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Gene Balance Predicts Transcriptional Responses Immediately Following Ploidy Change in Arabidopsis thaliana

Michael J. Song, Barney I. Potter, Jeff J. Doyle, Jeremy E. Coate
Michael J. Song
aUniversity and Jepson Herbaria and Department of Integrative Biology, University of California, Berkeley, California 94720
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  • ORCID record for Michael J. Song
Barney I. Potter
bFred Hutchinson Cancer Research Center, Seattle, Washington 98109
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Jeff J. Doyle
cSchool of Integrative Plant Science, Cornell University, Ithaca, New York 14853
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Jeremy E. Coate
dDepartment of Biology, Reed College, Portland, Oregon 97202
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  • For correspondence: michael_song@berkeley.edu

Published May 2020. DOI: https://doi.org/10.1105/tpc.19.00832

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  • © 2020 American Society of Plant Biologists. All rights reserved.

Abstract

The gene balance hypothesis postulates that there is selection on gene copy number (gene dosage) to preserve the stoichiometric balance among interacting proteins. This presupposes that gene product abundance is governed by gene dosage and that gene dosage responses are consistent for interacting genes in a dosage-balance-sensitive network or complex. Gene dosage responses, however, have rarely been quantified, and the available data suggest that they are highly variable. We sequenced the transcriptomes of two synthetic autopolyploid accessions of Arabidopsis (Arabidopsis thaliana) and their diploid progenitors, as well as one natural tetraploid and its synthetic diploid produced via haploid induction, to estimate transcriptome size and dosage responses immediately following ploidy change. Similar to what has been observed in previous studies, overall transcriptome size does not exhibit a simple doubling in response to genome doubling, and individual gene dosage responses are highly variable in all three accessions, indicating that expression is not strictly coupled with gene dosage. Nonetheless, putatively dosage balance-sensitive gene groups (Gene Ontology terms, metabolic networks, gene families, and predicted interacting proteins) exhibit smaller and more coordinated dosage responses than do putatively dosage-insensitive gene groups, suggesting that constraints on dosage balance operate immediately following whole-genome duplication and that duplicate gene retention patterns are shaped by selection to preserve dosage balance.

  • Received October 23, 2019.
  • Revised February 18, 2020.
  • Accepted March 14, 2020.
  • Published March 17, 2020.
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Gene Balance Predicts Transcriptional Responses Immediately Following Ploidy Change in Arabidopsis thaliana
Michael J. Song, Barney I. Potter, Jeff J. Doyle, Jeremy E. Coate
The Plant Cell May 2020, 32 (5) 1434-1448; DOI: 10.1105/tpc.19.00832

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Gene Balance Predicts Transcriptional Responses Immediately Following Ploidy Change in Arabidopsis thaliana
Michael J. Song, Barney I. Potter, Jeff J. Doyle, Jeremy E. Coate
The Plant Cell May 2020, 32 (5) 1434-1448; DOI: 10.1105/tpc.19.00832
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  • Peer Review Report
  • IN BRIEF: Gene Dosage Balance Immediately Following Whole-Genome Duplication in Arabidopsis thaliana

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The Plant Cell: 32 (5)
The Plant Cell
Vol. 32, Issue 5
May 2020
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