The cell morphological diversity of Saccharomycotina yeasts
Abstract
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.
- Authors:
-
[3];
[1]
- Vanderbilt University, Nashville, TN (United States)
- Westerdijk Fungal Biodiversity Institute, Utrecht (The Netherlands)
- University of Wisconsin-Madison, WI (United States)
- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Sponsoring Org.:
- 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
- OSTI Identifier:
- 2294038
- Grant/Contract Number:
- SC0018409; DEB-1442148; DEB-2110403; DEB-1442113; DEB-2110404; T34 GM136451
- Resource Type:
- Accepted Manuscript
- Journal Name:
- FEMS Yeast Research
- Additional Journal Information:
- Journal Volume: 24; Journal ID: ISSN 1567-1364
- Publisher:
- Federation of European Microbiological Societies - Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; evolutionary cell biology; cell size; cell shape; budding; hyphae; pseudohyphae; cell type; Saccharomycotina
Citation Formats
Chavez, Christina M., Groenewald, Marizeth, Hulfachor, Amanda B., Kpurubu, Gideon, Huerta, Rene, Hittinger, Chris Todd, and Rokas, Antonis. The cell morphological diversity of Saccharomycotina yeasts. United States: N. p., 2023.
Web. doi:10.1093/femsyr/foad055.
Chavez, Christina M., Groenewald, Marizeth, Hulfachor, Amanda B., Kpurubu, Gideon, Huerta, Rene, Hittinger, Chris Todd, & Rokas, Antonis. The cell morphological diversity of Saccharomycotina yeasts. United States. https://doi.org/10.1093/femsyr/foad055
Chavez, Christina M., Groenewald, Marizeth, Hulfachor, Amanda B., Kpurubu, Gideon, Huerta, Rene, Hittinger, Chris Todd, and Rokas, Antonis. Sat .
"The cell morphological diversity of Saccharomycotina yeasts". United States. https://doi.org/10.1093/femsyr/foad055. https://www.osti.gov/servlets/purl/2294038.
@article{osti_2294038,
title = {The cell morphological diversity of Saccharomycotina yeasts},
author = {Chavez, Christina M. and Groenewald, Marizeth and Hulfachor, Amanda B. and Kpurubu, Gideon and Huerta, Rene and Hittinger, Chris Todd and Rokas, Antonis},
abstractNote = {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.},
doi = {10.1093/femsyr/foad055},
journal = {FEMS Yeast Research},
number = ,
volume = 24,
place = {United States},
year = {Sat Dec 23 00:00:00 EST 2023},
month = {Sat Dec 23 00:00:00 EST 2023}
}
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Works referenced in this record:
Cell-size regulation in budding yeast does not depend on linear accumulation of Whi5
journal, June 2020
- Barber, Felix; Amir, Ariel; Murray, Andrew W.
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 25
Cell Polarization and Cytokinesis in Budding Yeast
journal, June 2012
- Bi, Erfei; Park, Hay-Oak
- Genetics, Vol. 191, Issue 2
Cell Polarity in Yeast
journal, October 2017
- Chiou, Jian-geng; Balasubramanian, Mohan K.; Lew, Daniel J.
- Annual Review of Cell and Developmental Biology, Vol. 33, Issue 1
The Genetic Landscape of a Cell
journal, January 2010
- Costanzo, M.; Baryshnikova, A.; Bellay, J.
- Science, Vol. 327, Issue 5964
The Regulation of Filamentous Growth in Yeast
journal, January 2012
- Cullen, Paul J.; Sprague, George F.
- Genetics, Vol. 190, Issue 1
Evolutionary dynamics in the fungal polarization network, a mechanistic perspective
journal, August 2017
- Diepeveen, Eveline T.; de la Cruz, Leila Iñigo; Laan, Liedewij
- Biophysical Reviews, Vol. 9, Issue 4
Patterns of Conservation and Diversification in the Fungal Polarization Network
journal, June 2018
- Diepeveen, Eveline T.; Gehrmann, Thies; Pourquié, Valérie
- Genome Biology and Evolution, Vol. 10, Issue 7
Gene loss and compensatory evolution promotes the emergence of morphological novelties in budding yeast
journal, April 2022
- Farkas, Zoltán; Kovács, Károly; Sarkadi, Zsuzsa
- Nature Ecology & Evolution, Vol. 6, Issue 6
The budding yeast life cycle: More complex than anticipated?
journal, December 2020
- Fischer, Gilles; Liti, Gianni; Llorente, Bertrand
- Yeast, Vol. 38, Issue 1
A genome-informed higher rank classification of the biotechnologically important fungal subphylum Saccharomycotina
journal, June 2023
- Groenewald, M.; Hittinger, C. T.; Bensch, K.
