Widespread antisense transcription of Populus genome under drought

Widespread antisense transcription of Populus genome under drought Antisense transcription is widespread in many genomes and plays important regulatory roles in gene expression. The objective of our study was to investigate the extent and functional relevance of antisense transcription in forest trees. We employed Populus, a model tree species, to probe the antisense transcriptional response of tree genome under drought, through stranded RNA-seq analysis. We detected nearly 48% of annotated Populus gene loci with antisense transcripts and 44% of them with co-transcription from both DNA strands. Global distribution of reads pattern across annotated gene regions uncovered that antisense transcription was enriched in untranslated regions while sense reads were predominantly mapped in coding exons. We further detected 1185 drought-responsive sense and antisense gene loci and identified a strong positive correlation between the expression of antisense and sense transcripts. Additionally, we assessed the antisense expression in introns and found a strong correlation between intronic expression and exonic expression, confirming antisense transcription of introns contributes to transcriptional activity of Populus genome under drought. Finally, we functionally characterized drought-responsive sense–antisense transcript pairs through gene ontology analysis and discovered that functional groups including transcription factors and histones were concordantly regulated at both sense and antisense transcriptional level. Overall, our study demonstrated the extensive occurrence of antisense transcripts of Populus genes under drought and provided insights into genome structure, regulation pattern and functional significance of drought-responsive antisense genes in forest trees. Datasets generated in this study serve as a foundation for future genetic analysis to improve our understanding of gene regulation by antisense transcription. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Molecular Genetics and Genomics Springer Journals

Widespread antisense transcription of Populus genome under drought

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Publisher
Springer Journals
Copyright
Copyright © 2018 by Springer-Verlag GmbH Germany, part of Springer Nature
Subject
Life Sciences; Plant Genetics and Genomics; Human Genetics; Microbial Genetics and Genomics; Animal Genetics and Genomics; Biochemistry, general
ISSN
1617-4615
eISSN
1617-4623
D.O.I.
10.1007/s00438-018-1456-z
Publisher site
See Article on Publisher Site

Abstract

Antisense transcription is widespread in many genomes and plays important regulatory roles in gene expression. The objective of our study was to investigate the extent and functional relevance of antisense transcription in forest trees. We employed Populus, a model tree species, to probe the antisense transcriptional response of tree genome under drought, through stranded RNA-seq analysis. We detected nearly 48% of annotated Populus gene loci with antisense transcripts and 44% of them with co-transcription from both DNA strands. Global distribution of reads pattern across annotated gene regions uncovered that antisense transcription was enriched in untranslated regions while sense reads were predominantly mapped in coding exons. We further detected 1185 drought-responsive sense and antisense gene loci and identified a strong positive correlation between the expression of antisense and sense transcripts. Additionally, we assessed the antisense expression in introns and found a strong correlation between intronic expression and exonic expression, confirming antisense transcription of introns contributes to transcriptional activity of Populus genome under drought. Finally, we functionally characterized drought-responsive sense–antisense transcript pairs through gene ontology analysis and discovered that functional groups including transcription factors and histones were concordantly regulated at both sense and antisense transcriptional level. Overall, our study demonstrated the extensive occurrence of antisense transcripts of Populus genes under drought and provided insights into genome structure, regulation pattern and functional significance of drought-responsive antisense genes in forest trees. Datasets generated in this study serve as a foundation for future genetic analysis to improve our understanding of gene regulation by antisense transcription.

