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Title: Dominance and Sexual Dimorphism Pervade the Salix purpurea L. Transcriptome

Abstract

The heritability of gene expression is critical in understanding heterosis and is dependent on allele-specific regulation by local and remote factors in the genome. We used RNA-Seq to test whether variation in gene expression among F 1 and F 2 intraspecific Salix purpurea progeny is attributable to cis- and trans-regulatory divergence. We assessed the mode of inheritance based on gene expression levels and allele-specific expression for F1 and F2 intraspecific progeny in two distinct tissue types: shoot tip and stem internode. In addition, we explored sexually dimorphic patterns of inheritance and regulatory divergence among F 1 progeny individuals. We show that in S. purpurea intraspecific crosses, gene expression inheritance largely exhibits a maternal dominant pattern, regardless of tissue type or pedigree. A significantly greater number of cis- and trans-regulated genes coincided with upregulation of the maternal parent allele in the progeny, irrespective of the magnitude, whereas the paternal allele was higher expressed for genes showing cis × trans or compensatory regulation. Importantly, consistent with previous genetic mapping results for sex in shrub willow, we have delimited sex-biased gene expression to a 2 Mb pericentromeric region on S. purpurea chr15 and further refined the sex determination region. Lastly, altogether, our resultsmore » offer insight into the inheritance of gene expression in S. purpurea as well as evidence of sexually dimorphic expression which may have contributed to the evolution of dioecy in Salix.« less

Authors:
 [1];  [2];  [2];  [1];  [2]; ORCiD logo [1]
  1. Cornell Univ., Geneva, NY (United States). New York State Agricultural Experiment Station, School of Integrative Plant Science, Horticulture Section
  2. J. Craig Venter Inst., Rockville, MD (United States)
Publication Date:
Research Org.:
Cornell Univ., Ithaca, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1426176
Grant/Contract Number:  
SC0008375
Resource Type:
Accepted Manuscript
Journal Name:
Genome Biology and Evolution
Additional Journal Information:
Journal Volume: 9; Journal Issue: 9; Journal ID: ISSN 1759-6653
Publisher:
Society for Molecular Biology and Evolution
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; differential expression; dioecy; regulatory divergence; sex determination; shrub willow; ZW system

Citation Formats

Carlson, Craig H., Choi, Yongwook, Chan, Agnes P., Serapiglia, Michelle J., Town, Christopher D., and Smart, Lawrence B. Dominance and Sexual Dimorphism Pervade the Salix purpurea L. Transcriptome. United States: N. p., 2017. Web. doi:10.1093/gbe/evx174.
Carlson, Craig H., Choi, Yongwook, Chan, Agnes P., Serapiglia, Michelle J., Town, Christopher D., & Smart, Lawrence B. Dominance and Sexual Dimorphism Pervade the Salix purpurea L. Transcriptome. United States. doi:10.1093/gbe/evx174.
Carlson, Craig H., Choi, Yongwook, Chan, Agnes P., Serapiglia, Michelle J., Town, Christopher D., and Smart, Lawrence B. Fri . "Dominance and Sexual Dimorphism Pervade the Salix purpurea L. Transcriptome". United States. doi:10.1093/gbe/evx174. https://www.osti.gov/servlets/purl/1426176.
@article{osti_1426176,
title = {Dominance and Sexual Dimorphism Pervade the Salix purpurea L. Transcriptome},
author = {Carlson, Craig H. and Choi, Yongwook and Chan, Agnes P. and Serapiglia, Michelle J. and Town, Christopher D. and Smart, Lawrence B.},
abstractNote = {The heritability of gene expression is critical in understanding heterosis and is dependent on allele-specific regulation by local and remote factors in the genome. We used RNA-Seq to test whether variation in gene expression among F1 and F2 intraspecific Salix purpurea progeny is attributable to cis- and trans-regulatory divergence. We assessed the mode of inheritance based on gene expression levels and allele-specific expression for F1 and F2 intraspecific progeny in two distinct tissue types: shoot tip and stem internode. In addition, we explored sexually dimorphic patterns of inheritance and regulatory divergence among F1 progeny individuals. We show that in S. purpurea intraspecific crosses, gene expression inheritance largely exhibits a maternal dominant pattern, regardless of tissue type or pedigree. A significantly greater number of cis- and trans-regulated genes coincided with upregulation of the maternal parent allele in the progeny, irrespective of the magnitude, whereas the paternal allele was higher expressed for genes showing cis × trans or compensatory regulation. Importantly, consistent with previous genetic mapping results for sex in shrub willow, we have delimited sex-biased gene expression to a 2 Mb pericentromeric region on S. purpurea chr15 and further refined the sex determination region. Lastly, altogether, our results offer insight into the inheritance of gene expression in S. purpurea as well as evidence of sexually dimorphic expression which may have contributed to the evolution of dioecy in Salix.},
doi = {10.1093/gbe/evx174},
journal = {Genome Biology and Evolution},
number = 9,
volume = 9,
place = {United States},
year = {2017},
month = {9}
}

