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Title: A comprehensive genomic scan reveals gene dosage balance impacts on quantitative traits in Populus trees

Abstract

Gene dosage variation and the associated changes in gene expression influence a wide variety of traits, ranging from cancer in humans to yield in plants. It is also expected to affect important traits of ecological and agronomic importance in forest trees, but this variation has not been systematically characterized or exploited. Here we performed a comprehensive scan of the Populus genome for dosage-sensitive loci affecting quantitative trait variation for spring and fall phenology and biomass production. The study population was a large collection of clonally propagated F1 hybrid lines of Populus that saturate the genome 10-fold with deletions and insertions (indels) of known sizes and positions. As a group, the phenotypic means of the indel lines consistently differed from control nonindel lines, with an overall negative effect of both insertions and deletions on all biomass-related traits but more diverse effects and an overall wider phenotypic distribution of the indel lines for the phenology-related traits. We also investigated the correlation between gene dosage at specific chromosomal locations and phenotype, to identify dosage quantitative trait loci (dQTL). Such dQTL were detected for most phenotypes examined, but stronger effect dQTL were identified for the phenology-related traits than for the biomass traits. Furthermore ourmore » genome-wide screen for dosage sensitivity in a higher eukaryote demonstrates the importance of global genomic balance and the impact of dosage on life history traits.« less

Authors:
 [1];  [2];  [3];  [4];  [4]; ORCiD logo [4];  [4];  [1]
  1. U.S. Dept. of Agriculture Forest Service, Davis, CA (United States); Univ. of California, Davis, CA (United States)
  2. U.S. Dept. of Agriculture Forest Service, Davis, CA (United States); Western Washington Univ., Bellingham, WA (United States)
  3. U.S. Dept. of Agriculture Forest Service, Davis, CA (United States)
  4. Univ. of California, Davis, CA (United States)
Publication Date:
Research Org.:
Univ. of California, Davis, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1558427
Grant/Contract Number:  
[SC0007183]
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
[ Journal Volume: 116; Journal Issue: 27]; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; gene dosage; quantitative trait; forest trees; genome balance; copy number variation

Citation Formats

Bastiaanse, Héloïse, Zinkgraf, Matthew, Canning, Courtney, Tsai, Helen, Lieberman, Meric, Comai, Luca, Henry, Isabelle, and Groover, Andrew. A comprehensive genomic scan reveals gene dosage balance impacts on quantitative traits in Populus trees. United States: N. p., 2019. Web. doi:10.1073/pnas.1903229116.
Bastiaanse, Héloïse, Zinkgraf, Matthew, Canning, Courtney, Tsai, Helen, Lieberman, Meric, Comai, Luca, Henry, Isabelle, & Groover, Andrew. A comprehensive genomic scan reveals gene dosage balance impacts on quantitative traits in Populus trees. United States. doi:10.1073/pnas.1903229116.
Bastiaanse, Héloïse, Zinkgraf, Matthew, Canning, Courtney, Tsai, Helen, Lieberman, Meric, Comai, Luca, Henry, Isabelle, and Groover, Andrew. Tue . "A comprehensive genomic scan reveals gene dosage balance impacts on quantitative traits in Populus trees". United States. doi:10.1073/pnas.1903229116.
@article{osti_1558427,
title = {A comprehensive genomic scan reveals gene dosage balance impacts on quantitative traits in Populus trees},
author = {Bastiaanse, Héloïse and Zinkgraf, Matthew and Canning, Courtney and Tsai, Helen and Lieberman, Meric and Comai, Luca and Henry, Isabelle and Groover, Andrew},
abstractNote = {Gene dosage variation and the associated changes in gene expression influence a wide variety of traits, ranging from cancer in humans to yield in plants. It is also expected to affect important traits of ecological and agronomic importance in forest trees, but this variation has not been systematically characterized or exploited. Here we performed a comprehensive scan of the Populus genome for dosage-sensitive loci affecting quantitative trait variation for spring and fall phenology and biomass production. The study population was a large collection of clonally propagated F1 hybrid lines of Populus that saturate the genome 10-fold with deletions and insertions (indels) of known sizes and positions. As a group, the phenotypic means of the indel lines consistently differed from control nonindel lines, with an overall negative effect of both insertions and deletions on all biomass-related traits but more diverse effects and an overall wider phenotypic distribution of the indel lines for the phenology-related traits. We also investigated the correlation between gene dosage at specific chromosomal locations and phenotype, to identify dosage quantitative trait loci (dQTL). Such dQTL were detected for most phenotypes examined, but stronger effect dQTL were identified for the phenology-related traits than for the biomass traits. Furthermore our genome-wide screen for dosage sensitivity in a higher eukaryote demonstrates the importance of global genomic balance and the impact of dosage on life history traits.},
doi = {10.1073/pnas.1903229116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = [27],
volume = [116],
place = {United States},
year = {2019},
month = {6}
}

