Uniparental nuclear inheritance following bisexual mating in fungi

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Abstract

Some remarkable animal species require an opposite-sex partner for their sexual development but discard the partner’s genome before gamete formation, generating hemi-clonal progeny in a process called hybridogenesis. Here, we discovered a similar phenomenon, termed pseudosexual reproduction, in a basidiomycete human fungal pathogen, Cryptococcus neoformans, where exclusive uniparental inheritance of nuclear genetic material was observed during bisexual reproduction. Analysis of strains expressing fluorescent reporter proteins revealed instances where only one of the parental nuclei was present in the terminal sporulating basidium. Whole-genome sequencing revealed the nuclear genome of the progeny was identical with one or the other parental genome. Pseudosexual reproduction was also detected in natural isolate crosses where it resulted in mainly MATa progeny, a bias observed in Cryptococcus ecological distribution as well. The mitochondria in these progeny were inherited from the MAT<strong>a</strong> parent, resulting in nuclear-mitochondrial genome exchange. The meiotic recombinase Dmc1 was found to be critical for pseudosexual reproduction. These findings reveal a novel, and potentially ecologically significant, mode of eukaryotic microbial reproduction that shares features with hybridogenesis in animals.

Data availability

The sequence data generated in this study were submitted to NCBI with the BioProject accession number PRJNA682203.

The following data sets were generated

1. Yadav V
2. Sun S
3. Heitman J
(2020) Uniparental reproduction in Cryptococcus neoformans
NCBI SRA, PRJNA682203.

https://dataview.ncbi.nlm.nih.gov/object/PRJNA682203?reviewer=e2jt63146mo4q30cnhtk8u6p6n

The following previously published data sets were used

1. Yadav V
2. Sun S
3. Coelho MA
4. Heitman J
(2020) Illumina reads of VYD135
SRA database, SRR10317030.

https://www.ncbi.nlm.nih.gov/sra/?term=SRR10317030
1. Broad Institute
(2012) Illumina whole genome shotgun sequencing of genomic DNA paired-end library 'Pond-151755' containing sample 'Cryptococcus neoformans H99'
SRA database, SRR642222.

https://www.ncbi.nlm.nih.gov/sra/?term=SRR642222
1. Borad Institute
(2012) Illumina whole genome shotgun sequencing of genomic DNA paired-end library 'Pond-151755' containing sample 'Cryptococcus neoformans H99'
SRA database, SRR647805.

https://www.ncbi.nlm.nih.gov/sra/?term=SRR647805

Article and author information

Author details

Vikas Yadav

Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-2650-9035
Sheng Sun

Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States

Competing interests
The authors declare that no competing interests exist.
Joseph Heitman

Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States

For correspondence
heitm001@duke.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6369-5995

Funding

National Institute of Allergy and Infectious Diseases (AI39115-24)

Joseph Heitman

National Institute of Allergy and Infectious Diseases (AI50113-16)

Joseph Heitman

National Institute of Allergy and Infectious Diseases (AI33654-04)

Joseph Heitman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.