Journal

Molecular Genetics and Genomics – Springer Journals

Published: Jun 6, 2018

References

  • A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests
    Allen, CD; Macalady, AK; Chenchouni, H; Bachelet, D; McDowell, N; Vennetier, M; Kitzberger, T; Rigling, A; Breshears, DD; Hogg, EH; Gonzalez, P; Fensham, R; Zhang, Z; Castro, J; Demidova, N; Lim, J-H; Allard, G; Running, SW; Semerci, A; Cobb, N
  • Antisense long noncoding RNAs regulate var gene activation in the malaria parasite Plasmodium falciparum
    Amit-Avraham, I; Pozner, G; Eshar, S; Fastman, Y; Kolevzon, N; Yavin, E; Dzikowski, R
  • Detecting differential usage of exons from RNA-seq data
    Anders, S; Reyes, A; Huber, W
  • Natural antisense transcript of natriuretic peptide precursor A (NPPA): structural organization and modulation of NPPA expression
    Annilo, T; Kepp, K; Laan, M
  • Plant responses to abiotic stress: the chromatin context of transcriptional regulation
    Asensi-Fabado, M-A; Amtmann, A; Perrella, G
  • The landscape of antisense gene expression in human cancers
    Balbin, OA; Malik, R; Dhanasekaran, SM; Prensner, JR; Cao, X; Wu, Y-M; Robinson, D; Wang, R; Chen, G; Beer, DG
  • A natural antisense transcript regulates Zeb2/Sip1 gene expression during Snail1-induced epithelial–mesenchymal transition
    Beltran, M; Puig, I; Peña, C; García, JM; Álvarez, AB; Peña, R; Bonilla, F; Herreros, AG
  • Head-to-head antisense transcription and R-loop formation promotes transcriptional activation
    Boque-Sastre, R; Soler, M; Oliveira-Mateos, C; Portela, A; Moutinho, C; Sayols, S; Villanueva, A; Esteller, M; Guil, S
  • Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert
    Brosché, M; Vinocur, B; Alatalo, ER; Lamminmaki, A; Teichmann, T; Ottow, EA; Djilianov, D; Afif, D; Bogeat-Triboulot, MB; Altman, A
  • How tree roots respond to drought
    Brunner, I; Herzog, C; Dawes, MA; Arend, M; Sperisen, C
  • Expression analysis of the long non-coding RNA antisense to Uchl1 (AS Uchl1) during dopaminergic cells’ differentiation in vitro and in neurochemical models of Parkinson’s disease
    Carrieri, C; Forrest, ARR; Santoro, C; Persichetti, F; Carninci, P; Zucchelli, S; Gustincich, S
  • A simple and efficient method for isolating RNA from pine trees
    Chang, S; Puryear, J; Cairney, J
  • Genotypic variation in drought tolerance of poplar in relation to abscisic acid
    Chen, S; Wang, S; Altman, A; Hüttermann, A
  • Genome-wide analysis of gene expression in response to drought stress in Populus simonii
    Chen, J; Song, Y; Zhang, H; Zhang, D
  • Genome-wide identification of novel long non-coding RNAs in Populus tomentosa tension wood, opposite wood and normal wood xylem by RNA-sEq
    Chen, J; Quan, M; Zhang, D
  • Genome-wide identification and characterization of novel lncRNAs in Populus under nitrogen deficiency
    Chen, M; Wang, C; Bao, H; Chen, H; Wang, Y
  • Transcriptome profiling of drought responsive noncoding RNAs and their target genes in rice
    Chung, PJ; Jung, H; Jeong, D-H; Ha, S-H; Choi, YD; Kim, J-K
  • Comparative transcriptomics of drought responses in Populus: a meta-analysis of genome-wide expression profiling in mature leaves and root apices across two genotypes
    Cohen, D; Bogeat-Triboulot, M-B; Tisserant, E; Balzergue, S; Martin-Magniette, M-L; Lelandais, G; Ningre, N; Renou, J-P; Tamby, J-P; Thiec, D
  • Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization
    Csorba, T; Questa, JI; Sun, Q; Dean, C
  • Regulatory roles of natural antisense transcripts
    Faghihi, MA; Wahlestedt, C
  • Control of seed dormancy in Arabidopsis by a cis-acting noncoding antisense transcript
    Fedak, H; Palusinska, M; Krzyczmonik, K; Brzezniak, L; Yatusevich, R; Pietras, Z; Kaczanowski, S; Swiezewski, S
  • Analysis of intronic and exonic reads in RNA-seq data characterizes transcriptional and post-transcriptional regulation
    Gaidatzis, D; Burger, L; Florescu, M; Stadler, MB
  • Qualimap: evaluating next-generation sequencing alignment data
    García-Alcalde, F; Okonechnikov, K; Carbonell, J; Cruz, LM; Götz, S; Tarazona, S; Dopazo, J; Meyer, TF; Conesa, A
  • Regulated antisense transcription controls expression of cell-type-specific genes in yeast
    Gelfand, B; Mead, J; Bruning, A; Apostolopoulos, N; Tadigotla, V; Nagaraj, V; Sengupta, AM; Vershon, AK