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This content will become publicly available on June 18, 2020
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Works referenced in this record:

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Multitrait genome‐wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits
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Genomic diversity in forest trees
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Recombination Rate Variation, Hitchhiking, and Demographic History Shape Deleterious Load in Poplar
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The Gene Balance Hypothesis: From Classical Genetics to Modern Genomics
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Prediction of deleterious human alleles
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Multiply to conquer: Copy number variations at Ppd-B1 and Vrn-A1 facilitate global adaptation in wheat
journal, July 2015


GIGANTEA- like genes control seasonal growth cessation in Populus
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A Tree Ortholog of APETALA1 Mediates Photoperiodic Control of Seasonal Growth
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Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa
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Vernalization: Winter and the Timing of Flowering in Plants
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A Unified Model for Budburst of Trees
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Targeted deep sequencing of flowering regulators in Brassica napus reveals extensive copy number variation
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Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome
journal, June 2013

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The Timing of Flowering: Figure 1.
journal, October 2010


Models of the spring phenology of boreal and temperate trees: is there something missing?
journal, September 2006


A genetic network mediating the control of bud break in hybrid aspen
journal, October 2018


    Works referencing / citing this record:

    Exploring the etiology of haploinsufficiency
    journal, January 2002


    Creation and Genomic Analysis of Irradiation Hybrids in Populus : Creation and Analysis of Irradiation Hybrids in
    journal, March 2016

    • Zinkgraf, Matthew; Haiby, Kathy; Lieberman, Meric C.
    • Current Protocols in Plant Biology, Vol. 1, Issue 2
    • DOI: 10.1002/cppb.20025

    Dosage-Dependent Gene Regulation in Multicellular Eukaryotes: Implications for Dosage Compensation, Aneuploid Syndromes, and Quantitative Traits
    journal, June 2001

    • Birchler, James A.; Bhadra, Utpal; Bhadra, Manika Pal
    • Developmental Biology, Vol. 234, Issue 2
    • DOI: 10.1006/dbio.2001.0262

    A Unified Model for Budburst of Trees
    journal, December 2000


    CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals
    journal, March 2010

    • Knox, Andrea K.; Dhillon, Taniya; Cheng, Hongmei
    • Theoretical and Applied Genetics, Vol. 121, Issue 1
    • DOI: 10.1007/s00122-010-1288-7

    Copy number variation of chromosome 5A and its association with Q gene expression, morphological aberrations, and agronomic performance of winter wheat cultivars
    journal, September 2013

    • Förster, Sebastian; Schumann, Erika; Baumann, Mario
    • Theoretical and Applied Genetics, Vol. 126, Issue 12
    • DOI: 10.1007/s00122-013-2192-8

    Copy number variation of CBF-A14 at the Fr-A2 locus determines frost tolerance in winter durum wheat
    journal, February 2016

    • Sieber, Alisa-Naomi; Longin, C. Friedrich H.; Leiser, Willmar L.
    • Theoretical and Applied Genetics, Vol. 129, Issue 6
    • DOI: 10.1007/s00122-016-2685-3

    Copy number variation at the HvCBF4–HvCBF2 genomic segment is a major component of frost resistance in barley
    journal, June 2016

    • Francia, Enrico; Morcia, Caterina; Pasquariello, Marianna
    • Plant Molecular Biology, Vol. 92, Issue 1-2
    • DOI: 10.1007/s11103-016-0505-4

    A Tree Ortholog of APETALA1 Mediates Photoperiodic Control of Seasonal Growth
    journal, March 2014


    Genomic diversity in forest trees
    journal, April 2007


    Dosage sensitivity and the evolution of gene families in yeast
    journal, July 2003

    • Papp, Balázs; Pál, Csaba; Hurst, Laurence D.
    • Nature, Vol. 424, Issue 6945
    • DOI: 10.1038/nature01771

