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Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels

View ORCID ProfileEvan S. Forsythe, View ORCID ProfileCorrinne E. Grover, View ORCID ProfileEmma R. Miller, View ORCID ProfileJustin L. Conover, View ORCID ProfileMark A. Arick II, View ORCID ProfileM. Carolina F. Chavarro, View ORCID ProfileSoraya C. M. Leal-Bertioli, View ORCID ProfileDaniel G. Peterson, View ORCID ProfileJoel Sharbrough, View ORCID ProfileJonathan F. Wendel, View ORCID ProfileDaniel B. Sloan
doi: https://doi.org/10.1101/2022.03.12.484027
Evan S. Forsythe
aDepartment of Biology, Colorado State University, Fort Collins, CO 80523
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Corrinne E. Grover
bDepartment of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50010
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Emma R. Miller
bDepartment of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50010
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Justin L. Conover
bDepartment of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50010
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Mark A. Arick II
cInstitute for Genomics, Biocomputing & Biotechnology, Mississippi State University, Mississippi State, MS 39762
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M. Carolina F. Chavarro
dInstitute of Plant Breeding, Genetics and Genomics, Athens, GA 30602
eBayer Crop Science, Chesterfield, MO 63017, USA
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Soraya C. M. Leal-Bertioli
dInstitute of Plant Breeding, Genetics and Genomics, Athens, GA 30602
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  • ORCID record for Soraya C. M. Leal-Bertioli
Daniel G. Peterson
cInstitute for Genomics, Biocomputing & Biotechnology, Mississippi State University, Mississippi State, MS 39762
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Joel Sharbrough
fDepartment of Biology, New Mexico Institute of Mining and Technology, Socorro, NM, 87801
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Jonathan F. Wendel
bDepartment of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50010
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  • ORCID record for Jonathan F. Wendel
Daniel B. Sloan
aDepartment of Biology, Colorado State University, Fort Collins, CO 80523
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  • For correspondence: dan.sloan@colostate.edu
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ABSTRACT

Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of proteins involved in cytonuclear interactions. Here, we use ribo-depleted RNA-seq to analyze transcript abundance for nuclear and organellar genomes in leaf tissue from four different polyploid angiosperms and their close diploid relatives. We find that, even though plastid genomes contain <1% of the number of genes in the nuclear genome, they generate the majority (69.9–82.3%) of mRNA transcripts in the cell. Mitochondrial genes are responsible for a much smaller percentage (1.3–3.7%) of the leaf mRNA pool but still produce much higher transcript abundances per gene compared to nuclear genome. Nuclear genes encoding proteins that functionally interact with mitochondrial or plastid gene products exhibit mRNA expression levels that are consistently more than ten-fold lower than their organellar counterparts, indicating an extreme cytonuclear imbalance at the RNA level despite the predominance of equimolar interactions at the protein level. Nevertheless, interacting nuclear and organellar genes show strongly correlated transcript abundances across functional categories, suggesting that the observed mRNA stoichiometric imbalance does not preclude coordination of cytonuclear expression. Finally, we show that nuclear genome doubling does not alter the cytonuclear expression ratios observed in diploid relatives in consistent or systematic ways, indicating that successful polyploid plants are able to compensate for cytonuclear perturbations associated with nuclear genome doubling.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted March 14, 2022.
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Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels
Evan S. Forsythe, Corrinne E. Grover, Emma R. Miller, Justin L. Conover, Mark A. Arick II, M. Carolina F. Chavarro, Soraya C. M. Leal-Bertioli, Daniel G. Peterson, Joel Sharbrough, Jonathan F. Wendel, Daniel B. Sloan
bioRxiv 2022.03.12.484027; doi: https://doi.org/10.1101/2022.03.12.484027
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Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels
Evan S. Forsythe, Corrinne E. Grover, Emma R. Miller, Justin L. Conover, Mark A. Arick II, M. Carolina F. Chavarro, Soraya C. M. Leal-Bertioli, Daniel G. Peterson, Joel Sharbrough, Jonathan F. Wendel, Daniel B. Sloan
bioRxiv 2022.03.12.484027; doi: https://doi.org/10.1101/2022.03.12.484027

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