  • Drought tolerance in three hybrid poplar clones submitted to different watering regimes
    Guo, X-Y; Zhang, X-S; Huang, Z-Y
  • Intraspecific variation in the Populus balsamifera drought transcriptome
    Hamanishi, ET; Raj, S; Wilkins, O; Thomas, BR; Mansfield, SD; Plant, AL; Campbell, MM
  • The antisense transcriptomes of human cells
    He, Y; Vogelstein, B; Velculescu, VE; Papadopoulos, N; Kinzler, KW
  • Short-rotation woody crops for bioenergy and biofuels applications
    Hinchee, M; Rottmann, W; Mullinax, L; Zhang, C; Chang, S; Cunningham, M; Pearson, L; Nehra, N
  • Circadian rhythms of sense and antisense transcription in sugarcane, a highly polyploid crop
    Hotta, CT; Nishiyama, MY; Souza, GM
  • A rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness
    Jabnoune, M; Secco, D; Lecampion, C; Robaglia, C; Shu, Q; Poirier, Y
  • Antisense transcription in the mammalian transcriptome
    Katayama, S; Tomaru, Y; Kasukawa, T; Waki, K; Nakanishi, M; Nakamura, M; Nishida, H; Yap, CC; Suzuki, M; Kawai, J
  • TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
    Kim, D; Pertea, G; Trapnell, C; Pimentel, H; Kelley, R; Salzberg, SL
  • Software for computing and annotating genomic ranges
    Lawrence, M; Huber, W; Pagès, H; Aboyoun, P; Carlson, M; Gentleman, R; Morgan, MT; Carey, VJ
  • Identification of sense and antisense transcripts regulated by drought in sugarcane
    Lembke, CG; Nishiyama, MY; Sato, PM; Andrade, RF; Souza, GM
  • Comprehensive comparative analysis of strand-specific RNA sequencing methods
    Levin, JZ; Yassour, M; Adiconis, X; Nusbaum, C; Thompson, DA; Friedman, N; Gnirke, A; Regev, A
  • The sequence alignment/map format and SAMtools
    Li, H; Handsaker, B; Wysoker, A; Fennell, T; Ruan, J; Homer, N; Marth, G; Abecasis, G; Durbin, R
  • Integrated detection of natural antisense transcripts using strand-specific RNA sequencing data
    Li, S; Liberman, LM; Mukherjee, N; Benfey, PN; Ohler, U
  • Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
    Love, MI; Huber, W; Anders, S
  • Strand-specific RNA-seq reveals widespread occurrence of novel cis- natural antisense transcripts in rice
    Lu, T; Zhu, C; Lu, G; Guo, Y; Zhou, Y; Zhang, Z; Zhao, Y; Li, W; Lu, Y; Tang, W
  • Arabidopsis non-coding RNA regulation in abiotic stress responses
    Matsui, A; Nguyen, AH; Nakaminami, K; Seki, M
  • Strand-specific RNA-Seq provides greater resolution of transcriptome profiling
    Mills, JD; Kawahara, Y; Janitz, M
  • Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides × Populus nigra
    Monclus, R; Dreyer, E; Villar, M; Delmotte, FM; Delay, D; Petit, JM; Barbaroux, C; Thiec, D; Brechet, C; Brignolas, F
  • Extensive relationship between antisense transcription and alternative splicing in the human genome
    Morrissy, AS; Griffith, M; Marra, MA
  • Intron retention is a major phenomenon in alternative splicing in Arabidopsis
    Ner-Gaon, H; Halachmi, R; Savaldi-Goldstein, S; Rubin, E; Ophir, R; Fluhr, R
  • Transcriptional interferences in cis natural antisense transcripts of humans and mice
    Osato, N; Suzuki, Y; Ikeo, K; Gojobori, T
  • Transcriptome analysis by strand-specific sequencing of complementary DNA
    Parkhomchuk, D; Borodina, T; Amstislavskiy, V; Banaru, M; Hallen, L; Krobitsch, S; Lehrach, H; Soldatov, A
  • Strand-specific RNA-seq reveals ordered patterns of sense and antisense transcription in Bacillus anthracis
    Passalacqua, KD; Varadarajan, A; Weist, C; Ondov, BD; Byrd, B; Read, TD; Bergman, NH
  • Stable intronic sequence RNAs have possible regulatory roles in Drosophila melanogaster
    Pek, JW; Osman, I; Tay, ML-I; Zheng, RT
  • Gene regulation by antisense transcription
    Pelechano, V; Steinmetz, LM
  • A drought-induced pervasive increase in tree mortality across Canada's boreal forests
    Peng, C; Ma, Z; Lei, X; Zhu, Q; Chen, H; Wang, W; Liu, S; Li, W; Fang, X; Zhou, X
  • Antisense artifacts in transcriptome microarray experiments are resolved by actinomycin D
    Perocchi, F; Xu, Z; Clauder-Münster, S; Steinmetz, LM
  • Flexible, quantitative and integrative genomic visualizations for publication-quality multi-panel figures
    Phanstiel, DH; Boyle, AP; Araya, CL; Snyder, MP; Sushi, R
