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Title: Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication

Abstract

Background: Transcription factors (TFs) play a key role in regulating plant development and response to environmental stimuli. While most genes revert to single copy after whole genome duplication (WGD) event, transcription factors are retained at a significantly higher rate. Little is known about how TF duplicates have diverged in their expression and regulation, the answer to which may contribute to a better understanding of the elevated retention rate among TFs. Results: In this work we assessed what features may explain differences in the retention of TF duplicates and other genes using Arabidopsis thaliana as a model. We integrated 34 expression, sequence, and conservation features to build a linear model for predicting the extent of duplicate retention following WGD events among TFs and 19 groups of genes with other functions. We found that TFs was the least well predicted, demonstrating the features of TFs are substantially deviated from duplicate genes in other function groups. Consistent with this, the evolution of TF expression patterns and cis-regulatory cites favors the partitioning of ancestral states among the resulting duplicates: one “ancestral” TF duplicate retains most ancestral expression and cis-regulatory sites, while the “non-ancestral” duplicate is enriched for novel regulatory sites. By modeling the retentionmore » of ancestral expression and cis-regulatory states in duplicate pairs using a system of differential equations, we discovered that TF duplicate pairs in a partitioned state are preferentially maintained. Conclusions: These TF duplicates with asymmetrically partitioned ancestral states are likely maintained because one copy retains ancestral functions while the other, at least in some cases, acquires novel cis-regulatory sites that may be important for novel, adaptive traits.« less

Authors:
 [1];  [2];  [3];  [4]; ORCiD logo [2]
  1. Michigan State Univ., East Lansing, MI (United States); Univ. of Tennessee, Knoxville, TN (United States)
  2. Michigan State Univ., East Lansing, MI (United States)
  3. Michigan State Univ., East Lansing, MI (United States); MYcroarray, Ann Arbor, MI (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
USDOE Great Lakes Bioenergy Research Center, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF)
OSTI Identifier:
1550801
Grant/Contract Number:  
SC0018409; IOS-1546617; DEB-1655386
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
BMC Evolutionary Biology (Online)
Additional Journal Information:
Journal Volume: 19; Journal Issue: 1; Journal ID: ISSN 1471-2148
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Expression divergence; cis-regulatory evolution; Duplicate retention

Citation Formats

Panchy, Nicholas L., Azodi, Christina B., Winship, Eamon F., O’Malley, Ronan C., and Shiu, Shin-Han. Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication. United States: N. p., 2019. Web. doi:10.1186/s12862-019-1398-z.
Panchy, Nicholas L., Azodi, Christina B., Winship, Eamon F., O’Malley, Ronan C., & Shiu, Shin-Han. Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication. United States. doi:10.1186/s12862-019-1398-z.
Panchy, Nicholas L., Azodi, Christina B., Winship, Eamon F., O’Malley, Ronan C., and Shiu, Shin-Han. Wed . "Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication". United States. doi:10.1186/s12862-019-1398-z. https://www.osti.gov/servlets/purl/1550801.
@article{osti_1550801,
title = {Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication},
author = {Panchy, Nicholas L. and Azodi, Christina B. and Winship, Eamon F. and O’Malley, Ronan C. and Shiu, Shin-Han},
abstractNote = {Background: Transcription factors (TFs) play a key role in regulating plant development and response to environmental stimuli. While most genes revert to single copy after whole genome duplication (WGD) event, transcription factors are retained at a significantly higher rate. Little is known about how TF duplicates have diverged in their expression and regulation, the answer to which may contribute to a better understanding of the elevated retention rate among TFs. Results: In this work we assessed what features may explain differences in the retention of TF duplicates and other genes using Arabidopsis thaliana as a model. We integrated 34 expression, sequence, and conservation features to build a linear model for predicting the extent of duplicate retention following WGD events among TFs and 19 groups of genes with other functions. We found that TFs was the least well predicted, demonstrating the features of TFs are substantially deviated from duplicate genes in other function groups. Consistent with this, the evolution of TF expression patterns and cis-regulatory cites favors the partitioning of ancestral states among the resulting duplicates: one “ancestral” TF duplicate retains most ancestral expression and cis-regulatory sites, while the “non-ancestral” duplicate is enriched for novel regulatory sites. By modeling the retention of ancestral expression and cis-regulatory states in duplicate pairs using a system of differential equations, we discovered that TF duplicate pairs in a partitioned state are preferentially maintained. Conclusions: These TF duplicates with asymmetrically partitioned ancestral states are likely maintained because one copy retains ancestral functions while the other, at least in some cases, acquires novel cis-regulatory sites that may be important for novel, adaptive traits.},
doi = {10.1186/s12862-019-1398-z},
journal = {BMC Evolutionary Biology (Online)},
issn = {1471-2148},
number = 1,
volume = 19,
place = {United States},
year = {2019},
month = {3}
}

