siRNAs regulate DNA methylation and interfere with gene and lncRNA expression in the heterozygous polyploid switchgrass

Abstract Background Understanding the DNA methylome and its relationship with non-coding RNAs, including microRNAs (miRNAs) and long non-coding RNAs (lncRNAs), is essential for elucidating the molecular mechanisms underlying key biological processes in plants. Few studies have examined the functiona...

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Main Authors: Haidong Yan, Aureliano Bombarely, Bin Xu, Taylor P. Frazier, Chengran Wang, Peilin Chen, Jing Chen, Tomas Hasing, Chenming Cui, Xinquan Zhang, Bingyu Zhao, Linkai Huang
Format: Article
Language:English
Published: BMC 2018-07-01
Series:Biotechnology for Biofuels
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13068-018-1202-0
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author Haidong Yan
Aureliano Bombarely
Bin Xu
Taylor P. Frazier
Chengran Wang
Peilin Chen
Jing Chen
Tomas Hasing
Chenming Cui
Xinquan Zhang
Bingyu Zhao
Linkai Huang
author_facet Haidong Yan
Aureliano Bombarely
Bin Xu
Taylor P. Frazier
Chengran Wang
Peilin Chen
Jing Chen
Tomas Hasing
Chenming Cui
Xinquan Zhang
Bingyu Zhao
Linkai Huang
author_sort Haidong Yan
collection DOAJ
description Abstract Background Understanding the DNA methylome and its relationship with non-coding RNAs, including microRNAs (miRNAs) and long non-coding RNAs (lncRNAs), is essential for elucidating the molecular mechanisms underlying key biological processes in plants. Few studies have examined the functional roles of the DNA methylome in grass species with highly heterozygous polyploid genomes. Results We performed genome-wide DNA methylation profiling in the tetraploid switchgrass (Panicum virgatum L.) cultivar ‘Alamo’ using bisulfite sequencing. Single-base-resolution methylation patterns were observed in switchgrass leaf and root tissues, which allowed for characterization of the relationship between DNA methylation and mRNA, miRNA, and lncRNA populations. The results of this study revealed that siRNAs positively regulate DNA methylation of the mCHH sites surrounding genes, and that DNA methylation interferes with gene and lncRNA expression in switchgrass. Ninety-six genes covered by differentially methylated regions (DMRs) were annotated by GO analysis as being involved in stimulus-related processes. Functionally, 82% (79/96) of these genes were found to be hypomethylated in switchgrass root tissue. Sequencing analysis of lncRNAs identified two lncRNAs that are potential precursors of miRNAs, which are predicted to target genes that function in cellulose biosynthesis, stress regulation, and stem and root development. Conclusions This study characterized the DNA methylome in switchgrass and elucidated its relevance to gene and non-coding RNAs. These results provide valuable genomic resources and references that will aid further epigenetic research in this important biofuel crop.
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spelling doaj.art-86e4dc50444c4ce990c5f3e1abd0c6292022-12-22T00:14:06ZengBMCBiotechnology for Biofuels1754-68342018-07-0111111910.1186/s13068-018-1202-0siRNAs regulate DNA methylation and interfere with gene and lncRNA expression in the heterozygous polyploid switchgrassHaidong Yan0Aureliano Bombarely1Bin Xu2Taylor P. Frazier3Chengran Wang4Peilin Chen5Jing Chen6Tomas Hasing7Chenming Cui8Xinquan Zhang9Bingyu Zhao10Linkai Huang11Department of Grassland Science, Animal Science and Technology College, Sichuan Agricultural UniversityDepartment of Horticulture, Virginia TechCollege of Grassland Science, Nanjing Agricultural UniversityDepartment of Plant Sciences, University of TennesseeDepartment of Grassland Science, Animal Science and Technology College, Sichuan Agricultural UniversityDepartment of Grassland Science, Animal Science and Technology College, Sichuan Agricultural UniversityDepartment of Grassland Science, Animal Science and Technology College, Sichuan Agricultural UniversityDepartment of Horticulture, Virginia TechDepartment of Plant Pathology, Physiology, and Weed Science, Virginia TechDepartment of Grassland Science, Animal Science and Technology College, Sichuan Agricultural UniversityDepartment of Horticulture, Virginia TechDepartment of Grassland Science, Animal Science and Technology College, Sichuan Agricultural UniversityAbstract Background Understanding the DNA methylome and its relationship with non-coding RNAs, including microRNAs (miRNAs) and long non-coding RNAs (lncRNAs), is essential for elucidating the molecular mechanisms underlying key biological processes in plants. Few studies have examined the functional roles of the DNA methylome in grass species with highly heterozygous polyploid genomes. Results We performed genome-wide DNA methylation profiling in the tetraploid switchgrass (Panicum virgatum L.) cultivar ‘Alamo’ using bisulfite sequencing. Single-base-resolution methylation patterns were observed in switchgrass leaf and root tissues, which allowed for characterization of the relationship between DNA methylation and mRNA, miRNA, and lncRNA populations. The results of this study revealed that siRNAs positively regulate DNA methylation of the mCHH sites surrounding genes, and that DNA methylation interferes with gene and lncRNA expression in switchgrass. Ninety-six genes covered by differentially methylated regions (DMRs) were annotated by GO analysis as being involved in stimulus-related processes. Functionally, 82% (79/96) of these genes were found to be hypomethylated in switchgrass root tissue. Sequencing analysis of lncRNAs identified two lncRNAs that are potential precursors of miRNAs, which are predicted to target genes that function in cellulose biosynthesis, stress regulation, and stem and root development. Conclusions This study characterized the DNA methylome in switchgrass and elucidated its relevance to gene and non-coding RNAs. These results provide valuable genomic resources and references that will aid further epigenetic research in this important biofuel crop.http://link.springer.com/article/10.1186/s13068-018-1202-0Panicum virgatum L.DNA methylationGene expressionNon-coding RNAsRNA-dependent DNA methylationDifferentially methylated regions
spellingShingle Haidong Yan
Aureliano Bombarely
Bin Xu
Taylor P. Frazier
Chengran Wang
Peilin Chen
Jing Chen
Tomas Hasing
Chenming Cui
Xinquan Zhang
Bingyu Zhao
Linkai Huang
siRNAs regulate DNA methylation and interfere with gene and lncRNA expression in the heterozygous polyploid switchgrass
Biotechnology for Biofuels
Panicum virgatum L.
DNA methylation
Gene expression
Non-coding RNAs
RNA-dependent DNA methylation
Differentially methylated regions
title siRNAs regulate DNA methylation and interfere with gene and lncRNA expression in the heterozygous polyploid switchgrass
title_full siRNAs regulate DNA methylation and interfere with gene and lncRNA expression in the heterozygous polyploid switchgrass
title_fullStr siRNAs regulate DNA methylation and interfere with gene and lncRNA expression in the heterozygous polyploid switchgrass
title_full_unstemmed siRNAs regulate DNA methylation and interfere with gene and lncRNA expression in the heterozygous polyploid switchgrass
title_short siRNAs regulate DNA methylation and interfere with gene and lncRNA expression in the heterozygous polyploid switchgrass
title_sort sirnas regulate dna methylation and interfere with gene and lncrna expression in the heterozygous polyploid switchgrass
topic Panicum virgatum L.
DNA methylation
Gene expression
Non-coding RNAs
RNA-dependent DNA methylation
Differentially methylated regions
url http://link.springer.com/article/10.1186/s13068-018-1202-0
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