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

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...

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Main Authors: Cervantes-Pérez, Sergio Alan, Yong-Villalobos, Lenin, Florez-Zapata, Nathalia M. V., Oropeza-Aburto, Araceli, Rico-Reséndiz, Félix, Amasende-Morales, Itzel, Lan, Tianying, Martínez, Octavio, Vielle-Calzada, Jean Philippe, Albert, Victor A., Herrera-Estrella, Luis
Other Authors: School of Biological Sciences
Format: Article
Language:English
Published: 2021
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Online Access:https://hdl.handle.net/10356/153775
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Institution: Nanyang Technological University
Language: English
id sg-ntu-dr.10356-153775
record_format dspace
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Biological sciences
Transposable Elements
Noncoding Transcription
spellingShingle Science::Biological sciences
Transposable Elements
Noncoding Transcription
Cervantes-Pérez, Sergio Alan
Yong-Villalobos, Lenin
Florez-Zapata, Nathalia M. V.
Oropeza-Aburto, Araceli
Rico-Reséndiz, Félix
Amasende-Morales, Itzel
Lan, Tianying
Martínez, Octavio
Vielle-Calzada, Jean Philippe
Albert, Victor A.
Herrera-Estrella, Luis
Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba
description 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.
author2 School of Biological Sciences
author_facet School of Biological Sciences
Cervantes-Pérez, Sergio Alan
Yong-Villalobos, Lenin
Florez-Zapata, Nathalia M. V.
Oropeza-Aburto, Araceli
Rico-Reséndiz, Félix
Amasende-Morales, Itzel
Lan, Tianying
Martínez, Octavio
Vielle-Calzada, Jean Philippe
Albert, Victor A.
Herrera-Estrella, Luis
format Article
author Cervantes-Pérez, Sergio Alan
Yong-Villalobos, Lenin
Florez-Zapata, Nathalia M. V.
Oropeza-Aburto, Araceli
Rico-Reséndiz, Félix
Amasende-Morales, Itzel
Lan, Tianying
Martínez, Octavio
Vielle-Calzada, Jean Philippe
Albert, Victor A.
Herrera-Estrella, Luis
author_sort Cervantes-Pérez, Sergio Alan
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
publishDate 2021
url https://hdl.handle.net/10356/153775
_version_ 1759857608392441856
spelling sg-ntu-dr.10356-1537752023-02-28T17:00:40Z Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba Cervantes-Pérez, Sergio Alan Yong-Villalobos, Lenin Florez-Zapata, Nathalia M. V. Oropeza-Aburto, Araceli Rico-Reséndiz, Félix Amasende-Morales, Itzel Lan, Tianying Martínez, Octavio Vielle-Calzada, Jean Philippe Albert, Victor A. Herrera-Estrella, Luis School of Biological Sciences Science::Biological sciences Transposable Elements Noncoding Transcription 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. Published version The authors thank G. Alejo-Jacuinde, B. Pérez-Sánchez and Q. Ortiz-Vasquez for help collecting plants and fowering specimens. Special thanks to R. Purbojati and S. Schuster for providing us the PacBio raw sequencing data. We thank J. Cervantes-Luevano for informatic support, Luis Delaye for evolutionary analysis advice and Koribinian Schneeberger for provided us syntenic dataset generating by SyRI. Authors acknowledge Dr. T. Markow for critical review of this manuscript. S.A.C.-P., I.A.-M. and F.R.-R are the recipients of a graduate scholarship from Conacyt. Tis work was supported in part by a Senior Scholar grant from the Howard Hughes Medical Institute and a Basic Science grant from CONACytT Mexico to L.H.-E. 2021-12-27T06:59:23Z 2021-12-27T06:59:23Z 2021 Journal Article Cervantes-Pérez, S. A., Yong-Villalobos, L., Florez-Zapata, N. M. V., Oropeza-Aburto, A., Rico-Reséndiz, F., Amasende-Morales, I., Lan, T., Martínez, O., Vielle-Calzada, J. P., Albert, V. A. & Herrera-Estrella, L. (2021). Atypical DNA methylation, sRNA-size distribution, and female gametogenesis in Utricularia gibba. Scientific Reports, 11(1), 15725-. https://dx.doi.org/10.1038/s41598-021-95054-y 2045-2322 https://hdl.handle.net/10356/153775 10.1038/s41598-021-95054-y 34344949 2-s2.0-85111992283 1 11 15725 en Scientific Reports © 2021 The Author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. application/pdf