    Global variation in copy number in the human genome
    journal, November 2006

    • Redon, Richard; Ishikawa, Shumpei; Fitch, Karen R.
    • Nature, Vol. 444, Issue 7118
    • DOI: 10.1038/nature05329

    Finding the missing heritability of complex diseases
    journal, October 2009

    • Manolio, Teri A.; Collins, Francis S.; Cox, Nancy J.
    • Nature, Vol. 461, Issue 7265
    • DOI: 10.1038/nature08494

    Genome-wide genetic changes during modern breeding of maize
    journal, June 2012

    • Jiao, Yinping; Zhao, Hainan; Ren, Longhui
    • Nature Genetics, Vol. 44, Issue 7
    • DOI: 10.1038/ng.2312

    Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
    journal, August 2014

    • Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli
    • Nature Genetics, Vol. 46, Issue 10
    • DOI: 10.1038/ng.3075

    Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results
    journal, November 1995

    • Lander, Eric; Kruglyak, Leonid
    • Nature Genetics, Vol. 11, Issue 3
    • DOI: 10.1038/ng1195-241

    A genetic network mediating the control of bud break in hybrid aspen
    journal, October 2018


    Targeted deep sequencing of flowering regulators in Brassica napus reveals extensive copy number variation
    journal, March 2017

    • Schiessl, Sarah; Huettel, Bruno; Kuehn, Diana
    • Scientific Data, Vol. 4, Issue 1
    • DOI: 10.1038/sdata.2017.13

    Sequence and gene expression evolution of paralogous genes in willows
    journal, December 2015

    • Harikrishnan, Srilakshmy L.; Pucholt, Pascal; Berlin, Sofia
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep18662

    Phenology is a major determinant of tree species range
    journal, September 2001


    FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar
    journal, June 2011

    • Hsu, C. -Y.; Adams, J. P.; Kim, H.
    • Proceedings of the National Academy of Sciences, Vol. 108, Issue 26
    • DOI: 10.1073/pnas.1104713108

    Gene balance hypothesis: Connecting issues of dosage sensitivity across biological disciplines
    journal, August 2012

    • Birchler, J. A.; Veitia, R. A.
    • Proceedings of the National Academy of Sciences, Vol. 109, Issue 37
    • DOI: 10.1073/pnas.1207726109

    Global impacts of chromosomal imbalance on gene expression in Arabidopsis and other taxa
    journal, November 2018

    • Hou, Jie; Shi, Xiaowen; Chen, Chen
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 48
    • DOI: 10.1073/pnas.1807796115

    Prediction of deleterious human alleles
    journal, March 2001


    Characterization of the Poplar Pan-Genome by Genome-Wide Identification of Structural Variation
    journal, August 2016

    • Pinosio, Sara; Giacomello, Stefania; Faivre-Rampant, Patricia
    • Molecular Biology and Evolution, Vol. 33, Issue 10
    • DOI: 10.1093/molbev/msw161

    Recombination Rate Variation, Hitchhiking, and Demographic History Shape Deleterious Load in Poplar
    journal, August 2016

    • Zhang, M.; Zhou, L.; Bawa, R.
    • Molecular Biology and Evolution, Vol. 33, Issue 11
    • DOI: 10.1093/molbev/msw169

    Models of the spring phenology of boreal and temperate trees: is there something missing?
    journal, September 2006


    Identification of deleterious mutations within three human genomes
    journal, July 2009


    Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus
    journal, October 2011

    • Rodgers-Melnick, E.; Mane, S. P.; Dharmawardhana, P.
    • Genome Research, Vol. 22, Issue 1
    • DOI: 10.1101/gr.125146.111

    The Timing of Flowering: Figure 1.
    journal, October 2010


    Molecular Characterization of Rht-1 Dwarfing Genes in Hexaploid Wheat
    journal, October 2011

    • Pearce, Stephen; Saville, Robert; Vaughan, Simon P.
    • Plant Physiology, Vol. 157, Issue 4
    • DOI: 10.1104/pp.111.183657

    PtABI3 Impinges on the Growth and Differentiation of Embryonic Leaves during Bud Set in Poplar
    journal, July 2002

    • Rohde, Antje; Prinsen, Els; De Rycke, Riet
    • The Plant Cell, Vol. 14, Issue 8
    • DOI: 10.1105/tpc.003186