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    Works referencing / citing this record:

    Gene Ontology: tool for the unification of biology
    journal, May 2000

    • Ashburner, Michael; Ball, Catherine A.; Blake, Judith A.
    • Nature Genetics, Vol. 25, Issue 1
    • DOI: 10.1038/75556

    Expression Partitioning between Genes Duplicated by Polyploidy under Abiotic Stress and during Organ Development
    journal, October 2007


    Redundancy and rewiring of genetic networks following genome-wide duplication events
    journal, April 2012


    Gene Duplicability of Core Genes Is Highly Consistent across All Angiosperms
    journal, January 2016

    • Li, Zhen; Defoort, Jonas; Tasdighian, Setareh
    • The Plant Cell, Vol. 28, Issue 2
    • DOI: 10.1105/tpc.15.00877

    The evolutionary significance of polyploidy
    journal, May 2017

    • Van de Peer, Yves; Mizrachi, Eshchar; Marchal, Kathleen
    • Nature Reviews Genetics, Vol. 18, Issue 7
    • DOI: 10.1038/nrg.2017.26

    The flowering world: a tale of duplications
    journal, December 2009


    The Pfam protein families database: towards a more sustainable future
    journal, December 2015

    • Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
    • Nucleic Acids Research, Vol. 44, Issue D1
    • DOI: 10.1093/nar/gkv1344

    Mutations in the Dof Zinc Finger Genes DAG2 and DAG1 Influence with Opposite Effects the Germination of Arabidopsis Seeds
    journal, June 2002

    • Gualberti, Giuliana; Papi, Maura; Bellucci, Luigi
    • The Plant Cell, Vol. 14, Issue 6
    • DOI: 10.1105/tpc.010491

    A gene expression map of Arabidopsis thaliana development
    journal, April 2005

    • Schmid, Markus; Davison, Timothy S.; Henz, Stefan R.
    • Nature Genetics, Vol. 37, Issue 5
    • DOI: 10.1038/ng1543

    Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss
    journal, February 2011

    • Schnable, J. C.; Springer, N. M.; Freeling, M.
    • Proceedings of the National Academy of Sciences, Vol. 108, Issue 10
    • DOI: 10.1073/pnas.1101368108

    Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences
    journal, December 2015

    • Freeling, Michael; Scanlon, Michael J.; Fowler, John E.
    • Current Opinion in Genetics & Development, Vol. 35
    • DOI: 10.1016/j.gde.2015.11.002

    Functional Divergence of Duplicated Genes Formed by Polyploidy during Arabidopsis Evolution
    journal, June 2004

    • Blanc, Guillaume; Wolfe, Kenneth H.
    • The Plant Cell, Vol. 16, Issue 7
    • DOI: 10.1105/tpc.021410

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    journal, July 2014

    • Soltis, D. E.; Visger, C. J.; Soltis, P. S.
    • American Journal of Botany, Vol. 101, Issue 7
    • DOI: 10.3732/ajb.1400178

    The Role of Lineage-Specific Gene Family Expansion in the Evolution of Eukaryotes
    journal, July 2002


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    journal, October 2004


    Escape from adaptive conflict after duplication in an anthocyanin pathway gene
    journal, June 2008


    Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat
    journal, October 2011

    • Zhang, Z.; Belcram, H.; Gornicki, P.
    • Proceedings of the National Academy of Sciences, Vol. 108, Issue 46
    • DOI: 10.1073/pnas.1110552108

    TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
    journal, January 2013


    PGDD: a database of gene and genome duplication in plants
    journal, November 2012

    • Lee, Tae-Ho; Tang, Haibao; Wang, Xiyin
    • Nucleic Acids Research, Vol. 41, Issue D1
    • DOI: 10.1093/nar/gks1104

    Origin and Early Evolution of Angiosperms
    journal, June 2008

    • Soltis, Douglas E.; Bell, Charles D.; Kim, Sangtae
    • Annals of the New York Academy of Sciences, Vol. 1133, Issue 1
    • DOI: 10.1196/annals.1438.005

