Characterization of a large sex determination region in Salix purpurea L. (Salicaceae)
Abstract
Dioecy has evolved numerous times in plants, but heteromorphic sex chromosomes are apparently rare. Sex determination has been studied in multiple Salix and Populus (Salicaceae) species, and P. trichocarpa has an XY sex determination system on chromosome 19, while S. suchowensis and S. viminalis have a ZW system on chromosome 15. Here we use whole genome sequencing coupled with quantitative trait locus mapping and a genome-wide association study to characterize the genomic composition of the non-recombining portion of the sex determination region. We demonstrate that Salix purpurea also has a ZW system on chromosome 15. The sex determination region has reduced recombination, high structural polymorphism, an abundance of transposable elements, and contains genes that are involved in sex expression in other plants. We also show that chromosome 19 contains sex-associated markers in this S. purpurea assembly, along with other autosomes. This raises the intriguing possibility of a translocation of the sex determination region within the Salicaceae lineage, suggesting a common evolutionary origin of the Populus and Salix sex determination loci.
- Authors:
-
[6];
[1]
- West Virginia Univ., Morgantown, WV (United States). Dept. of Biology
- Cornell Univ., Geneva, NY (United States). School of Integrative Plant Science, New York State Agricultural Experiment Station, Horticulture Section
- HudsonAlpha Inst. of Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- HudsonAlpha Inst. of Biotechnology, Huntsville, AL (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA; National Science Foundation (NSF)
- OSTI Identifier:
- 1494877
- Alternate Identifier(s):
- OSTI ID: 1619108
- Grant/Contract Number:
- AC05-00OR22725; 4705-630 WVU-USDA-9703; DEB-1542509
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Genetics and Genomics
- Additional Journal Information:
- Journal Volume: 293; Journal Issue: 6; Journal ID: ISSN 1617-4615
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Sex; Salix; Genome; Suppressed recombination; Dioecy
Citation Formats
Zhou, Ran, Macaya-Sanz, David, Rodgers-Melnick, Eli, Carlson, Craig H., Gouker, Fred E., Evans, Luke M., Schmutz, Jeremy, Jenkins, Jerry W., Yan, Juying, Tuskan, Gerald A., Smart, Lawrence B., and DiFazio, Stephen P. Characterization of a large sex determination region in Salix purpurea L. (Salicaceae). United States: N. p., 2018.
Web. doi:10.1007/s00438-018-1473-y.
Zhou, Ran, Macaya-Sanz, David, Rodgers-Melnick, Eli, Carlson, Craig H., Gouker, Fred E., Evans, Luke M., Schmutz, Jeremy, Jenkins, Jerry W., Yan, Juying, Tuskan, Gerald A., Smart, Lawrence B., & DiFazio, Stephen P. Characterization of a large sex determination region in Salix purpurea L. (Salicaceae). United States. doi:https://doi.org/10.1007/s00438-018-1473-y
Zhou, Ran, Macaya-Sanz, David, Rodgers-Melnick, Eli, Carlson, Craig H., Gouker, Fred E., Evans, Luke M., Schmutz, Jeremy, Jenkins, Jerry W., Yan, Juying, Tuskan, Gerald A., Smart, Lawrence B., and DiFazio, Stephen P. Wed .
"Characterization of a large sex determination region in Salix purpurea L. (Salicaceae)". United States. doi:https://doi.org/10.1007/s00438-018-1473-y. https://www.osti.gov/servlets/purl/1494877.