- Studies in Mycology, Vol. 105, Issue 1
Life cycle of the budding yeast Saccharomyces cerevisiae
journal, December 1988
- Herskowitz, I.
- Microbiological Reviews, Vol. 52, Issue 4
Genomics and the making of yeast biodiversity
journal, December 2015
- Hittinger, Chris Todd; Rokas, Antonis; Bai, Feng-Yan
- Current Opinion in Genetics & Development, Vol. 35
Large-Scale Survey of Intraspecific Fitness and Cell Morphology Variation in a Protoploid Yeast Species
journal, April 2016
- Jung, Paul P.; Sigwalt, Anastasie; Ohnuki, Shinsuke
- G3 Genes|Genomes|Genetics, Vol. 6, Issue 4
Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution
journal, August 2019
- Krassowski, Tadeusz; Kominek, Jacek; Shen, Xing-Xing
- Current Biology, Vol. 29, Issue 15
Alloascoidea hylecoetigen. nov., comb. nov.,Alloascoidea africanacomb. nov.,Ascoidea tardasp. nov., andNadsonia starkeyi-henriciicomb. nov., new members of theSaccharomycotina(Ascomycota)
journal, April 2013
- Kurtzman, Cletus P.; Robnett, Christie J.
- FEMS Yeast Research, Vol. 13, Issue 5
Evolutionary adaptation after crippling cell polarization follows reproducible trajectories
journal, October 2015
- Laan, Liedewij; Koschwanez, John H.; Murray, Andrew W.
- eLife, Vol. 4
A genome-scale phylogeny of the kingdom Fungi
journal, April 2021
- Li, Yuanning; Steenwyk, Jacob L.; Chang, Ying
- Current Biology, Vol. 31, Issue 8
Evolutionary cell biology: Two origins, one objective: Fig. 1.
journal, November 2014
- Lynch, Michael; Field, Mark C.; Goodson, Holly V.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 48
Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts
journal, July 2014
- Nagy, László G.; Ohm, Robin A.; Kovács, Gábor M.
- Nature Communications, Vol. 5, Issue 1
Factors driving metabolic diversity in the budding yeast subphylum
journal, March 2018
- Opulente, Dana A.; Rollinson, Emily J.; Bernick-Roehr, Cleome
- BMC Biology, Vol. 16, Issue 1
Different effectors of dimorphism in Yarrowia lipolytica
journal, December 2002
- Ruiz-Herrera, José; Sentandreu, Rafael
- Archives of Microbiology, Vol. 178, Issue 6, p. 477-483
The Pathogenic Yeast Candida parapsilosis Forms Pseudohyphae through Different Signaling Pathways Depending on the Available Carbon Source
journal, June 2022
- Rupert, Christopher B.; Rusche, Laura N.
- mSphere, Vol. 7, Issue 3
A new species of blastobotrys: Blastobotrys navarrensis sp. nov. (Hyphomycetes)
journal, January 1978
- Sesma, Bego�a; Ramirez, C.
- Mycopathologia, Vol. 63, Issue 1
Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum
journal, November 2018
- Shen, Xing-Xing; Opulente, Dana A.; Kominek, Jacek
- Cell, Vol. 175, Issue 6
Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast
journal, May 2013
- Skelly, D. A.; Merrihew, G. E.; Riffle, M.
- Genome Research, Vol. 23, Issue 9
Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts
journal, May 2019
- Steenwyk, Jacob L.; Opulente, Dana A.; Kominek, Jacek
- PLOS Biology, Vol. 17, Issue 5
An orthologous gene coevolution network provides insight into eukaryotic cellular and genomic structure and function
journal, May 2022
- Steenwyk, Jacob L.; Phillips, Megan A.; Yang, Feng
- Science Advances, Vol. 8, Issue 18
Cellular quiescence in budding yeast
journal, January 2021
- Sun, Siyu; Gresham, David
- Yeast, Vol. 38, Issue 1
Blastobotrys nivea gen.nov., sp.nov.
journal, January 1967
- Klopotek, Agnes
- Archiv f�r Mikrobiologie, Vol. 58, Issue 1
Single-cell phenomics reveals intra-species variation of phenotypic noise in yeast
journal, January 2013
- Yvert, Gaël; Ohnuki, Shinsuke; Nogami, Satoru
- BMC Systems Biology, Vol. 7, Issue 1