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. 2020 Oct 19;10(1):17625.
doi: 10.1038/s41598-020-74679-5.

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

Affiliations

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

Maura G Tyrrell et al. Sci Rep. .

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.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
DAPI-DNA values for A. gallica nuclei show spores and vegetative nuclei are haploid, in contrast to the diploid nuclei from prophase I basidia. (a). Field-collected prophase I basidia (N = 30). (b). Field-collected spores (N = 30). (c). Field-collected vegetative stages (rhizomorphs and soil mycelia, N = 50). (d). Cultured rhizomorphs (N = 202). Shapiro–Wilk W goodness-of-fit test: Ho = normal distribution; small P-values reject Ho.
Figure 2
Figure 2
EF1α x HaeIII RFLP patterns for Raynham differ for spores and rhizomorphs. Spores have either allele E1 (lanes 2, 4, 6, 8–11) or allele E2 (lanes 3, 5, 7). Rhizomorphs have both alleles (pattern E1E2, lanes 13–22). Lanes 1, 12, and 23 are markers.
Figure 3
Figure 3
Cytoplasmic bridges (thin arrows) connect one hypha (thick arrow) to 3 nearby hyphae in a rhizomorph fixed in 95% ethanol upon collection from the field. Bar = 10 μM.
Figure 4
Figure 4
DAPI staining shows nuclei (arrows) in cytoplasmic bridges between hyphae grown from rhizomorph hyphal filament tip isolates. (a) Nucleus within a bridge. (b) Nucleus entering or exiting a bridge. Bars = 10 μM.
Figure 5
Figure 5
Reaction norm lines show that spore cell lines and rhizomorph hyphal filament lines from single genetic individuals from Bridgewater and Raynham, MA, differed for both growth and phenotypic plasticity. All ANOVA P-values were significant (P < 0.0001) for line effects (growth differences among lines), treatment effects (effect of gallic acid concentration on growth), and line × treatment effects (phenotypic plasticity for spore and rhizomorph lines). F-values and degrees of freedom are listed in Supplementary Table S6. N = 1571 culture plates, 1547 with independent environmental histories (Supplementary methods).
Figure 6
Figure 6
Haploid Genetic Mosaicism is exemplified in two rhizomorph hyphal filament lines (09r27 and 09r50) isolated from the Raynham genet. The mycelium containing hyphae with these haplotypes exhibits both within-line and among-line nuclear heterogeneity.
Figure 7
Figure 7
In this model, Haploid Genetic Mosaicism is maintained by nuclear exchange across cytoplasmic bridges connecting rhizomorph hyphal filament tips.
Figure 8
Figure 8
The samples collected from all seven sites in southeastern Massachusetts, USA, were shown by somatic incompatibility tests to represent different genets (individuals). (This map was created using ArcMap 10.4 with data from the Massachusetts Bureau of Geographic Information).

References

    1. Raper JR. Genetics of Sexuality in Higher Fungi. New York: The Ronald Press Company; 1966.
    1. Gladfelter A, Berman J. Dancing genomes: Fungal nuclear positioning. Nat. Rev. Microbiol. 2009;7:875–886. doi: 10.1038/nrmicro2249. - DOI - PMC - PubMed
    1. Otto SP, Gerstein AC. The evolution of haploidy and diploidy. Curr. Biol. 2008;18:R1121–R1124. doi: 10.1016/j.cub.2008.09.039. - DOI - PubMed
    1. Korhonen K. The origin of clamped and clampless basidia in Armillariella ostoyae. Karstenia. 1980;20:23–27. doi: 10.29203/ka.1980.193. - DOI
    1. Grillo R, Korhonen K, Tirro A. The origin of dikaryotic hyphae in fruit bodies of Armillaria borealis and A. tabescens developed in pure culture. In: Johansson M, Stenlid J, editors. Proceedings 8th International Conference on Root and Butt Rots. Uppsala: Swedish University of Agricultural Sciences; 1994. pp. 504–511.

Publication types

Supplementary concepts