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


    A System for Dosage-Based Functional Genomics in Poplar
    journal, August 2015

    • Henry, Isabelle M.; Zinkgraf, Matthew S.; Groover, Andrew T.
    • The Plant Cell, Vol. 27, Issue 9
    • DOI: 10.1105/tpc.15.00349

    Bud set in poplar - genetic dissection of a complex trait in natural and hybrid populations
    journal, October 2010


    Leaf-out phenology of temperate woody plants: from trees to ecosystems: Tansley review
    journal, July 2011


    A tandem segmental duplication (TSD) in green revolution gene Rht-D1b region underlies plant height variation
    journal, July 2012


    Gene copy number variations involved in balsam poplar ( Populus balsamifera L.) adaptive variations
    journal, October 2018

    • Prunier, Julien; Giguère, Isabelle; Ryan, Natalie
    • Molecular Ecology, Vol. 28, Issue 6
    • DOI: 10.1111/mec.14836

    Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa
    journal, November 2013

    • McKown, Athena D.; Guy, Robert D.; Klápště, Jaroslav
    • New Phytologist, Vol. 201, Issue 4
    • DOI: 10.1111/nph.12601

    GIGANTEA- like genes control seasonal growth cessation in Populus
    journal, March 2018

    • Ding, Jihua; Böhlenius, Henrik; Rühl, Mark Georg
    • New Phytologist, Vol. 218, Issue 4
    • DOI: 10.1111/nph.15087

    Multitrait genome‐wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits
    journal, April 2019

    • Chhetri, Hari B.; Macaya‐Sanz, David; Kainer, David
    • New Phytologist, Vol. 223, Issue 1
    • DOI: 10.1111/nph.15777

    Copy number variations of CBF genes at the Fr-A2 locus are essential components of winter hardiness in wheat
    journal, February 2017

    • Würschum, Tobias; Longin, C. Friedrich H.; Hahn, Volker
    • The Plant Journal, Vol. 89, Issue 4
    • DOI: 10.1111/tpj.13424

    The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
    journal, September 2006


    Aneuploidy Drives Genomic Instability in Yeast
    journal, August 2011


    Copy Number Variation of Multiple Genes at Rhg1 Mediates Nematode Resistance in Soybean
    journal, October 2012


    Dormancy of Trees in Winter
    journal, January 1971


    Trans-Acting Dosage Effects on the Expression of Model Gene Systems in Maize Aneuploids
    journal, December 1994


    Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication
    journal, March 2018


    Genetic variation in dosage effects in maize aneuploids
    journal, August 1996

    • Lee, E. A.; Coe, E. H.; Darrah, L. L.
    • Genome, Vol. 39, Issue 4
    • DOI: 10.1139/g96-090

    Dosage effects on morphological and quantitative traits in maize aneuploids
    journal, October 1996

    • Lee, E. A.; Darrah, L. L.; Coe, E. H.
    • Genome, Vol. 39, Issue 5
    • DOI: 10.1139/g96-113

    Regulation and Identity of Florigen: FLOWERING LOCUS T Moves Center Stage
    journal, June 2008


    Vernalization: Winter and the Timing of Flowering in Plants
    journal, November 2009


    Five QTL hotspots for yield in short rotation coppice bioenergy poplar: The Poplar Biomass Loci
    journal, January 2009

    • Rae, Anne M.; Street, Nathaniel; Robinson, Kathryn
    • BMC Plant Biology, Vol. 9, Issue 1
    • DOI: 10.1186/1471-2229-9-23

    Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome
    journal, June 2013

    • Muñoz-Amatriaín, María; Eichten, Steven R.; Wicker, Thomas
    • Genome Biology, Vol. 14, Issue 6
    • DOI: 10.1186/gb-2013-14-6-r58

    Multiply to conquer: Copy number variations at Ppd-B1 and Vrn-A1 facilitate global adaptation in wheat
    journal, July 2015


    The distribution and impact of common copy-number variation in the genome of the domesticated apple, Malus x domestica Borkh
    journal, October 2015


    A major locus controls local adaptation and adaptive life history variation in a perennial plant
    journal, June 2018


    Quantitative Trait Loci Analysis Using the False Discovery Rate
    journal, June 2005


    Predicting the Timing of Budburst in Temperate Trees
    journal, January 1992

    • Hunter, Alison F.; Lechowicz, Martin J.
    • The Journal of Applied Ecology, Vol. 29, Issue 3
    • DOI: 10.2307/2404467