Comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus Pseudozyma (Ustilaginales)

Abstract Background The Ustilaginales comprise hundreds of plant-parasitic fungi with a characteristic life cycle that directly links sexual reproduction and parasitism: One of the two mating-type loci codes for a transcription factor that not only facilitates mating, but also initiates the infectio...

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Main Authors: Lena Steins, Marco Alexandre Guerreiro, Marine Duhamel, Fei Liu, Qi-Ming Wang, Teun Boekhout, Dominik Begerow
Format: Article
Language:English
Published: BMC 2023-06-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-023-09387-1
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author Lena Steins
Marco Alexandre Guerreiro
Marine Duhamel
Fei Liu
Qi-Ming Wang
Teun Boekhout
Dominik Begerow
author_facet Lena Steins
Marco Alexandre Guerreiro
Marine Duhamel
Fei Liu
Qi-Ming Wang
Teun Boekhout
Dominik Begerow
author_sort Lena Steins
collection DOAJ
description Abstract Background The Ustilaginales comprise hundreds of plant-parasitic fungi with a characteristic life cycle that directly links sexual reproduction and parasitism: One of the two mating-type loci codes for a transcription factor that not only facilitates mating, but also initiates the infection process. However, several species within the Ustilaginales have no described parasitic stage and were historically assigned to the genus Pseudozyma. Molecular studies have shown that the group is polyphyletic, with members being scattered in various lineages of the Ustilaginales. Together with recent findings of conserved fungal effectors in these non-parasitic species, this raises the question if parasitism has been lost recently and in multiple independent events or if there are hitherto undescribed parasitic stages of these fungi. Results In this study, we sequenced genomes of five Pseudozyma species together with six parasitic species from the Ustilaginales to compare their genomic capability to perform two central functions in sexual reproduction: mating and meiosis. While the loss of sexual capability is assumed in certain lineages and asexual species are common in Asco- and Basidiomycota, we were able to successfully annotate potentially functional mating and meiosis genes that are conserved throughout the whole group. Conclusion Our data suggest that at least the key functions of a sexual lifestyle are maintained in the analyzed genomes, challenging the current understanding of the so-called asexual species with respect to their evolution and ecological role.
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spelling doaj.art-0fd541c89e7446878e47a588687a53d92023-06-18T11:07:37ZengBMCBMC Genomics1471-21642023-06-0124111410.1186/s12864-023-09387-1Comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus Pseudozyma (Ustilaginales)Lena Steins0Marco Alexandre Guerreiro1Marine Duhamel2Fei Liu3Qi-Ming Wang4Teun Boekhout5Dominik Begerow6Evolution of Plants and Fungi, Ruhr-University BochumEvolution of Plants and Fungi, Ruhr-University BochumEvolution of Plants and Fungi, Ruhr-University BochumSchool of Life Sciences, Institute of Life Sciences and Green Development, Hebei UniversitySchool of Life Sciences, Institute of Life Sciences and Green Development, Hebei UniversityCollege of Science, King Saud UniversityEvolution of Plants and Fungi, Ruhr-University BochumAbstract Background The Ustilaginales comprise hundreds of plant-parasitic fungi with a characteristic life cycle that directly links sexual reproduction and parasitism: One of the two mating-type loci codes for a transcription factor that not only facilitates mating, but also initiates the infection process. However, several species within the Ustilaginales have no described parasitic stage and were historically assigned to the genus Pseudozyma. Molecular studies have shown that the group is polyphyletic, with members being scattered in various lineages of the Ustilaginales. Together with recent findings of conserved fungal effectors in these non-parasitic species, this raises the question if parasitism has been lost recently and in multiple independent events or if there are hitherto undescribed parasitic stages of these fungi. Results In this study, we sequenced genomes of five Pseudozyma species together with six parasitic species from the Ustilaginales to compare their genomic capability to perform two central functions in sexual reproduction: mating and meiosis. While the loss of sexual capability is assumed in certain lineages and asexual species are common in Asco- and Basidiomycota, we were able to successfully annotate potentially functional mating and meiosis genes that are conserved throughout the whole group. Conclusion Our data suggest that at least the key functions of a sexual lifestyle are maintained in the analyzed genomes, challenging the current understanding of the so-called asexual species with respect to their evolution and ecological role.https://doi.org/10.1186/s12864-023-09387-1Smut fungiPlant pathogensMatingMeiosisAsexualComparative genomics
spellingShingle Lena Steins
Marco Alexandre Guerreiro
Marine Duhamel
Fei Liu
Qi-Ming Wang
Teun Boekhout
Dominik Begerow
Comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus Pseudozyma (Ustilaginales)
BMC Genomics
Smut fungi
Plant pathogens
Mating
Meiosis
Asexual
Comparative genomics
title Comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus Pseudozyma (Ustilaginales)
title_full Comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus Pseudozyma (Ustilaginales)
title_fullStr Comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus Pseudozyma (Ustilaginales)
title_full_unstemmed Comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus Pseudozyma (Ustilaginales)
title_short Comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus Pseudozyma (Ustilaginales)
title_sort comparative genomics of smut fungi suggest the ability of meiosis and mating in asexual species of the genus pseudozyma ustilaginales
topic Smut fungi
Plant pathogens
Mating
Meiosis
Asexual
Comparative genomics
url https://doi.org/10.1186/s12864-023-09387-1
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