The Genetic Regulation of Alternative Splicing in Populus deltoides

Alternative splicing (AS) is a mechanism of regulation of the proteome via enabling the production of multiple mRNAs from a single gene. To date, the dynamics of AS and its effects on the protein sequences of individuals in a large and genetically unrelated population of trees have not been investig...

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Main Authors: Jerald D. Noble, Kelly M. Balmant, Christopher Dervinis, Gustavo de los Campos, Márcio F. R. Resende, Matias Kirst, William Brad Barbazuk
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.00590/full
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author Jerald D. Noble
Kelly M. Balmant
Christopher Dervinis
Gustavo de los Campos
Gustavo de los Campos
Márcio F. R. Resende
Márcio F. R. Resende
Matias Kirst
Matias Kirst
Matias Kirst
William Brad Barbazuk
William Brad Barbazuk
William Brad Barbazuk
William Brad Barbazuk
author_facet Jerald D. Noble
Kelly M. Balmant
Christopher Dervinis
Gustavo de los Campos
Gustavo de los Campos
Márcio F. R. Resende
Márcio F. R. Resende
Matias Kirst
Matias Kirst
Matias Kirst
William Brad Barbazuk
William Brad Barbazuk
William Brad Barbazuk
William Brad Barbazuk
author_sort Jerald D. Noble
collection DOAJ
description Alternative splicing (AS) is a mechanism of regulation of the proteome via enabling the production of multiple mRNAs from a single gene. To date, the dynamics of AS and its effects on the protein sequences of individuals in a large and genetically unrelated population of trees have not been investigated. Here we describe the diversity of AS events within a previously genotyped population of 268 individuals of Populus deltoides and their putative downstream functional effects. Using a robust bioinformatics pipeline, the AS events and resulting transcript isoforms were discovered and quantified for each individual in the population. Analysis of the AS revealed that, as expected, most AS isoforms are conserved. However, we also identified a substantial collection of new, unannotated splice junctions and transcript isoforms. Heritability estimates for the expression of transcript isoforms showed that approximately half of the isoforms are heritable. The genetic regulators of these AS isoforms and splice junction usage were then identified using a genome-wide association analysis. The expression of AS isoforms was predominately cis regulated while splice junction usage was generally regulated in trans. Additionally, we identified 696 genes encoding alternatively spliced isoforms that changed putative protein domains relative to the longest protein coding isoform of the gene, and 859 genes exhibiting this same phenomenon relative to the most highly expressed isoform. Finally, we found that 748 genes gained or lost micro-RNA binding sites relative to the longest protein coding isoform of a given gene, while 940 gained or lost micro-RNA binding sites relative to the most highly expressed isoform. These results indicate that a significant fraction of AS events are genetically regulated and that this isoform usage can result in protein domain architecture changes.
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spelling doaj.art-522f560b8e2b420ea3b5c3f26b7853402022-12-22T01:08:15ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-06-011110.3389/fpls.2020.00590525233The Genetic Regulation of Alternative Splicing in Populus deltoidesJerald D. Noble0Kelly M. Balmant1Christopher Dervinis2Gustavo de los Campos3Gustavo de los Campos4Márcio F. R. Resende5Márcio F. R. Resende6Matias Kirst7Matias Kirst8Matias Kirst9William Brad Barbazuk10William Brad Barbazuk11William Brad Barbazuk12William Brad Barbazuk13Plant Molecular and Cellular Biology Graduate Program, University of Florida, Gainesville, FL, United StatesSchool of Forest Resources and Conservation, University of Florida, Gainesville, FL, United StatesSchool of Forest Resources and Conservation, University of Florida, Gainesville, FL, United StatesDepartment of Epidemiology and Biostatistics, Michigan State University, East Lansing, MI, United StatesDepartment of Statistics and Probability, Michigan State University, East Lansing, MI, United StatesPlant Molecular and Cellular Biology Graduate Program, University of Florida, Gainesville, FL, United StatesDepartment of Horticultural Science, University of Florida, Gainesville, FL, United StatesPlant Molecular and Cellular Biology Graduate Program, University of Florida, Gainesville, FL, United StatesSchool of Forest Resources and Conservation, University of Florida, Gainesville, FL, United StatesGenetics Institute, University of Florida, Gainesville, FL, United StatesPlant Molecular and Cellular Biology Graduate Program, University of Florida, Gainesville, FL, United StatesGenetics Institute, University of Florida, Gainesville, FL, United StatesDepartment of Biology, University of Florida, Gainesville, FL, United StatesInterdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL, United StatesAlternative splicing (AS) is a mechanism of regulation of the proteome via enabling the production of multiple mRNAs from a single gene. To date, the dynamics of AS and its effects on the protein sequences of individuals in a large and genetically unrelated population of trees have not been investigated. Here we describe the diversity of AS events within a previously genotyped population of 268 individuals of Populus deltoides and their putative downstream functional effects. Using a robust bioinformatics pipeline, the AS events and resulting transcript isoforms were discovered and quantified for each individual in the population. Analysis of the AS revealed that, as expected, most AS isoforms are conserved. However, we also identified a substantial collection of new, unannotated splice junctions and transcript isoforms. Heritability estimates for the expression of transcript isoforms showed that approximately half of the isoforms are heritable. The genetic regulators of these AS isoforms and splice junction usage were then identified using a genome-wide association analysis. The expression of AS isoforms was predominately cis regulated while splice junction usage was generally regulated in trans. Additionally, we identified 696 genes encoding alternatively spliced isoforms that changed putative protein domains relative to the longest protein coding isoform of the gene, and 859 genes exhibiting this same phenomenon relative to the most highly expressed isoform. Finally, we found that 748 genes gained or lost micro-RNA binding sites relative to the longest protein coding isoform of a given gene, while 940 gained or lost micro-RNA binding sites relative to the most highly expressed isoform. These results indicate that a significant fraction of AS events are genetically regulated and that this isoform usage can result in protein domain architecture changes.https://www.frontiersin.org/article/10.3389/fpls.2020.00590/fullalternative splicingpopulationisoformpoplarsplicing QTLtranscriptome
spellingShingle Jerald D. Noble
Kelly M. Balmant
Christopher Dervinis
Gustavo de los Campos
Gustavo de los Campos
Márcio F. R. Resende
Márcio F. R. Resende
Matias Kirst
Matias Kirst
Matias Kirst
William Brad Barbazuk
William Brad Barbazuk
William Brad Barbazuk
William Brad Barbazuk
The Genetic Regulation of Alternative Splicing in Populus deltoides
Frontiers in Plant Science
alternative splicing
population
isoform
poplar
splicing QTL
transcriptome
title The Genetic Regulation of Alternative Splicing in Populus deltoides
title_full The Genetic Regulation of Alternative Splicing in Populus deltoides
title_fullStr The Genetic Regulation of Alternative Splicing in Populus deltoides
title_full_unstemmed The Genetic Regulation of Alternative Splicing in Populus deltoides
title_short The Genetic Regulation of Alternative Splicing in Populus deltoides
title_sort genetic regulation of alternative splicing in populus deltoides
topic alternative splicing
population
isoform
poplar
splicing QTL
transcriptome
url https://www.frontiersin.org/article/10.3389/fpls.2020.00590/full
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