The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.
Invasive Californian death caps develop mushrooms unisexually and bisexually
Open accessPublished version of a preprint
Abstract
Canonical sexual reproduction among basidiomycete fungi involves the fusion of two haploid individuals of different mating types, resulting in a heterokaryotic mycelial body made up of genetically different nuclei. Using population genomics data and experiments, we discover mushrooms of the invasive and deadly Amanita phalloides can also be homokaryotic; evidence of sexual reproduction by single, unmated individuals. In California, genotypes of homokaryotic mushrooms are also found in heterokaryotic mushrooms, implying nuclei of homokaryotic mycelia are also involved in outcrossing. We find death cap mating is controlled by a single mating type locus, but the development of homokaryotic mushrooms appears to bypass mating type gene control. Ultimately, sporulation is enabled by nuclei able to reproduce alone as well as with others, and nuclei competent for both unisexuality and bisexuality have persisted in invaded habitats for at least 17 but potentially as long as 30 years. The diverse reproductive strategies of invasive death caps are likely facilitating its rapid spread, suggesting a profound similarity between plant, animal and fungal invasions.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
Protein complex prediction with AlphaFold-Multimer
Evans, R., O’Neill, M., Pritzel, A., Antropova, N., Senior, A., Green, T., Žídek, A., Bates, R., Blackwell, S., Yim, J., et al. (2021) · doi:10.1101/2021.10.04.463034 · Cited by 3,808
The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update
Afgan, E., Baker, D., Batut, B., van den Beek, M., Bouvier, D., Čech, M., Chilton, J., Clements, D., Coraor, N., Grüning, B. A., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky379 · Cited by 3,662
Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak
Fraser, J. A., Giles, S. S., Wenink, E. C., Geunes-Boyer, S. G., Wright, J. R., Diezmann, S., Allen, A., Stajich, J. E., Dietrich, F. S., Perfect, J. R., et al. (2005) · Nature · doi:10.1038/nature04220 · Cited by 499
Flagged first, then by citations
Research works printed but not linked: 85
- Gladieux, P. et al. The population biology of fungal invasions. Mol. Ecol. 24, 1969–1986 (2015). · DOI
- Pringle, A. & Vellinga, E. C. Last chance to know? Using literature to explore the biogeography and invasion biology of the death cap mushroom Amanita phalloides (Vaill. ex Fr.:Fr.) link. Biol. Invasions 8, 1131–1144 (2006). · DOI
- Pringle, A., Adams, R. I., Cross, H. B. & Bruns, T. D. The ectomycorrhizal fungus Amanita phalloides was introduced and is expanding its range on the west coast of North America. Mol. Ecol. 18, 813–833 (2009). · DOI
- Vo, K. T. et al. Amanita phalloides mushroom poisonings—Northern California, December 2016. MMWR Morb. Mortal. Wkly. Rep. 66, 549–553 (2017). · DOI
- Baker, H. G. Self-compatibility and establishment after ‘long-distance’ dispersal. Evolution 9, 347–349 (1955).
