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Title: A Variable Polyglutamine Repeat Affects Subcellular Localization and Regulatory Activity of a Populus ANGUSTIFOLIA Protein

Abstract

Polyglutamine (polyQ) stretches have been reported to occur in proteins across many organisms including animals, fungi and plants. Expansion of these repeats has attracted much attention due their associations with numerous human diseases including Huntington's and other neurological maladies. This suggests that the relative length of polyQ stretches is an important modulator of their function. Here, we report the identification of a Populus C-terminus binding protein (CtBP) ANGUSTIFOLIA (PtAN1) which contains a polyQ stretch whose functional relevance had not been established. Analysis of 917 resequenced Populus trichocarpa genotypes revealed three allelic variants at this locus encoding 11-, 13- and 15-glutamine residues. Transient expression assays using Populus leaf mesophyll protoplasts revealed that the 11Q variant exhibited strong nuclear localization whereas the 15Q variant was only found in the cytosol, with the 13Q variant exhibiting localization in both subcellular compartments. We assessed functional implications by evaluating expression changes of putative PtAN1 targets in response to overexpression of the three allelic variants and observed allele-specific differences in expression levels of putative targets. Our results provide evidence that variation in polyQ length modulates PtAN1 function by altering subcellular localization.

Authors:
 [1]; ORCiD logo [2];  [1];  [1];  [3];  [3];  [4];  [5];  [2];  [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division. BioEnergy Science Center
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division. BioEnergy Science Center. Center for Bioenergy Innovation
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division. BioEnergy Science Center. Center for Bioenergy Innovation; Univ. of Tennessee, Knoxville, TN (United States). The Bredesen Center for Interdisciplinary Research and Graduate Education
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1468119
Alternate Identifier(s):
OSTI ID: 1615277
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
G3
Additional Journal Information:
Journal Volume: 8; Journal Issue: 8; Journal ID: ISSN 2160-1836
Publisher:
Genetics Society of America
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; polyQ; subcellular localization; cell wall; lignin; Populus

Citation Formats

Bryan, Anthony C., Zhang, Jin, Guo, Jianjun, Ranjan, Priya, Singan, Vasanth, Barry, Kerrie, Schmutz, Jeremy, Weighill, Deborah, Jacobson, Daniel, Jawdy, Sara, Tuskan, Gerald A., Chen, Jin-Gui, and Muchero, Wellington. A Variable Polyglutamine Repeat Affects Subcellular Localization and Regulatory Activity of a Populus ANGUSTIFOLIA Protein. United States: N. p., 2018. Web. doi:10.1534/g3.118.200188.
Bryan, Anthony C., Zhang, Jin, Guo, Jianjun, Ranjan, Priya, Singan, Vasanth, Barry, Kerrie, Schmutz, Jeremy, Weighill, Deborah, Jacobson, Daniel, Jawdy, Sara, Tuskan, Gerald A., Chen, Jin-Gui, & Muchero, Wellington. A Variable Polyglutamine Repeat Affects Subcellular Localization and Regulatory Activity of a Populus ANGUSTIFOLIA Protein. United States. https://doi.org/10.1534/g3.118.200188
Bryan, Anthony C., Zhang, Jin, Guo, Jianjun, Ranjan, Priya, Singan, Vasanth, Barry, Kerrie, Schmutz, Jeremy, Weighill, Deborah, Jacobson, Daniel, Jawdy, Sara, Tuskan, Gerald A., Chen, Jin-Gui, and Muchero, Wellington. Fri . "A Variable Polyglutamine Repeat Affects Subcellular Localization and Regulatory Activity of a Populus ANGUSTIFOLIA Protein". United States. https://doi.org/10.1534/g3.118.200188. https://www.osti.gov/servlets/purl/1468119.
@article{osti_1468119,
title = {A Variable Polyglutamine Repeat Affects Subcellular Localization and Regulatory Activity of a Populus ANGUSTIFOLIA Protein},
author = {Bryan, Anthony C. and Zhang, Jin and Guo, Jianjun and Ranjan, Priya and Singan, Vasanth and Barry, Kerrie and Schmutz, Jeremy and Weighill, Deborah and Jacobson, Daniel and Jawdy, Sara and Tuskan, Gerald A. and Chen, Jin-Gui and Muchero, Wellington},
abstractNote = {Polyglutamine (polyQ) stretches have been reported to occur in proteins across many organisms including animals, fungi and plants. Expansion of these repeats has attracted much attention due their associations with numerous human diseases including Huntington's and other neurological maladies. This suggests that the relative length of polyQ stretches is an important modulator of their function. Here, we report the identification of a Populus C-terminus binding protein (CtBP) ANGUSTIFOLIA (PtAN1) which contains a polyQ stretch whose functional relevance had not been established. Analysis of 917 resequenced Populus trichocarpa genotypes revealed three allelic variants at this locus encoding 11-, 13- and 15-glutamine residues. Transient expression assays using Populus leaf mesophyll protoplasts revealed that the 11Q variant exhibited strong nuclear localization whereas the 15Q variant was only found in the cytosol, with the 13Q variant exhibiting localization in both subcellular compartments. We assessed functional implications by evaluating expression changes of putative PtAN1 targets in response to overexpression of the three allelic variants and observed allele-specific differences in expression levels of putative targets. Our results provide evidence that variation in polyQ length modulates PtAN1 function by altering subcellular localization.},
doi = {10.1534/g3.118.200188},
journal = {G3},
number = 8,
volume = 8,
place = {United States},
year = {Fri Jun 08 00:00:00 EDT 2018},
month = {Fri Jun 08 00:00:00 EDT 2018}
}

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Works referencing / citing this record:

Data Integration in Poplar: ‘Omics Layers and Integration Strategies
journal, September 2019

  • Weighill, Deborah; Tschaplinski, Timothy J.; Tuskan, Gerald A.
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