Mosaic fungal individuals have the potential to evolve within a single generation

Maura G. Tyrrell; Diane C. Peabody; Robert B. Peabody; Magdalena James-Pederson; Rachel G. Hirst; Elisha Allan-Perkins; Heather Bickford; Amy Shafrir; Robert J. Doiron; Amber C. Churchill; Juan Carlos Ramirez-Tapia; Benjamin Seidel; Lynes Torres; Kathryn Fallavollita; Thomas Hernon; Lindsay Wiswell; Sarah Wilson; Erica Mondo; Kathleen Salisbury; Carrie Peabody; Patrick Cabral; Lauren Presti; Kelsey McKenna-Hoffman; Michele Flannery; Kaitlin Daly; Darius Haghighat; Danie Lukason

doi:10.1038/s41598-020-74679-5

Mosaic fungal individuals have the potential to evolve within a single generation

Maura G. Tyrrell
, Diane C. Peabody
, Robert B. Peabody
, Magdalena James-Pederson
, Rachel G. Hirst
, Elisha Allan-Perkins
, Heather Bickford
, Amy Shafrir
, Robert J. Doiron
, Amber C. Churchill
, Juan Carlos Ramirez-Tapia
, Benjamin Seidel
, Lynes Torres
, Kathryn Fallavollita
, Thomas Hernon
, Lindsay Wiswell
, Sarah Wilson
, Erica Mondo
, Kathleen Salisbury
, Carrie Peabody

Patrick Cabral, Lauren Presti, Kelsey McKenna-Hoffman, Michele Flannery, Kaitlin Daly, Darius Haghighat, Danie Lukason

Western Sydney University

Research output: Contribution to journal › Article › peer-review

6 Citations (Scopus)

Abstract

Although cells of mushroom-producing fungi typically contain paired haploid nuclei (n + n), most Armillaria gallica vegetative cells are uninucleate. As vegetative nuclei are produced by fusions of paired haploid nuclei, they are thought to be diploid (2n). Here we report finding haploid vegetative nuclei in A. gallica at multiple sites in southeastern Massachusetts, USA. Sequencing multiple clones of a single-copy gene isolated from single hyphal filaments revealed nuclear heterogeneity both among and within hyphae. Cytoplasmic bridges connected hyphae in field-collected and cultured samples, and we propose nuclear migration through bridges maintains this nuclear heterogeneity. Growth studies demonstrate among- and within-hypha phenotypic variation for growth in response to gallic acid, a plant-produced antifungal compound. The existence of both genetic and phenotypic variation within vegetative hyphae suggests that fungal individuals have the potential to evolve within a single generation in response to environmental variation over time and space.

Original language	English
Article number	17625
Number of pages	13
Journal	Scientific Reports
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41598-020-74679-5
Publication status	Published - 1 Dec 2020

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© 2020, The Author(s).

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Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. Te images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Â© Te Author(s) 2020.

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10.1038/s41598-020-74679-5

Cite this

Tyrrell, M. G., Peabody, D. C., Peabody, R. B., James-Pederson, M., Hirst, R. G., Allan-Perkins, E., Bickford, H., Shafrir, A., Doiron, R. J., Churchill, A. C., Ramirez-Tapia, J. C., Seidel, B., Torres, L., Fallavollita, K., Hernon, T., Wiswell, L., Wilson, S., Mondo, E., Salisbury, K., ... Lukason, D. (2020). Mosaic fungal individuals have the potential to evolve within a single generation. Scientific Reports, 10(1), Article 17625. https://doi.org/10.1038/s41598-020-74679-5

@article{c64dc1a3637349219fda6394db368d6e,

title = "Mosaic fungal individuals have the potential to evolve within a single generation",

abstract = "Although cells of mushroom-producing fungi typically contain paired haploid nuclei (n + n), most Armillaria gallica vegetative cells are uninucleate. As vegetative nuclei are produced by fusions of paired haploid nuclei, they are thought to be diploid (2n). Here we report finding haploid vegetative nuclei in A. gallica at multiple sites in southeastern Massachusetts, USA. Sequencing multiple clones of a single-copy gene isolated from single hyphal filaments revealed nuclear heterogeneity both among and within hyphae. Cytoplasmic bridges connected hyphae in field-collected and cultured samples, and we propose nuclear migration through bridges maintains this nuclear heterogeneity. Growth studies demonstrate among- and within-hypha phenotypic variation for growth in response to gallic acid, a plant-produced antifungal compound. The existence of both genetic and phenotypic variation within vegetative hyphae suggests that fungal individuals have the potential to evolve within a single generation in response to environmental variation over time and space.",

