Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba

Abstract The most studied DNA methylation pathway in plants is the RNA Directed DNA Methylation (RdDM), a conserved mechanism that involves the role of noncoding RNAs to control the expansion of the noncoding genome. Genome-wide DNA methylation levels have been reported to correlate with genome size...

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Autores principales: Sergio Alan Cervantes-Pérez, Lenin Yong-Villalobos, Nathalia M. V. Florez-Zapata, Araceli Oropeza-Aburto, Félix Rico-Reséndiz, Itzel Amasende-Morales, Tianying Lan, Octavio Martínez, Jean Philippe Vielle-Calzada, Victor A. Albert, Luis Herrera-Estrella
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Publicado: Nature Portfolio 2021
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spelling oai:doaj.org-article:93464d22550e4bb09bd87baba028fe912021-12-02T17:06:31ZAtypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba10.1038/s41598-021-95054-y2045-2322https://doaj.org/article/93464d22550e4bb09bd87baba028fe912021-08-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-95054-yhttps://doaj.org/toc/2045-2322Abstract The most studied DNA methylation pathway in plants is the RNA Directed DNA Methylation (RdDM), a conserved mechanism that involves the role of noncoding RNAs to control the expansion of the noncoding genome. Genome-wide DNA methylation levels have been reported to correlate with genome size. However, little is known about the catalog of noncoding RNAs and the impact on DNA methylation in small plant genomes with reduced noncoding regions. Because of the small length of intergenic regions in the compact genome of the carnivorous plant Utricularia gibba, we investigated its repertoire of noncoding RNA and DNA methylation landscape. Here, we report that, compared to other angiosperms, U. gibba has an unusual distribution of small RNAs and reduced global DNA methylation levels. DNA methylation was determined using a novel strategy based on long-read DNA sequencing with the Pacific Bioscience platform and confirmed by whole-genome bisulfite sequencing. Moreover, some key genes involved in the RdDM pathway may not represented by compensatory paralogs or comprise truncated proteins, for example, U. gibba DICER-LIKE 3 (DCL3), encoding a DICER endonuclease that produces 24-nt small-interfering RNAs, has lost key domains required for complete function. Our results unveil that a truncated DCL3 correlates with a decreased proportion of 24-nt small-interfering RNAs, low DNA methylation levels, and developmental abnormalities during female gametogenesis in U. gibba. Alterations in female gametogenesis are reminiscent of RdDM mutant phenotypes in Arabidopsis thaliana. It would be interesting to further study the biological implications of the DCL3 truncation in U. gibba, as it could represent an initial step in the evolution of RdDM pathway in compact genomes.Sergio Alan Cervantes-PérezLenin Yong-VillalobosNathalia M. V. Florez-ZapataAraceli Oropeza-AburtoFélix Rico-ReséndizItzel Amasende-MoralesTianying LanOctavio MartínezJean Philippe Vielle-CalzadaVictor A. AlbertLuis Herrera-EstrellaNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-14 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Sergio Alan Cervantes-Pérez
Lenin Yong-Villalobos
Nathalia M. V. Florez-Zapata
Araceli Oropeza-Aburto
Félix Rico-Reséndiz
Itzel Amasende-Morales
Tianying Lan
Octavio Martínez
Jean Philippe Vielle-Calzada
Victor A. Albert
Luis Herrera-Estrella
Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba
description Abstract The most studied DNA methylation pathway in plants is the RNA Directed DNA Methylation (RdDM), a conserved mechanism that involves the role of noncoding RNAs to control the expansion of the noncoding genome. Genome-wide DNA methylation levels have been reported to correlate with genome size. However, little is known about the catalog of noncoding RNAs and the impact on DNA methylation in small plant genomes with reduced noncoding regions. Because of the small length of intergenic regions in the compact genome of the carnivorous plant Utricularia gibba, we investigated its repertoire of noncoding RNA and DNA methylation landscape. Here, we report that, compared to other angiosperms, U. gibba has an unusual distribution of small RNAs and reduced global DNA methylation levels. DNA methylation was determined using a novel strategy based on long-read DNA sequencing with the Pacific Bioscience platform and confirmed by whole-genome bisulfite sequencing. Moreover, some key genes involved in the RdDM pathway may not represented by compensatory paralogs or comprise truncated proteins, for example, U. gibba DICER-LIKE 3 (DCL3), encoding a DICER endonuclease that produces 24-nt small-interfering RNAs, has lost key domains required for complete function. Our results unveil that a truncated DCL3 correlates with a decreased proportion of 24-nt small-interfering RNAs, low DNA methylation levels, and developmental abnormalities during female gametogenesis in U. gibba. Alterations in female gametogenesis are reminiscent of RdDM mutant phenotypes in Arabidopsis thaliana. It would be interesting to further study the biological implications of the DCL3 truncation in U. gibba, as it could represent an initial step in the evolution of RdDM pathway in compact genomes.
format article
author Sergio Alan Cervantes-Pérez
Lenin Yong-Villalobos
Nathalia M. V. Florez-Zapata
Araceli Oropeza-Aburto
Félix Rico-Reséndiz
Itzel Amasende-Morales
Tianying Lan
Octavio Martínez
Jean Philippe Vielle-Calzada
Victor A. Albert
Luis Herrera-Estrella
author_facet Sergio Alan Cervantes-Pérez
Lenin Yong-Villalobos
Nathalia M. V. Florez-Zapata
Araceli Oropeza-Aburto
Félix Rico-Reséndiz
Itzel Amasende-Morales
Tianying Lan
Octavio Martínez
Jean Philippe Vielle-Calzada
Victor A. Albert
Luis Herrera-Estrella
author_sort Sergio Alan Cervantes-Pérez
title Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba
title_short Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba
title_full Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba
title_fullStr Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba
title_full_unstemmed Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba
title_sort atypical dna methylation, srna-size distribution, and female gametogenesis in utricularia gibba
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/93464d22550e4bb09bd87baba028fe91
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