    DOF AFFECTING GERMINATION 2 is a positive regulator of light-mediated seed germination and is repressed by DOF AFFECTING GERMINATION 1
    journal, January 2015

    • Santopolo, Silvia; Boccaccini, Alessandra; Lorrai, Riccardo
    • BMC Plant Biology, Vol. 15, Issue 1
    • DOI: 10.1186/s12870-015-0453-1

    Importance of Lineage-Specific Expansion of Plant Tandem Duplicates in the Adaptive Response to Environmental Stimuli
    journal, August 2008

    • Hanada, Kousuke; Zou, Cheng; Lehti-Shiu, Melissa D.
    • Plant Physiology, Vol. 148, Issue 2
    • DOI: 10.1104/pp.108.122457

    Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape
    journal, May 2016


    Genome duplication and the origin of angiosperms
    journal, November 2005


    Doubling down on genomes: Polyploidy and crop plants
    journal, October 2014

    • Renny-Byfield, Simon; Wendel, Jonathan F.
    • American Journal of Botany, Vol. 101, Issue 10
    • DOI: 10.3732/ajb.1400119

    Prevalent Role of Gene Features in Determining Evolutionary Fates of Whole-Genome Duplication Duplicated Genes in Flowering Plants
    journal, February 2013

    • Jiang, Wen-kai; Liu, Yun-long; Xia, En-hua
    • Plant Physiology, Vol. 161, Issue 4
    • DOI: 10.1104/pp.112.200147

    Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events
    journal, March 2003

    • Bowers, John E.; Chapman, Brad A.; Rong, Junkang
    • Nature, Vol. 422, Issue 6930
    • DOI: 10.1038/nature01521

    The Gene Balance Hypothesis: From Classical Genetics to Modern Genomics
    journal, February 2007


    Finding and Comparing Syntenic Regions among Arabidopsis and the Outgroups Papaya, Poplar, and Grape: CoGe with Rosids
    journal, October 2008

    • Lyons, Eric; Pedersen, Brent; Kane, Josh
    • Plant Physiology, Vol. 148, Issue 4
    • DOI: 10.1104/pp.108.124867

    Evolutionary Rate and Duplicability in the Arabidopsis thaliana Protein–Protein Interaction Network
    journal, November 2012

    • Alvarez-Ponce, David; Fares, Mario A.
    • Genome Biology and Evolution, Vol. 4, Issue 12
    • DOI: 10.1093/gbe/evs101

    Following Gene Duplication, Paralog Interference Constrains Transcriptional Circuit Evolution
    journal, October 2013

    • Baker, Christopher R.; Hanson-Smith, Victor; Johnson, Alexander D.
    • Science, Vol. 342, Issue 6154
    • DOI: 10.1126/science.1240810

    Evolutionary Dynamics and Functional Specialization of Plant Paralogs Formed by Whole and Small-Scale Genome Duplications
    journal, July 2012

    • Carretero-Paulet, Lorenzo; Fares, Mario A.
    • Molecular Biology and Evolution, Vol. 29, Issue 11
    • DOI: 10.1093/molbev/mss162

    MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
    journal, January 2013

    • Katoh, K.; Standley, D. M.
    • Molecular Biology and Evolution, Vol. 30, Issue 4
    • DOI: 10.1093/molbev/mst010

    Ancestral polyploidy in seed plants and angiosperms
    journal, April 2011

    • Jiao, Yuannian; Wickett, Norman J.; Ayyampalayam, Saravanaraj
    • Nature, Vol. 473, Issue 7345
    • DOI: 10.1038/nature09916

    The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution: Research review
    journal, November 2009


    Molecular Mechanisms Underlying Origin and Diversification of the Angiosperm Flower
    journal, August 2007


    Transcription Factor Families Have Much Higher Expansion Rates in Plants than in Animals
    journal, September 2005

    • Shiu, Shin-Han; Shih, Ming-Che; Li, Wen-Hsiung
    • Plant Physiology, Vol. 139, Issue 1
    • DOI: 10.1104/pp.105.065110

    Molecular evidence for an ancient duplication of the entire yeast genome
    journal, June 1997

    • Wolfe, Kenneth H.; Shields, Denis C.
    • Nature, Vol. 387, Issue 6634
    • DOI: 10.1038/42711

    A Role for KNAT Class II Genes in Root Development
    journal, January 2007

    • Truernit, Elisabeth; Haseloff, Jim
    • Plant Signaling & Behavior, Vol. 2, Issue 1
    • DOI: 10.4161/psb.2.1.3604

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