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Works referenced in this record:

Ribosomal Protein S3, a New Substrate of Akt, Serves as a Signal Mediator between Neuronal Apoptosis and DNA Repair
journal, July 2010

  • Lee, Sang Bae; Kwon, Il-Sun; Park, Jihye
  • Journal of Biological Chemistry, Vol. 285, Issue 38
  • DOI: 10.1074/jbc.M110.131367

RNA-Seq Analysis of Allele-Specific Expression, Hybrid Effects, and Regulatory Divergence in Hybrids Compared with Their Parents from Natural Populations
journal, May 2013

  • Bell, Graeme D. M.; Kane, Nolan C.; Rieseberg, Loren H.
  • Genome Biology and Evolution, Vol. 5, Issue 7
  • DOI: 10.1093/gbe/evt072

What makes the sex ratio female-biased in the dioecious tree Salix sachalinensis?
journal, September 2007


High-density linkage mapping and evolution of paralogs and orthologs in Salix and Populus
journal, January 2010


Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009


Genotype × environment interaction analysis of North American shrub willow yield trials confirms superior performance of triploid hybrids
journal, March 2016

  • Fabio, Eric S.; Volk, Timothy A.; Miller, Raymond O.
  • GCB Bioenergy, Vol. 9, Issue 2
  • DOI: 10.1111/gcbb.12344

The fasciclin-like arabinogalactan protein family of Eucalyptus grandis contains members that impact wood biology and biomechanics
journal, February 2015

  • MacMillan, Colleen P.; Taylor, Lynette; Bi, Yingdong
  • New Phytologist, Vol. 206, Issue 4
  • DOI: 10.1111/nph.13320

Genetic mapping of sex-linked markers in Salix viminalis L.
journal, August 2003


Early selection of novel triploid hybrids of shrub willow with improved biomass yield relative to diploids
journal, January 2014

  • Serapiglia, Michelle J.; Gouker, Fred E.; Smart, Lawrence B.
  • BMC Plant Biology, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2229-14-74

CmCGG Methylation-Independent Parent-of-Origin Effects on Genome-Wide Transcript Levels in Isogenic Reciprocal F1 Triploid Plants
journal, November 2013


Untapped Potential: Opportunities and Challenges for Sustainable Bioenergy Production from Marginal Lands in the Northeast USA
journal, September 2014

  • Stoof, Cathelijne R.; Richards, Brian K.; Woodbury, Peter B.
  • BioEnergy Research, Vol. 8, Issue 2
  • DOI: 10.1007/s12155-014-9515-8

A mixed model approach for evaluating yield improvements in interspecific hybrids of shrub willow, a dedicated bioenergy crop
journal, February 2017


The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations
journal, June 2003

  • Rieseberg, Loren H.; Widmer, Alex; Arntz, A. Michele
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 358, Issue 1434
  • DOI: 10.1098/rstb.2003.1283

AMY‐1, a novel C‐MYC binding protein that stimulates transcription activity of C‐MYC
journal, August 1998


Quantitative Genetics of Traits Indicative of Biomass Production and Heterosis in 34 Full-sib F1 Salix eriocephala Families
journal, March 2008

  • Cameron, Kimberly D.; Phillips, Ingrid S.; Kopp, Richard F.
  • BioEnergy Research, Vol. 1, Issue 1
  • DOI: 10.1007/s12155-008-9006-x

Compensatory cis-trans Evolution and the Dysregulation of Gene Expression in Interspecific Hybrids of Drosophila
journal, September 2005


Transcriptional analysis of nucleolar dominance in polyploid plants: Biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica
journal, April 1997

  • Chen, Z. J.; Pikaard, C. S.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 7
  • DOI: 10.1073/pnas.94.7.3442

The quantitative genetics of sexual dimorphism: assessing the importance of sex-linkage
journal, August 2006


The roles of cis- and trans-regulation in the evolution of regulatory incompatibilities and sexually dimorphic gene expression
journal, September 2013

