sci 371(1706): 10.1098/rstb.2015.0539.
","pubmedId":"27619702","doi":""},{"reference":"Schoustra S, Rundle HD, Dali R, Kassen R. 2010. Fitness-associated sexual reproduction in a filamentous fungus. Curr Biol 20(15): 1350-5.
","pubmedId":"20598542","doi":""},{"reference":"Speijer D, Lukeš J, Eliáš M. 2015. Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc Natl Acad Sci U S A 112(29): 8827-34.
","pubmedId":"26195746","doi":""},{"reference":"Treinin M, Simchen G. 1993. Mitochondrial activity is required for the expression of IME1, a regulator of meiosis in yeast. Curr Genet 23(3): 223-7.
","pubmedId":"8435851","doi":""},{"reference":"Tsai IJ, Bensasson D, Burt A, Koufopanou V. 2008. Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle. Proc Natl Acad Sci U S A 105(12): 4957-62.
","pubmedId":"18344325","doi":""},{"reference":"Vaughan-Martini A, Martini A. 2011. Saccharomyces Meyen ex Reess (1870). The Yeasts : 733-746.
","pubmedId":"","doi":"10.1016/B978-0-444-52149-1.00061-6"},{"reference":"van Tol N, Rolloos M, van Loon P, van der Zaal BJ. 2018. MeioSeed: a CellProfiler-based program to count fluorescent seeds for crossover frequency analysis in Arabidopsis thaliana. Plant Methods 14: 32.
","pubmedId":"29692862","doi":""},{"reference":"Vershon AK, Pierce M. 2000. Transcriptional regulation of meiosis in yeast. Curr Opin Cell Biol 12(3): 334-9.
","pubmedId":"10801467","doi":""},{"reference":"Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, et al., Yutani. 2019. Welcome to the Tidyverse. Journal of Open Source Software 4: 1686.
","pubmedId":"","doi":"10.21105/joss.01686"},{"reference":"Zhao H, Wang Q, Liu C, Shang Y, Wen F, Wang F, et al., Li W. 2018. A Role for the Respiratory Chain in Regulating Meiosis Initiation in Saccharomyces cerevisiae. Genetics 208(3): 1181-1194.
","pubmedId":"29301906","doi":""}],"title":"Sodium chloride stress inhibits Saccharomyces paradoxus meiosis
","reviews":[],"curatorReviews":[]},{"id":"615dea3a-b0b8-4627-8b3a-f83ae5208ce1","decision":"publish","abstract":"Meiosis is a common response to nutrient deprivation in yeasts. Our goal was to determine whether the yeast Saccharomyces paradoxus performed meiosis under other abiotic stress factors, specifically salt stress. We predicted that S. paradoxus meiosis would increase in the presence of salt because osmotic stress activates the IME1 transcription factor in its model yeast relative S. cerevisiae. Contrary to our prediction, the sporulation rate of S. paradoxus decreased as salinity increased. We hypothesize that this is due to salt inhibiting mitochondrial function, but more studies are needed to determine the cause.
","acknowledgements":"This work was conducted as part of Wheaton College’s Research Experience in Biology course series. We thank the Biological, Chemical, and Environmental Sciences department at Wheaton College, Massachusetts, for developing and maintaining this series. We also thank class members Julianne Coyne, Matt Fais, Syan Martin, and Juliana Michelon de Caux for conversations and input during development of this project.
","authors":[{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","dataCuration","investigation","methodology","writing_originalDraft","writing_reviewEditing"],"email":"germain_mima@wheatoncollege.edu","firstName":"Gemima","lastName":"Germain","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","formalAnalysis","investigation","methodology","writing_originalDraft","writing_reviewEditing"],"email":"lamphere_sylvia@wheatoncollege.edu","firstName":"Sylvia","lastName":"Lamphere","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["conceptualization","dataCuration","investigation","methodology","writing_reviewEditing"],"email":"molinari_ella@wheatoncollege.edu","firstName":"Ella","lastName":"Molinari","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["Wheaton College - Massachusetts, Norton, MA, US"],"departments":["Department of Biological, Chemical, and Environmental Sciences"],"credit":["dataCuration","formalAnalysis","fundingAcquisition","investigation","project","resources","supervision","validation","visualization","writing_originalDraft","writing_reviewEditing"],"email":"boynton_primrose@wheatoncollege.edu","firstName":"Primrose","lastName":"Boynton","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0003-0720-8966"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[{"description":"Sporulation data","doi":"10.22002/b0mff-2ex45","resourceType":"Dataset","name":"sporulation data.csv","url":"https://portal.micropublication.org/uploads/8ca9ea742921a9306878e9daed5ede44.csv"}],"funding":"This work was funded by the Biological, Chemical, and Environmental Sciences department at Wheaton College, Massachusetts. Publication fees were provided by Wheaton College’s Library, Technology, and Learning Committee.