@article{osti_1494877,
title = {Characterization of a large sex determination region in Salix purpurea L. (Salicaceae)},
author = {Zhou, Ran and Macaya-Sanz, David and Rodgers-Melnick, Eli and Carlson, Craig H. and Gouker, Fred E. and Evans, Luke M. and Schmutz, Jeremy and Jenkins, Jerry W. and Yan, Juying and Tuskan, Gerald A. and Smart, Lawrence B. and DiFazio, Stephen P.},
abstractNote = {Dioecy has evolved numerous times in plants, but heteromorphic sex chromosomes are apparently rare. Sex determination has been studied in multiple Salix and Populus (Salicaceae) species, and P. trichocarpa has an XY sex determination system on chromosome 19, while S. suchowensis and S. viminalis have a ZW system on chromosome 15. Here we use whole genome sequencing coupled with quantitative trait locus mapping and a genome-wide association study to characterize the genomic composition of the non-recombining portion of the sex determination region. We demonstrate that Salix purpurea also has a ZW system on chromosome 15. The sex determination region has reduced recombination, high structural polymorphism, an abundance of transposable elements, and contains genes that are involved in sex expression in other plants. We also show that chromosome 19 contains sex-associated markers in this S. purpurea assembly, along with other autosomes. This raises the intriguing possibility of a translocation of the sex determination region within the Salicaceae lineage, suggesting a common evolutionary origin of the Populus and Salix sex determination loci.},
doi = {10.1007/s00438-018-1473-y},
journal = {Molecular Genetics and Genomics},
number = 6,
volume = 293,
place = {United States},
year = {2018},
month = {7}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 14 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Evolutionary Strata on the X Chromosomes of the Dioecious Plant Silene latifolia : Evidence From New Sex-Linked Genes
journal, February 2007
- Bergero, Roberta; Forrest, Alan; Kamau, Esther
- Genetics, Vol. 175, Issue 4
Argot2: a large scale function prediction tool relying on semantic similarity of weighted Gene Ontology terms
journal, March 2012
- Falda, Marco; Toppo, Stefano; Pescarolo, Alessandro
- BMC Bioinformatics, Vol. 13, Issue S4
What makes the sex ratio female-biased in the dioecious tree Salix sachalinensis?
journal, September 2007
- Ueno, Naoto; Suyama, Yoshihisa; Seiwa, Kenji
- Journal of Ecology, Vol. 95, Issue 5
Inter- and Intraspecific Variation in Floral Scent in the Genus Salix and its Implication for Pollination
journal, March 2007
- Füssel, Ulrike; Dötterl, Stefan; Jürgens, Andreas
- Journal of Chemical Ecology, Vol. 33, Issue 4
A Complete and Accurate Short Sequence Alignment Algorithm for Repeats
journal, January 2016
- Lian, Shuaibin; Liu, Tianliang; Gong, Ke
- Journal of Biosciences and Medicines, Vol. 04, Issue 12
Variance component model to account for sample structure in genome-wide association studies
journal, March 2010
- Kang, Hyun Min; Sul, Jae Hoon; Service, Susan K.
- Nature Genetics, Vol. 42, Issue 4
A Gradual Process of Recombination Restriction in the Evolutionary History of the Sex Chromosomes in Dioecious Plants
journal, December 2004
- Nicolas, Michael; Marais, Gabriel; Hykelova, Vladka
- PLoS Biology, Vol. 3, Issue 1
TASSEL-GBS: A High Capacity Genotyping by Sequencing Analysis Pipeline
journal, February 2014
- Glaubitz, Jeffrey C.; Casstevens, Terry M.; Lu, Fei
- PLoS ONE, Vol. 9, Issue 2
Evolution towards dioecy in heterostylous populations
journal, January 1979
- Lloyd, David G.
- Plant Systematics and Evolution, Vol. 131, Issue 1-2
Demographic Studies of a Dioecious Tree. I. Colonization, Sex and Age Structure of a Population of Salix Cinerea
journal, December 1989
- Alliende, M. C.; Harper, J. L.
- The Journal of Ecology, Vol. 77, Issue 4
Sex Determination: Why So Many Ways of Doing It?
journal, July 2014
- Bachtrog, Doris; Mank, Judith E.; Peichel, Catherine L.
- PLoS Biology, Vol. 12, Issue 7
The sex-linked region in Populus tremuloides Turesson 141 corresponds to a pericentromeric region of about two million base pairs on P. trichocarpa chromosome 19
journal, May 2013
- Kersten, B.; Pakull, B.; Groppe, K.
- Plant Biology, Vol. 16, Issue 2
Deciphering evolutionary strata on plant sex chromosomes and fungal mating-type chromosomes through compositional segmentation
journal, December 2015
- Pandey, Ravi S.; Azad, Rajeev K.
- Plant Molecular Biology, Vol. 90, Issue 4-5
Transitions Between Male and Female Heterogamety Caused by Sex-Antagonistic Selection
journal, July 2010
- van Doorn, G. Sander; Kirkpatrick, Mark
- Genetics, Vol. 186, Issue 2
Plant Sex Chromosomes
journal, April 2016
- Charlesworth, Deborah
- Annual Review of Plant Biology, Vol. 67, Issue 1
Sex Chromosomes and the Evolution of Sexual Dimorphism: Lessons from the Genome
journal, February 2009
- Mank, Judith E.