  • Using Populus as a lignocellulosic feedstock for bioethanol
    Porth, I; El-Kassaby, YA
  • A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance
    Qin, T; Zhao, H; Cui, P; Albesher, N; Xiong, L
  • BEDTools: a flexible suite of utilities for comparing genomic features
    Quinlan, AR; Hall, IM
  • Drought tolerance of two black poplar (Populus nigra L.) clones: contribution of carbohydrates and oxidative stress defence
    Regier, N; Streb, S; COCOZZA, C; Schaub, M; Cherubini, P; Zeeman, SC; Frey, B
  • Antisense intronic non-coding RNA levels correlate to the degree of tumor differentiation in prostate cancer
    Reis, EM; Nakaya, HI; Louro, R; Canavez, FC; Flatschart, AVF; Almeida, GT; Egidio, CM; Paquola, AC; Machado, AA; Festa, F
  • Tree responses to drought
    Ryan, MG
  • Identification of drought-responsive and novel Populus trichocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis
    Shuai, P; Liang, D; Zhang, Z; Yin, W; Xia, X
  • Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa
    Shuai, P; Liang, D; Tang, S; Zhang, Z; Ye, C-Y; Su, Y; Xia, X; Yin, W
  • Identification of phasiRNAs and their drought- responsiveness in Populus trichocarpa
    Shuai, P; Su, Y; Liang, D; Zhang, Z; Xia, X; Yin, W
  • Strand-specific RNA-Seq reveals widespread and developmentally regulated transcription of natural antisense transcripts in Plasmodium falciparum
    Siegel, TN; Hon, C-C; Zhang, Q; Lopez-Rubio, J-J; Scheidig-Benatar, C; Martins, RM; Sismeiro, O; Coppée, J-Y; Scherf, A
  • Next-generation biomass feedstocks for biofuel production
    Simmons, BA; Loque, D; Blanch, HW
  • The genetics and genomics of the drought response in Populus
    Street, NR; Skogström, O; Sjödin, A; Tucker, J; Rodríguez-Acosta, M; Nilsson, P; Jansson, S; Taylor, G
  • Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target
    Swiezewski, S; Liu, F; Magusin, A; Dean, C
  • Population genomic analysis of gibberellin-responsive long non-coding RNAs in Populus
    Tian, J; Song, Y; Du, Q; Yang, X; Ci, D; Chen, J; Xie, J; Li, B; Zhang, D
  • The genome of black cottonwood, Populus trichocarpa (Torr. & Gray)
    Tuskan, GA; Difazio, S; Jansson, S; Bohlmann, J; Grigoriev, I; Hellsten, U; Putnam, N; Ralph, S; Rombauts, S; Salamov, A
  • Adaptive mechanisms and genomic plasticity for drought tolerance identified in European black poplar (Populus nigra L.)
    Viger, M; Smith, HK; Cohen, D; Dewoody, J; Trewin, H; Steenackers, M; Bastien, C; Taylor, G
  • Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana
    Wang, X-J; Gaasterland, T; Chua, N-H
  • RSeQC: quality control of RNA-seq experiments
    Wang, L; Wang, S; Li, W
  • Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis
    Wang, H; Chung, PJ; Liu, J; Jang, I-C; Kean, M; Xu, J; Chua, N-H
  • Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis
    Wang, H; Chung, PJ; Liu, J; Jang, I-C; Kean, MJ; Xu, J; Chua, N-H
  • Non-coding RNAs and their roles in stress response in plants
    Wang, J; Meng, X; Dobrovolskaya, OB; Orlov, YL; Chen, M
  • Genotype and time of day shape the Populus drought response
    Wilkins, O; Waldron, L; Nahal, H; Provart, NJ; Campbell, MM
  • GMAP: a genomic mapping and alignment program for mRNA and EST sequences
    Wu, TD; Watanabe, CK
  • Natural antisense transcripts are significantly involved in regulation of drought stress in maize
    Xu, J; Wang, Q; Freeling, M; Zhang, X; Xu, Y; Mao, Y; Tang, X; Wu, F; Lan, H; Cao, M
  • The R-loop is a common chromatin feature of the Arabidopsis genome
    Xu, W; Xu, H; Li, K; Fan, Y; Liu, Y; Yang, X; Sun, Q
  • Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species
    Yassour, M; Pfiffner, J; Levin, JZ; Adiconis, X; Gnirke, A; Nusbaum, C; Thompson, DA; Friedman, N; Regev, A
  • Gene ontology analysis for RNA-seq: accounting for selection bias
    Young, MD; Wakefield, MJ; Smyth, GK; Oshlack, A
  • Alternative splicing and gene duplication differentially shaped the regulation of isochorismate synthase in Populus and Arabidopsis
    Yuan, Y; Chung, JD; Fu, X; Johnson, VE; Ranjan, P; Booth, SL; Harding, SA; Tsai, CJ
  • Protein-coding cis-natural antisense transcripts have high and broad expression in Arabidopsis
    Zhan, S; Lukens, L

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