The cell morphological diversity of Saccharomycotina yeasts

Chavez, Christina M.; Groenewald, Marizeth; Hulfachor, Amanda B.; Kpurubu, Gideon; Huerta, Rene; Hittinger, Chris Todd; Rokas, Antonis

doi:10.1093/femsyr/foad055

The cell morphological diversity of Saccharomycotina yeasts

Journal Article · Fri Dec 22 23:00:00 EST 2023 · FEMS Yeast Research

DOI:https://doi.org/10.1093/femsyr/foad055· OSTI ID:2294038

Chavez, Christina M. ^[1]; Groenewald, Marizeth ^[2]; Hulfachor, Amanda B. ^[3]; Kpurubu, Gideon ^[4]; Huerta, Rene ^[4]; ^[3]; ^[4]

Vanderbilt University, Nashville, TN (United States); Vanderbilt University Department of Biological Sciences
Westerdijk Fungal Biodiversity Institute, Utrecht (The Netherlands)
University of Wisconsin-Madison, WI (United States)
Vanderbilt University, Nashville, TN (United States)

The ~1 200 known species in subphylum Saccharomycotina are a highly diverse clade of unicellular fungi. During its lifecycle, a typical yeast exhibits multiple cell types with various morphologies; these morphologies vary across Saccharomycotina species. Here, we synthesize the evolutionary dimensions of variation in cellular morphology of yeasts across the subphylum, focusing on variation in cell shape, cell size, type of budding, and filament production. Examination of 332 representative species across the subphylum revealed that the most common budding cell shapes are ovoid, spherical, and ellipsoidal, and that their average length and width is 5.6 µm and 3.6 µm, respectively. 58.4% of yeast species examined can produce filamentous cells, and 87.3% of species reproduce asexually by multilateral budding, which does not require utilization of cell polarity for mitosis. Interestingly, ~1.8% of species examined have not been observed to produce budding cells, but rather only produce filaments of septate hyphae and/or pseudohyphae. 76.9% of yeast species examined have sexual cycle descriptions, with most producing one to four ascospores that are most commonly hat-shaped (37.4%). Systematic description of yeast cellular morphological diversity and reconstruction of its evolution promises to enrich our understanding of the evolutionary cell biology of this major fungal lineage.

View Accepted Manuscript (DOE)

Research Organization:: Great Lakes Bioenergy Research Center, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Institute of General Medical Sciences of the National Institutes of Health

Grant/Contract Number:: SC0018409

OSTI ID:: 2294038

Journal Information:: FEMS Yeast Research, Journal Name: FEMS Yeast Research Vol. 24; ISSN 1567-1364

Publisher:: Federation of European Microbiological Societies - Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (31)