- The American Naturalist, Vol. 173, Issue 2
Different autosomes evolved into sex chromosomes in the sister genera of Salix and Populus
journal, March 2015
- Hou, Jing; Ye, Ning; Zhang, Defang
- Scientific Reports, Vol. 5, Issue 1
Widespread Triploidy in Western North American Aspen (Populus tremuloides)
journal, October 2012
- Mock, Karen E.; Callahan, Colin M.; Islam-Faridi, M. Nurul
- PLoS ONE, Vol. 7, Issue 10
Identification of a RAPD marker linked to sex determination in the basket willow (Salix viminalis L.)
journal, January 1998
- Alstrom-Rapaport, C.
- Journal of Heredity, Vol. 89, Issue 1
MutS2 Promotes Homologous Recombination in Bacillus subtilis
journal, October 2016
- Burby, Peter E.; Simmons, Lyle A.
- Journal of Bacteriology, Vol. 199, Issue 2
High-quality draft assemblies of mammalian genomes from massively parallel sequence data
journal, December 2010
- Gnerre, S.; MacCallum, I.; Przybylski, D.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 4
The relative and absolute frequencies of angiosperm sexual systems: Dioecy, monoecy, gynodioecy, and an updated online database
journal, October 2014
- Renner, Susanne S.
- American Journal of Botany, Vol. 101, Issue 10
Dna Mismatch Repair
journal, June 2005
- Kunkel, Thomas A.; Erie, Dorothy A.
- Annual Review of Biochemistry, Vol. 74, Issue 1
Evolution of Plant Breeding Systems
journal, September 2006
- Charlesworth, Deborah
- Current Biology, Vol. 16, Issue 17
Sex Chromosomes and the Evolution of Sexual Dimorphism
journal, July 1984
- Rice, William R.
- Evolution, Vol. 38, Issue 4
An extinct genus of Salicaceae based on twigs with attached flowers, fruits, and foliage from the Eocene Green River Formation of Utah and Colorado, USA
journal, September 2003
- Boucher, Lisa D.; Manchester, Steven R.; Judd, Walter S.
- American Journal of Botany, Vol. 90, Issue 9
Detection of genomic variations and DNA polymorphisms and impact on analysis of meiotic recombination and genetic mapping
journal, June 2014
- Qi, Ji; Chen, Yamao; Copenhaver, Gregory P.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
PPR-SMR protein SOT1 has RNA endonuclease activity
journal, February 2017
- Zhou, Wen; Lu, Qingtao; Li, Qingwei
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 8
Principal components analysis corrects for stratification in genome-wide association studies
journal, July 2006
- Price, Alkes L.; Patterson, Nick J.; Plenge, Robert M.
- Nature Genetics, Vol. 38, Issue 8
Phytozome: a comparative platform for green plant genomics
journal, November 2011
- Goodstein, David M.; Shu, Shengqiang; Howson, Russell
- Nucleic Acids Research, Vol. 40, Issue D1
Changes in the heterogametic mechanism of sex determination
journal, August 1977
- Bull, James J.; Charnov, Eric L.
- Heredity, Vol. 39, Issue 1
Genomics of sex chromosomes
journal, April 2007
- Ming, R.; Moore, P.
- Current Opinion in Plant Biology, Vol. 10, Issue 2
Genetic linkage mapping in aspen (Populus tremula L. and Populus tremuloides Michx.)
journal, April 2009
- Pakull, Birte; Groppe, Katrin; Meyer, Matthias
- Tree Genetics & Genomes, Vol. 5, Issue 3
Population genetics of partial male-sterility and the evolution of monoecy and dioecy
journal, October 1978
- Charlesworth, D.; Charlesworth, B.
- Heredity, Vol. 41, Issue 2
Ploidy Level Affects Important Biomass Traits of Novel Shrub Willow (Salix) Hybrids
journal, August 2014
- Serapiglia, Michelle J.; Gouker, Fred E.; Hart, J. Foster
- BioEnergy Research, Vol. 8, Issue 1
Turnover of sex chromosomes induced by sexual conflict
journal, October 2007
- van Doorn, G. S.; Kirkpatrick, M.
