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Widespread antisense transcription of Populus genome under drought

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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.

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Acknowledgements

We would like to thank Information Technology unit at Michigan Technological University for IT support. We also appreciate prompt technical assistance from the developers and authors of software tools employed in our analysis, including Dr. Douglas H. Phanstiel (Sushi package), Dr. Liguo Wang and Dr. Shengqin Wang (RSeQC), and Dr. Devon Ryan (R script in expression analysis of intronic reads).

Funding

This study is financially supported in part by Michigan Technological University Research Excellence Fund Research Seed Grants and the National Institute of Food and Agriculture, US Department of Agriculture, under Award 2012-67014-19445 to Dr. Yuan.

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  1. School of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, 49931, USA

    Yinan Yuan & Su Chen

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  1. Yinan Yuan
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  2. Su Chen
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YY conceived the study, designed and performed the experiment. YY and SC analyzed the data. YY drafted the manuscript.

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Correspondence to Yinan Yuan.

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The authors declare that they have no conflict of interest.

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This article does not contain any studies involving human participants and/or animals.

Dataset access

All sequence reads from this study have been submitted to NCBI Sequence Read Archive (SRA; http://www.ncbi.nlm.nih.gov/sra) under accession no. SRP103219. The raw count data for sense and antisense gene expression of our analysis is available in the NCBI Gene Expression Omnibus (GEO; http://www.ncbi.nlm.nih.gov/geo) under accession number GSE97463. Reviewer can access to the data through https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?token=etyrokscbhslrop&acc=GSE97463.

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Communicated by S. Hohmann.

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Yuan, Y., Chen, S. Widespread antisense transcription of Populus genome under drought. Mol Genet Genomics 293, 1017–1033 (2018). https://doi.org/10.1007/s00438-018-1456-z

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