The budding yeast life cycle: More complex than anticipated? Fischer, Gilles; Liti, Gianni; Llorente, Bertrand Yeast, Vol. 38, Issue 1 https://doi.org/10.1002/yea.3533	journal	December 2020
Cellular quiescence in budding yeast Sun, Siyu; Gresham, David Yeast, Vol. 38, Issue 1 https://doi.org/10.1002/yea.3545	journal	January 2021
A new species of blastobotrys: Blastobotrys navarrensis sp. nov. (Hyphomycetes) Sesma, Bego�a; Ramirez, C. Mycopathologia, Vol. 63, Issue 1 https://doi.org/10.1007/BF00473158	journal	January 1978
Blastobotrys nivea gen.nov., sp.nov. Klopotek, Agnes Archiv f�r Mikrobiologie, Vol. 58, Issue 1 https://doi.org/10.1007/BF00691172	journal	January 1967
Different effectors of dimorphism in Yarrowia lipolytica Ruiz-Herrera, José; Sentandreu, Rafael Archives of Microbiology, Vol. 178, Issue 6, p. 477-483 https://doi.org/10.1007/s00203-002-0478-3	journal	December 2002
Evolutionary dynamics in the fungal polarization network, a mechanistic perspective Diepeveen, Eveline T.; de la Cruz, Leila Iñigo; Laan, Liedewij Biophysical Reviews, Vol. 9, Issue 4 https://doi.org/10.1007/s12551-017-0286-2	journal	August 2017
Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum Shen, Xing-Xing; Opulente, Dana A.; Kominek, Jacek Cell, Vol. 175, Issue 6 https://doi.org/10.1016/j.cell.2018.10.023	journal	November 2018
Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution Krassowski, Tadeusz; Kominek, Jacek; Shen, Xing-Xing Current Biology, Vol. 29, Issue 15 https://doi.org/10.1016/j.cub.2019.06.056	journal	August 2019
A genome-scale phylogeny of the kingdom Fungi Li, Yuanning; Steenwyk, Jacob L.; Chang, Ying Current Biology, Vol. 31, Issue 8 https://doi.org/10.1016/j.cub.2021.01.074	journal	April 2021
Genomics and the making of yeast biodiversity Hittinger, Chris Todd; Rokas, Antonis; Bai, Feng-Yan Current Opinion in Genetics & Development, Vol. 35 https://doi.org/10.1016/j.gde.2015.10.008	journal	December 2015
Reproductive isolation in Saccharomyces Greig, D. Heredity, Vol. 102, Issue 1 https://doi.org/10.1038/hdy.2008.73	journal	July 2008
Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts Nagy, László G.; Ohm, Robin A.; Kovács, Gábor M. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5471	journal	July 2014
Gene loss and compensatory evolution promotes the emergence of morphological novelties in budding yeast Farkas, Zoltán; Kovács, Károly; Sarkadi, Zsuzsa Nature Ecology & Evolution, Vol. 6, Issue 6 https://doi.org/10.1038/s41559-022-01730-1	journal	April 2022
Evolutionary cell biology: Two origins, one objective: Fig. 1. Lynch, Michael; Field, Mark C.; Goodson, Holly V. Proceedings of the National Academy of Sciences, Vol. 111, Issue 48 https://doi.org/10.1073/pnas.1415861111	journal	November 2014
Cell-size regulation in budding yeast does not depend on linear accumulation of Whi5 Barber, Felix; Amir, Ariel; Murray, Andrew W. Proceedings of the National Academy of Sciences, Vol. 117, Issue 25 https://doi.org/10.1073/pnas.2001255117	journal	June 2020
Patterns of Conservation and Diversification in the Fungal Polarization Network Diepeveen, Eveline T.; Gehrmann, Thies; Pourquié, Valérie Genome Biology and Evolution, Vol. 10, Issue 7 https://doi.org/10.1093/gbe/evy121	journal	June 2018
Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast Skelly, D. A.; Merrihew, G. E.; Riffle, M. Genome Research, Vol. 23, Issue 9 https://doi.org/10.1101/gr.155762.113	journal	May 2013
Alloascoidea hylecoetigen. nov., comb. nov.,Alloascoidea africanacomb. nov.,Ascoidea tardasp. nov., andNadsonia starkeyi-henriciicomb. nov., new members of theSaccharomycotina(Ascomycota) Kurtzman, Cletus P.; Robnett, Christie J. FEMS Yeast Research, Vol. 13, Issue 5 https://doi.org/10.1111/1567-1364.12044	journal	April 2013
An orthologous gene coevolution network provides insight into eukaryotic cellular and genomic structure and function Steenwyk, Jacob L.; Phillips, Megan A.; Yang, Feng Science Advances, Vol. 8, Issue 18 https://doi.org/10.1126/sciadv.abn0105	journal	May 2022
The Genetic Landscape of a Cell Costanzo, M.; Baryshnikova, A.; Bellay, J. Science, Vol. 327, Issue 5964 https://doi.org/10.1126/science.1180823	journal	January 2010
Life cycle of the budding yeast Saccharomyces cerevisiae Herskowitz, I. Microbiological Reviews, Vol. 52, Issue 4 https://doi.org/10.1128/mr.52.4.536-553.1988	journal	December 1988
The Pathogenic Yeast Candida parapsilosis Forms Pseudohyphae through Different Signaling Pathways Depending on the Available Carbon Source Rupert, Christopher B.; Rusche, Laura N. mSphere, Vol. 7, Issue 3 https://doi.org/10.1128/msphere.00029-22	journal	June 2022
Cell Polarity in Yeast Chiou, Jian-geng; Balasubramanian, Mohan K.; Lew, Daniel J. Annual Review of Cell and Developmental Biology, Vol. 33, Issue 1 https://doi.org/10.1146/annurev-cellbio-100616-060856	journal	October 2017
Single-cell phenomics reveals intra-species variation of phenotypic noise in yeast Yvert, Gaël; Ohnuki, Shinsuke; Nogami, Satoru BMC Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1752-0509-7-54	journal	January 2013
Factors driving metabolic diversity in the budding yeast subphylum Opulente, Dana A.; Rollinson, Emily J.; Bernick-Roehr, Cleome BMC Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12915-018-0498-3	journal	March 2018
Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts Steenwyk, Jacob L.; Opulente, Dana A.; Kominek, Jacek PLOS Biology, Vol. 17, Issue 5 https://doi.org/10.1371/journal.pbio.3000255	journal	May 2019
Large-Scale Survey of Intraspecific Fitness and Cell Morphology Variation in a Protoploid Yeast Species Jung, Paul P.; Sigwalt, Anastasie; Ohnuki, Shinsuke G3 Genes\|Genomes\|Genetics, Vol. 6, Issue 4 https://doi.org/10.1534/g3.115.026682	journal	April 2016
The Regulation of Filamentous Growth in Yeast Cullen, Paul J.; Sprague, George F. Genetics, Vol. 190, Issue 1 https://doi.org/10.1534/genetics.111.127456	journal	January 2012
Cell Polarization and Cytokinesis in Budding Yeast Bi, Erfei; Park, Hay-Oak Genetics, Vol. 191, Issue 2 https://doi.org/10.1534/genetics.111.132886	journal	June 2012
A genome-informed higher rank classification of the biotechnologically important fungal subphylum Saccharomycotina Groenewald, M.; Hittinger, C. T.; Bensch, K. Studies in Mycology, Vol. 105, Issue 1 https://doi.org/10.3114/sim.2023.105.01	journal	June 2023
Evolutionary adaptation after crippling cell polarization follows reproducible trajectories Laan, Liedewij; Koschwanez, John H.; Murray, Andrew W. eLife, Vol. 4 https://doi.org/10.7554/eLife.09638	journal	October 2015