- Pannell, J. R. et al. The scope of Baker’s law. N. Phytol. 208, 656–667 (2015). · DOI
- Coelho, M. A., Bakkeren, G., Sun, S., Hood, M. E. & Giraud, T. Fungal sex: the Basidiomycota. Microbiol. Spectr. 5, 147–175 (2017). · DOI
- Heitman, J., Kronstad, J. W., Taylor, J. W. & Casselton, L. A. Sex in Fungi: Molecular Determination And Evolutionary Implications (ASM Press, 2007). · DOI
- Lin, X., Hull, C. M. & Heitman, J. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434, 1017–1021 (2005). · DOI
- Roach, K. C., Feretzaki, M., Sun, S. & Heitman, J. in Advances in Genetics Vol. 5, Ch. 5 (eds. Friedmann, T., Dunlap, J. C. & Goodwin, S. F.) 255–305 (Academic Press, 2014). · DOI
- Wilson, A. M. et al. Homothallism: an umbrella term for describing diverse sexual behaviours. IMA Fungus 6, 207–214 (2015). · DOI
- Leslie, J. F. & Leonard, T. J. Monokaryotic fruiting in Schizophyllum commune: survey of a population from Wisconsin. Am. Midl. Nat. 103, 367–374 (1980). · DOI
- Murata, Y., Fujii, M., Zolan, M. E. & Kamada, T. Molecular analysis of pcc1, a gene that leads to A-regulated sexual morphogenesis in Coprinus cinereus. Genetics 149, 1753–1761 (1998). · DOI
- Stahl, U. & Esser, K. Genetics of fruit body production in higher basidiomycetes. Mol. Gen. Genet. 148, 183–197 (1976). · DOI
- Wang, Y.-W. & Ané, C. C. KIMGENS: a novel method to estimate kinship in organisms with mixed haploid diploid genetic systems robust to population structure. Bioinformatics 38, 3044–3050 (2022). · DOI
- Horton, T. R. The number of nuclei in basidiospores of 63 species of ectomycorrhizal Homobasidiomycetes. Mycologia 98, 233–238 (2006). · DOI
- Lewis, C. E. The basidium of Amanita bisporigera. Bot. Gaz. 41, 348–352 (1906). · DOI
- James, T. Y., Srivilai, P., Kües, U. & Vilgalys, R. Evolution of the bipolar mating system of the mushroom Coprinellus disseminatus from Its tetrapolar ancestors involves loss of mating-type-specific pheromone receptor function. Genetics 172, 1877–1891 (2006). · DOI
- van Diepen, L. T. A., Olson, Å., Ihrmark, K., Stenlid, J. & James, T. Y. Extensive trans-specific polymorphism at the mating type locus of the root decay fungus Heterobasidion. Mol. Biol. Evol. 30, 2286–2301 (2013). · DOI
- Peris, D. et al. Large-scale fungal strain sequencing unravels the molecular diversity in mating loci maintained by long-term balancing selection. PLoS Genet. 18, e1010097 (2022). · DOI
- David-Palma, M., Sampaio, J. P. & Gonçalves, P. Genetic dissection of sexual reproduction in a primary homothallic basidiomycete. PLOS Genet. 12, e1006110 (2016). · DOI
- Passer, A. R. et al. Obligate sexual reproduction of a homothallic fungus closely related to the Cryptococcus pathogenic species complex. eLife 11, e79114 (2022). · DOI
- Brown, A. J. & Casselton, L. A. Mating in mushrooms: increasing the chances but prolonging the affair. Trends Genet. 17, 393–400 (2001). · DOI
- Yadav, V., Sun, S. & Heitman, J. Uniparental nuclear inheritance following bisexual mating in fungi. eLife 10, e66234 (2021). · DOI
- Banham, A. H. et al. An N-terminal dimerization domain permits homeodomain proteins to choose compatible partners and initiate sexual development in the mushroom Coprinus cinereus. Plant Cell 7, 773–783 (1995).
- Kües, U. et al. Two classes of homeodomain proteins specify the multiple a mating types of the mushroom Coprinus cinereus. Plant Cell 6, 1467–1475 (1994).
- Taylor, J. W. et al. Assembling the Tree of Life (eds Cracraft, J. & Donoghue, M. J.) 171–194 (Oxford University Press, 2004).