","image":{"url":"https://portal.micropublication.org/uploads/d6f916b52b9bfe55c40583ef17d97470.jpeg"},"imageCaption":"Sporulation efficiency decreases as the amount of salt in the environment increases. A) Photograph of vegetative cells (1) and sporulated tetrads (2). B) Relationship between percent salt and proportion of cells sporulating. Small black points are individual sporulation observations; black lines connect values for the same S. paradoxus isolate. Large red points are averages for each category of salt percentage (0, 3%, or 6% sodium chloride).
","imageTitle":"S. paradoxus sporulation in different concentrations of salt
","methods":"We grew sixteen wild S. paradoxus isolates (Table 1) in each of three salt concentrations: no salt (0% NaCl), low salt (3% NaCl), and high salt (6% NaCl) (Table 2). All isolates had been isolated in 2017 or 2018 from soil or leaf litter next to oak trees in Nehmtener Forst, a mixed temperate forest in Nehmten, Schleswig-Holstein, Germany (Boynton et al. 2021). We inoculated each isolate from a colony on a petri dish into a single replicate of 1 mL of each medium type using a sterile stick and included uninoculated controls of each medium type to control for culture contamination. We incubated cultures at 26°C with 180 rpm (revolutions per minute) shaking. After seven days of incubation, we mixed each culture, pipetted 5 µl onto a microscope slide, and took a photograph under a compound microscope. We scored sporulation frequencies by drawing a transect on each photograph and counting sporulated and nonsporulated cells (Figure 1A), up to 100 total cells, along each transect. Spores are observed as four haploid cells inside an ascus formed during sporulation; non-spores remain in their vegetative state as single or budding cells (Figure 1A). Sporulation proportion is equal to the number of sporulated cells divided by 100 (the total number of counted cells).
We modeled proportions of cells sporulated as a function of salt concentration using a generalized mixed-effects model, modeling variance in sporulation using the binomial family with a logit link function; we varied slopes and intercepts for each S. paradoxus isolate to account for the repeated-measures design of our experiment. Marginal R2GLMM (i.e., proportion of variance in sporulation explained by salt concentration) (Nakagawa et al. 2017) was calculated using the theoretical method of determining binomial observation errors. Statistical analyses were done using R version 4.5.2 (R Core Team, 2025) and the tidyverse, lme4, AICcmodavg, and MuMIn packages (Bartón 2025, Bates et al. 2015, Mazerolle 2023, Wickham et al., 2019).
","reagents":"Table 1: Fungal strains
Species | Strain | Reference |
S. paradoxus | 5056 | Boynton et al. 2021 |
S. paradoxus | 5057 | Boynton et al. 2021 |
S. paradoxus | 5062 | Boynton et al. 2021 |
S. paradoxus | 5069 | Boynton et al. 2021 |
S. paradoxus | 5074 | Boynton et al. 2021 |
S. paradoxus | 5078 | Boynton et al. 2021 |
S. paradoxus | 5080 | Boynton et al. 2021 |
S. paradoxus | 5081 | Boynton et al. 2021 |
S. paradoxus | 5082 | Boynton et al. 2021 |
S. paradoxus | 5093 | Boynton et al. 2021 |
S. paradoxus | 5135 | Boynton et al. 2021 |
S. paradoxus | 5144 | Boynton et al. 2021 |
S. paradoxus | 5165 | Boynton et al. 2021 |
S. paradoxus | 5167 | Boynton et al. 2021 |
S. paradoxus | 5185 | Boynton et al. 2021 |
S. paradoxus | 5202 | Boynton et al. 2021 |
Table 2: Growth media
Medium | Composition |
YPD 0% salt | 10 g/L yeast extract, 20 g/L peptone, and 20 g/L dextrose |
YPD 3% salt | 10 g/L yeast extract, 20 g/L peptone, 20 g/L dextrose, and 30 g/L sodium chloride |
YPD 6% salt | 10 g/L yeast extract, 20 g/L peptone, 20 g/L dextrose, and 60 g/L sodium chloride |
Sex, the life cycle characterized by meiosis and mating, is facultative for most eukaryotes (Nieuwenhuis and James 2016, Speijer et al. 2015). Sexual life cycles have many costs compared to asexual reproduction, including reduced growth rates, metabolic investments in meiosis and mating, and costs of finding mates, but the machinery for sex is conserved over the eukaryotic tree of life because it is the primary mechanism for eukaryotic genetic recombination (Lehtonen et al. 2012, Speijer et al. 2015). The advantages of sexual recombination, especially in the face of changing environments, can explain its ubiquity (Becks and Agrawal 2012, Lively and Morran, 2014). Sex is favored in changing environments in experimental studies (Morran et al. 2011), and stressful environments often trigger meiosis in facultatively sexual eukaryotes (Ram and Hadany 2016, Schoustra et al. 2010). For example, the facultatively sexual model yeast Saccharomyces cerevisiae undergoes meiosis and produces haploid spores (sporulation) in laboratory environments when it is nutrient-starved (Mitchell 1994) (Figure 1A), but its wild sister species S. paradoxus, which has similar physiology, rarely undergoes meiosis in non-domesticated environments (Tsai et al. 2008, Vaughan-Martini and Martini 2011). We would like to understand if meiosis as a response to stress is generalizable to a non-nutrient-related stressor in S. paradoxus.