  • Meiklejohn, C. D.; Coolon, J. D.; Hartl, D. L.
  • Genome Research, Vol. 24, Issue 1
  • DOI: 10.1101/gr.156414.113

Comparative interrogation of the developing xylem transcriptomes of two wood-forming species: Populus trichocarpa and Eucalyptus grandis
journal, February 2015

  • Hefer, Charles A.; Mizrachi, Eshchar; Myburg, Alexander A.
  • New Phytologist, Vol. 206, Issue 4
  • DOI: 10.1111/nph.13277

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

Global RNA sequencing reveals that genotype-dependent allele-specific expression contributes to differential expression in rice F1 hybrids
journal, January 2013


The Fasciclin-Like Arabinogalactan Proteins of Arabidopsis. A Multigene Family of Putative Cell Adhesion Molecules
journal, November 2003

  • Johnson, Kim L.; Jones, Brian J.; Bacic, Antony
  • Plant Physiology, Vol. 133, Issue 4
  • DOI: 10.1104/pp.103.031237

Differential expression of genes encoding phosphate transporters contributes to arsenic tolerance and accumulation in shrub willow (Salix spp.)
journal, January 2012


Identification of imprinted genes subject to parent-of-origin specific expression in Arabidopsis thaliana seeds
journal, January 2011

  • McKeown, Peter C.; Laouielle-Duprat, Sylvia; Prins, Pjotr
  • BMC Plant Biology, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2229-11-113

Intra-Specific Regulatory Variation in Drosophila pseudoobscura
journal, December 2013


A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011

  • DePristo, Mark A.; Banks, Eric; Poplin, Ryan
  • Nature Genetics, Vol. 43, Issue 5
  • DOI: 10.1038/ng.806

Genetic strategies for dissecting complex traits in biomass willows (Salix spp.)
journal, November 2013


The development of improved willow clones for eastern North America
journal, April 2001

  • Kopp, R. F.; Smart, L. B.; Maynard, C. A.
  • The Forestry Chronicle, Vol. 77, Issue 2
  • DOI: 10.5558/tfc77287-2

Evolutionary changes in cis and trans gene regulation
journal, July 2004

  • Wittkopp, Patricia J.; Haerum, Belinda K.; Clark, Andrew G.
  • Nature, Vol. 430, Issue 6995
  • DOI: 10.1038/nature02698

Sexually antagonistic genes: experimental evidence
journal, June 1992


Correlations of expression of cell wall biosynthesis genes with variation in biomass composition in shrub willow (Salix spp.) biomass crops
journal, December 2011

  • Serapiglia, Michelle J.; Cameron, Kimberly D.; Stipanovic, Arthur J.
  • Tree Genetics & Genomes, Vol. 8, Issue 4
  • DOI: 10.1007/s11295-011-0462-7

Poplar genes encoding fasciclin-like arabinogalactan proteins are highly expressed in tension wood
journal, September 2004


Regulatory divergence in Drosophila revealed by mRNA-seq
journal, March 2010

  • McManus, C. J.; Coolon, J. D.; Duff, M. O.
  • Genome Research, Vol. 20, Issue 6
  • DOI: 10.1101/gr.102491.109

What causes female bias in the secondary sex ratios of the dioecious woody shrub Salix sitchensis colonizing a primary successional landscape?
journal, August 2015

  • Che-Castaldo, Christian; Crisafulli, Charlie M.; Bishop, John G.
  • American Journal of Botany, Vol. 102, Issue 8
  • DOI: 10.3732/ajb.1500143

Major Chromosomal Rearrangements Distinguish Willow and Poplar After the Ancestral “Salicoid” Genome Duplication
journal, June 2016

  • Hou, Jing; Ye, Ning; Dong, Zhongyuan
  • Genome Biology and Evolution, Vol. 8, Issue 6
  • DOI: 10.1093/gbe/evw127

Regulatory changes underlying expression differences within and between Drosophila species
journal, February 2008

  • Wittkopp, Patricia J.; Haerum, Belinda K.; Clark, Andrew G.
  • Nature Genetics, Vol. 40, Issue 3
  • DOI: 10.1038/ng.77

edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009


Sex-Specific Effects of Cis -Regulatory Variants in Drosophila melanogaster
journal, October 2013


Nonadditive Expression and Parent-of-Origin Effects Identified by Microarray and Allele-Specific Expression Profiling of Maize Endosperm
journal, August 2007