author = "Tyrrell, \{Maura G.\} and Peabody, \{Diane C.\} and Peabody, \{Robert B.\} and Magdalena James-Pederson and Hirst, \{Rachel G.\} and Elisha Allan-Perkins and Heather Bickford and Amy Shafrir and Doiron, \{Robert J.\} and Churchill, \{Amber C.\} and Ramirez-Tapia, \{Juan Carlos\} and Benjamin Seidel and Lynes Torres and Kathryn Fallavollita and Thomas Hernon and Lindsay Wiswell and Sarah Wilson and Erica Mondo and Kathleen Salisbury and Carrie Peabody and Patrick Cabral and Lauren Presti and Kelsey McKenna-Hoffman and Michele Flannery and Kaitlin Daly and Darius Haghighat and Danie Lukason",

note = "Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = dec,

day = "1",

doi = "10.1038/s41598-020-74679-5",

language = "English",

volume = "10",

journal = "Scientific Reports",

issn = "2045-2322",

publisher = "Nature Research",

number = "1",

}

Tyrrell, MG, Peabody, DC, Peabody, RB, James-Pederson, M, Hirst, RG, Allan-Perkins, E, Bickford, H, Shafrir, A, Doiron, RJ, Churchill, AC, Ramirez-Tapia, JC, Seidel, B, Torres, L, Fallavollita, K, Hernon, T, Wiswell, L, Wilson, S, Mondo, E, Salisbury, K, Peabody, C, Cabral, P, Presti, L, McKenna-Hoffman, K, Flannery, M, Daly, K, Haghighat, D & Lukason, D 2020, 'Mosaic fungal individuals have the potential to evolve within a single generation', Scientific Reports, vol. 10, no. 1, 17625. https://doi.org/10.1038/s41598-020-74679-5

TY - JOUR

T1 - Mosaic fungal individuals have the potential to evolve within a single generation

AU - Tyrrell, Maura G.

AU - Peabody, Diane C.

AU - Peabody, Robert B.

AU - James-Pederson, Magdalena

AU - Hirst, Rachel G.

AU - Allan-Perkins, Elisha

AU - Bickford, Heather

AU - Shafrir, Amy

AU - Doiron, Robert J.

AU - Churchill, Amber C.

AU - Ramirez-Tapia, Juan Carlos

AU - Seidel, Benjamin

AU - Torres, Lynes

AU - Fallavollita, Kathryn

AU - Hernon, Thomas

AU - Wiswell, Lindsay

AU - Wilson, Sarah

AU - Mondo, Erica

AU - Salisbury, Kathleen

AU - Peabody, Carrie

AU - Cabral, Patrick

AU - Presti, Lauren

AU - McKenna-Hoffman, Kelsey

AU - Flannery, Michele

AU - Daly, Kaitlin

AU - Haghighat, Darius

AU - Lukason, Danie

PY - 2020/12/1

Y1 - 2020/12/1

N2 - Although cells of mushroom-producing fungi typically contain paired haploid nuclei (n + n), most Armillaria gallica vegetative cells are uninucleate. As vegetative nuclei are produced by fusions of paired haploid nuclei, they are thought to be diploid (2n). Here we report finding haploid vegetative nuclei in A. gallica at multiple sites in southeastern Massachusetts, USA. Sequencing multiple clones of a single-copy gene isolated from single hyphal filaments revealed nuclear heterogeneity both among and within hyphae. Cytoplasmic bridges connected hyphae in field-collected and cultured samples, and we propose nuclear migration through bridges maintains this nuclear heterogeneity. Growth studies demonstrate among- and within-hypha phenotypic variation for growth in response to gallic acid, a plant-produced antifungal compound. The existence of both genetic and phenotypic variation within vegetative hyphae suggests that fungal individuals have the potential to evolve within a single generation in response to environmental variation over time and space.

AB - Although cells of mushroom-producing fungi typically contain paired haploid nuclei (n + n), most Armillaria gallica vegetative cells are uninucleate. As vegetative nuclei are produced by fusions of paired haploid nuclei, they are thought to be diploid (2n). Here we report finding haploid vegetative nuclei in A. gallica at multiple sites in southeastern Massachusetts, USA. Sequencing multiple clones of a single-copy gene isolated from single hyphal filaments revealed nuclear heterogeneity both among and within hyphae. Cytoplasmic bridges connected hyphae in field-collected and cultured samples, and we propose nuclear migration through bridges maintains this nuclear heterogeneity. Growth studies demonstrate among- and within-hypha phenotypic variation for growth in response to gallic acid, a plant-produced antifungal compound. The existence of both genetic and phenotypic variation within vegetative hyphae suggests that fungal individuals have the potential to evolve within a single generation in response to environmental variation over time and space.

UR - https://hdl.handle.net/1959.7/uws:64996

U2 - 10.1038/s41598-020-74679-5

DO - 10.1038/s41598-020-74679-5

M3 - Article

SN - 2045-2322

VL - 10

JO - Scientific Reports

JF - Scientific Reports

IS - 1

M1 - 17625

ER -

Mosaic fungal individuals have the potential to evolve within a single generation

Abstract

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