Similarly to nutrient stress, we hypothesized that salt (sodium chloride) stress might increase S. paradoxus meiosis frequency. In Saccharomyces, meiosis is induced by the transcription factor IME1 (Vershon and Pierce 2000). In S. cerevisiae, signaling proteins in the Hog1 osmotic stress response pathway, triggered by high environmental sodium chloride, bind to regulatory DNA associated with IME1, inducing transcription (Kahana-Edwin et al. 2013). Additionally, salt increases crossovers during meiosis in another model eukaryote, Arabidopsis thaliana (van Tol et al. 2018). We hypothesized that these molecular mechanisms are likely to translate to increased S. paradoxus sporulation as environmental sodium chloride concentrations increase. In this project, we tested whether increased sodium chloride concentrations increase rates of S. paradoxus meiosis.
Contrary to our expectation, salt decreased S. paradoxus sporulation in a laboratory experiment. We cultured sixteen S. paradoxus strains, previously isolated from a forest in Germany, in growth medium with each of three salt concentrations: 0%, 3%, and 6%. We chose these salt concentrations because they affected a different Saccharomyces phenotype, sensitivity to killer toxins, in a different study (Llorente et al. 1997). We grew cells in standard growth media supplemented with sodium chloride (Table 2) for seven days. This long incubation allowed S. paradoxus cells to deplete carbon and nitrogen in the environment and begin to undergo meiosis. We scored cultures for sporulation frequency from photographs taken under a microscope. Sporulation decreased from a mean of 90% sporulated cells with no added salt to a mean of 67% with 6% salt (Z = -8.5, p < 10-15, marginal R2GLMM = 0.46, Figure 1B).
We hypothesize that interactions among salt stress, mitochondrial function, and meiosis might explain why meiosis decreased as salt concentration increased. Mitochondrial function is necessary for activating the IME1 transcription factor, which induces meiosis (Treinin and Simchen 1992, Zhao et al. 2018). Osmotic stress has a variety of potential impacts on mitochondrial function: it is associated with changes in mitochondrial gene expression and accumulation of reactive oxygen species in mitochondria (Di Noia et al. 2023, Pastor et al. 2009). Some mutations in S. cerevisiae cells also result in decreased respiration with salt stress (Guaragnella et al. 2021), suggesting that salt can directly inhibit respiration. An alternative explanation for our observations is that salt stress increased mitosis rates while meiosis rates stayed the same, decreasing the relative number of sporulated cells we saw. We consider this unlikely because salt stress is associated with the Hog1 pathway, which halts the mitotic cell cycle (de Nadal and Posas 2022). Other impacts of salt on cell function, such as increasing glycerol accumulation or disrupting DNA replication, are more likely to increase meiotic frequency relative to mitosis (Cruz-León et al. 2022, Patel and Miller 1972), so we do not consider these responsible for the pattern we observed.
Our results suggest that, while sexual life cycles may be favored with nutrient stress, they are not favored in all stressful environments. This diversity in responses to stress could be a result of molecular interactions inside the cell, for example, in the mitochondrion; it also might reflect the diversity of ecological impacts of different stressors for individual yeast cells. The identities and importances of stressors S. paradoxus encounters in natural environments could explain its population-wide infrequent rate of meiosis (Tsai et al. 2008).
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