  • Stupar, Robert M.; Hermanson, Peter J.; Springer, Nathan M.
  • Plant Physiology, Vol. 145, Issue 2
  • DOI: 10.1104/pp.107.101428

A Y-chromosome-encoded small RNA acts as a sex determinant in persimmons
journal, October 2014


Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids
journal, January 2012

  • Shi, Xiaoli; Ng, Danny W-K.; Zhang, Changqing
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms1954

The evolutionary causes and consequences of sex-biased gene expression
journal, January 2013

  • Parsch, John; Ellegren, Hans
  • Nature Reviews Genetics, Vol. 14, Issue 2
  • DOI: 10.1038/nrg3376

Independent Effects of cis - and trans -regulatory Variation on Gene Expression in Drosophila melanogaster
journal, February 2008


Infrageneric Classification of Salix (Salicaceae) in the New World
journal, January 1997


Recent Y chromosome divergence despite ancient origin of dioecy in poplars ( Populus )
journal, April 2015

  • Geraldes, A.; Hefer, C. A.; Capron, A.
  • Molecular Ecology, Vol. 24, Issue 13
  • DOI: 10.1111/mec.13126

Genome structure and emerging evidence of an incipient sex chromosome in Populus
journal, February 2008

  • Yin, T.; DiFazio, S. P.; Gunter, L. E.
  • Genome Research, Vol. 18, Issue 3
  • DOI: 10.1101/gr.7076308

The obscure events contributing to the evolution of an incipient sex chromosome in Populus: a retrospective working hypothesis
journal, March 2012

  • Tuskan, Gerald A.; DiFazio, Steve; Faivre-Rampant, Patricia
  • Tree Genetics & Genomes, Vol. 8, Issue 3
  • DOI: 10.1007/s11295-012-0495-6

BRR2a Affects Flowering Time via FLC Splicing
journal, April 2016


Confirmation of Single-Locus Sex Determination and Female Heterogamety in Willow Based on Linkage Analysis
journal, February 2016


β-Galactosyl Yariv Reagent Binds to the β-1,3-Galactan of Arabinogalactan Proteins
journal, January 2013

  • Kitazawa, Kiminari; Tryfona, Theodora; Yoshimi, Yoshihisa
  • Plant Physiology, Vol. 161, Issue 3
  • DOI: 10.1104/pp.112.211722

Allele-Specific Expression Patterns Reveal Biases and Embryo-Specific Parent-of-Origin Effects in Hybrid Maize
journal, August 2007


Sexual homomorphism in dioecious trees: extensive tests fail to detect sexual dimorphism in Populus
journal, May 2017


Electrical Capacitance as a Predictor of Root Dry Weight in Shrub Willow ( Salix ; Salicaceae) Parents and Progeny
journal, August 2016

  • Carlson, Craig H.; Smart, Lawrence B.
  • Applications in Plant Sciences, Vol. 4, Issue 8
  • DOI: 10.3732/apps.1600031

Single locus sex determination and female heterogamety in the basket willow (Salix viminalis L.)
journal, February 2015

  • Pucholt, P.; Rönnberg-Wästljung, A-C; Berlin, S.
  • Heredity, Vol. 114, Issue 6
  • DOI: 10.1038/hdy.2014.125

AtREM1 , a Member of a New Family of B3 Domain-Containing Genes, Is Preferentially Expressed in Reproductive Meristems
journal, February 2002

  • Franco-Zorrilla, José M.; Cubas, Pilar; Jarillo, José A.
  • Plant Physiology, Vol. 128, Issue 2
  • DOI: 10.1104/pp.010323

A Multigenic Network of ARGONAUTE4 Clade Members Controls Early Megaspore Formation in Arabidopsis
journal, September 2016


MYB transcription factor gene involved in sex determination in Asparagus officinalis
journal, November 2016

  • Murase, Kohji; Shigenobu, Shuji; Fujii, Sota
  • Genes to Cells, Vol. 22, Issue 1
  • DOI: 10.1111/gtc.12453

Brassinosteroid control of sex determination in maize
journal, November 2011

  • Hartwig, T.; Chuck, G. S.; Fujioka, S.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 49
  • DOI: 10.1073/pnas.1108359108

NUCLEAR FACTOR Y, Subunit A (NF-YA) Proteins Positively Regulate Flowering and Act Through FLOWERING LOCUS T
journal, December 2016


Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies
journal, February 2014

  • Xu, Chunming; Bai, Yan; Lin, Xiuyun
  • Molecular Biology and Evolution, Vol. 31, Issue 5
  • DOI: 10.1093/molbev/msu085

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