- Johannesson, H. & Stenlid, J. Nuclear reassortment between vegetative mycelia in natural populations of the basidiomycete Heterobasidion annosum. Fungal Genet. Biol. 41, 563–570 (2004). · DOI
- Blakeslee, A. F. Sexual reproduction in the Mucorineae. Proc. Am. Acad. Arts Sci. 40, 205–319 (1904). · DOI
- Lamoure, D. Indices of useful informations for intercompatibility tests in Basidiomycetes V. - Agaricales sensu lato. Cryptogam. Mycol. 10, 41–80 (1989). · DOI
- Wilson, A. M. et al. Doing it alone: unisexual reproduction in filamentous ascomycete fungi. Fungal Biol. Rev. 35, 1–13 (2021). · DOI
- Orban, A., Hennicke, F. & Rühl, M. Volatilomes of Cyclocybe aegerita during different stages of monokaryotic and dikaryotic fruiting. Biol. Chem. 401, 995–1004 (2020). · DOI
- Elders, H. & Hennicke, F. The Pacific tree-parasitic fungus Cyclocybe parasitica exhibits monokaryotic fruiting, showing phenotypes known from bracket fungi and from Cyclocybe aegerita. J. Fungus 7, 394 (2021). · DOI
- Orban, A., Weber, A., Herzog, R., Hennicke, F. & Rühl, M. Transcriptome of different fruiting stages in the cultivated mushroom Cyclocybe aegerita suggests a complex regulation of fruiting and reveals enzymes putatively involved in fungal oxylipin biosynthesis. BMC Genom. 22, 324 (2021). · DOI
- Chen, B. et al. Fruiting body formation in Volvariella volvacea can occur independently of its MAT-A-controlled bipolar mating system, enabling homothallic and heterothallic life cycles. G3-Genes Genom. Genet. 6, 2135–2146 (2016). · DOI
- Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014). · DOI · Paper page
- Wang, J. R., Holt, J., McMillan, L. & Jones, C. D. FMLRC: hybrid long read error correction using an FM-index. BMC Bioinform. 19, 50 (2018). · DOI
- Gnerre, S. et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl Acad. Sci. USA 108, 1513–1518 (2011). · DOI
- Warren, R. L. et al. LINKS: scalable, alignment-free scaffolding of draft genomes with long reads. Gigascience 4, 35 (2015). · DOI
- Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014). · DOI
- Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013). · DOI · Paper page
- Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015). · DOI · Paper page
- McKenna, A. et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010). · DOI · Paper page
- Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009). · DOI · Paper page
- Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011). · DOI
- Li, H. Toward better understanding of artifacts in variant calling from high-coverage samples. Bioinformatics 30, 2843–2851 (2014). · DOI
- Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015). · DOI · Paper page
- Humann, J. L., Lee, T., Ficklin, S. & Main, D. in Gene Prediction: Methods and Protocols (ed. Kollmar, M.) (Springer, 2019).
- Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol. 9, R7 (2008). · DOI
- Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011). · DOI
- Haas, B. J. et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654–5666 (2003). · DOI
- Ter-Hovhannisyan, V., Lomsadze, A., Chernoff, Y. O. & Borodovsky, M. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 18, 1979–1990 (2008). · DOI
- Hoff, K. J., Lomsadze, A., Borodovsky, M. & Stanke, M. Whole-genome annotation with BRAKER. Methods Mol. Biol. 1962, 65–95 (2019). · DOI
- Johnson, A. D. et al. SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 24, 2938–2939 (2008). · DOI
- Stanke, M., Diekhans, M., Baertsch, R. & Haussler, D. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 5, 637–644 (2008). · DOI · Paper page
- Testa, A. C., Hane, J. K., Ellwood, S. R. & Oliver, R. P. CodingQuarry: highly accurate hidden Markov model gene prediction in fungal genomes using RNA-seq transcripts. BMC Genom. 16, 170 (2015). · DOI
- Jones, P. et al. InterProScan 5: Genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014). · DOI
- El-Gebali, S. et al. The Pfam protein families database in 2019. Nucleic Acids Res. 47, D427–D432 (2019). · DOI · Paper page
- Pulman, J. A., Childs, K. L., Sgambelluri, R. M. & Walton, J. D. Expansion and diversification of the MSDIN family of cyclic peptide genes in the poisonous agarics Amanita phalloides and A. bisporigera. BMC Genom. 17, 1038 (2016). · DOI
- Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281 (2014). · DOI
- Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002). · DOI · Paper page
- Nguyen, L. T., Schmidt, H. A., Von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015). · DOI · Paper page
- Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., Von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017). · DOI · Paper page
- Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018). · DOI · Paper page
- Zhang, C., Rabiee, M., Sayyari, E. & Mirarab, S. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinform. 19, 15–30 (2018). · DOI · Paper page
- Rabiee, M. & Mirarab, S. Forcing external constraints on tree inference using ASTRAL. BMC Genom. 21, 218 (2020). · DOI
- Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990). · DOI · Paper page
- Wheeler, D. L. et al. Database resources of the national center for biotechnology information. Nucleic Acids Res. 31, 28–33 (2006). · DOI
- Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009). · DOI · Paper page
- Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012). · DOI
- Wick, R. R., Schultz, M. B., Zobel, J. & Holt, K. E. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31, 3350–3352 (2015). · DOI
- Stanke, M. & Morgenstern, B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 33, W465–W467 (2005). · DOI
- Hinnebusch, A. G. Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev. 75, 434–467 (2011). · DOI
- Darriba, D. I. et al. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol. Biol. Evol. 37, 291–294 (2020). · DOI
- Dobson, L., Reményi, I. & Tusnády, G. E. CCTOP: a consensus constrained topology prediction web server. Nucleic Acids Res. 43, W408–W412 (2015). · DOI
- Almagro Armenteros, J. J. et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat. Biotechnol. 37, 420–423 (2019). · DOI
- Cianfrocco, M. A., Wong-Barnum, M., Youn, C., Wagner, R. & Leschziner, A. COSMIC2: a science gateway for cryo-electron microscopy structure determination. In: Proceedings of the Practice and Experience in Advanced Research Computing 2017 on Sustainability, Success and Impact 1–5 (ACM, 2017) https://doi.org/10.1145/3093338.3093390. · DOI
- Kosugi, S., Hasebe, M., Tomita, M. & Yanagawa, H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl Acad. Sci. USA 106, 10171–10176 (2009). · DOI
- Yang, Y. et al. Sixty-five years of the long march in protein secondary structure prediction: the final stretch? Brief. Bioinform. 19, 482–494 (2018).
- Paradis, E. Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26, 419–420 (2010). · DOI
- Nordberg, H. et al. The genome portal of the department of energy joint genome institute: 2014 updates. Nucleic Acids Res. 42, D26–D31 (2014). · DOI
- Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009). · DOI
- Morel, B., Kozlov, A. M., Stamatakis, A. & Szöllősi, G. J. GeneRax: a tool for species-tree-aware maximum likelihood-based gene family tree inference under gene duplication, transfer, and loss. Mol. Biol. Evol. 37, 2763–2774 (2020). · DOI
- Schindelin, J. et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012). · DOI · Paper page
- James, P., Halladay, J. & Craig, E. A. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425–1436 (1996). · DOI
Metadata
- Authors
- Wang, Y.-W., McKeon, M. C., Elmore, H., Hess, J., Golan, J., Gage, H., Mao, W., Harrow, E., Gonçalves, S. C., Hull, C. M., & Pringle, A.
- Affiliations
- University of Wisconsin–Madison (US)
- University of Coimbra (PT)
- Corresponding author
- Wang, Yen-Wen
- ORCID
- Venue
- Nature Communications
- Published
- 2023-10-24
- Volume
- 14
- Issue
- 1
- Pages
- 6560-6560
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC10598064
- OpenAlex
- W4387909444
- Cited by
- 20
- References
- 4
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 5 · 2023: 5
- FWCI
- 1.78
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, cc-by)
- Funders
- Mycological Society of America
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycorrhizal Fungi and Plant Interactions
- Keywords
- Amanita phalloides, death cap mushroom, fungal invasion, bisexuality, mating-type locus, heterokaryosis, outcrossing, sporulation, California
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review