- Nature, Vol. 449, Issue 7164
In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning
journal, November 2011
- Greco, Maria; Chiappetta, Adriana; Bruno, Leonardo
- Journal of Experimental Botany, Vol. 63, Issue 2
Dominance and Sexual Dimorphism Pervade the Salix purpurea L. Transcriptome
journal, September 2017
- Carlson, Craig H.; Choi, Yongwook; Chan, Agnes P.
- Genome Biology and Evolution, Vol. 9, Issue 9
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
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
The evolution of restricted recombination in sex chromosomes
journal, February 2009
- Bergero, Roberta; Charlesworth, Deborah
- Trends in Ecology & Evolution, Vol. 24, Issue 2
Nuclease activity of the MutS homologue MutS2 from Thermus thermophilus is confined to the Smr domain
journal, January 2007
- Fukui, K.; Kosaka, H.; Kuramitsu, S.
- Nucleic Acids Research, Vol. 35, Issue 3
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
Genetic linkage maps of Populus alba L. and comparative mapping analysis of sex determination across Populus species
journal, June 2010
- Paolucci, Isabella; Gaudet, Muriel; Jorge, Véronique
- Tree Genetics & Genomes, Vol. 6, Issue 6
Polygenic sex determination
journal, June 2013
- Moore, Emily C.; Roberts, Reade B.
- Current Biology, Vol. 23, Issue 12
Revisiting the Dioecy-Polyploidy Association: Alternate Pathways and Research Opportunities
journal, January 2013
- Ashman, T. -L.; Kwok, A.; Husband, B. C.
- Cytogenetic and Genome Research, Vol. 140, Issue 2-4
A simple PCR-based marker to determine sex in aspen
journal, June 2014
- Pakull, B.; Kersten, B.; Lüneburg, J.
- Plant Biology, Vol. 17, Issue 1
Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution
journal, January 2013
- Melters, Daniël P.; Bradnam, Keith R.; Young, Hugh A.
- Genome Biology, Vol. 14, Issue 1
Sequence characterization of the putatively sex-linked Ssu72 -like locus in willow and its homologue in poplarThis note is one of a selection of papers published in the Special Issue on Poplar Research in Canada.
journal, November 2007
- Temmel, Nyssa A.; Rai, Hardeep S.; Cronk, Quentin C. B.
- Canadian Journal of Botany, Vol. 85, Issue 11
The genomics of plant sex chromosomes
journal, July 2015
- Vyskot, Boris; Hobza, Roman
- Plant Science, Vol. 236
Polyploidy and sexual system in angiosperms: Is there an association?
journal, June 2016
- Glick, Lior; Sabath, Niv; Ashman, Tia-Lynn
- American Journal of Botany, Vol. 103, Issue 7
Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants
journal, December 2012
- Lin, H.; Niu, L.; McHale, N. A.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 1
Infrageneric Classification of Salix (Salicaceae) in the New World
journal, January 1997
- Argus, George W.
- Systematic Botany Monographs, Vol. 52
Recent Sex Chromosome Divergence despite Ancient Dioecy in the Willow Salix viminalis
journal, April 2017
- Pucholt, Pascal; Wright, Alison E.; Conze, Lei Liu
- Molecular Biology and Evolution, Vol. 34, Issue 8
Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait
journal, February 2007
- Gaudet, M.; Jorge, V.; Paolucci, I.
- Tree Genetics & Genomes, Vol. 4, Issue 1
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
Expansion of the Cell Plate in Plant Cytokinesis Requires a Kinesin-like Protein/MAPKKK Complex
journal, April 2002
- Nishihama, Ryuichi; Soyano, Takashi; Ishikawa, Masaki
- Cell, Vol. 109, Issue 1
Boys and Girls Come Out to Play: The Molecular Biology of Dioecious Plants
journal, August 2000
- Ainsworth, C.
- Annals of Botany, Vol. 86, Issue 2
Sex Chromosomes in Land Plants
journal, June 2011
- Ming, Ray; Bendahmane, Abdelhafid; Renner, Susanne S.
- Annual Review of Plant Biology, Vol. 62, Issue 1
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
Organelle motility in the pollen tube: a tale of 20 years
journal, January 2009
- Cai, G.; Cresti, M.
- Journal of Experimental Botany, Vol. 60, Issue 2
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
Structure and Function of the Small MutS-Related Domain
journal, January 2011
- Fukui, Kenji; Kuramitsu, Seiki
- Molecular Biology International, Vol. 2011
About PAR: The distinct evolutionary dynamics of the pseudoautosomal region
journal, September 2011
- Otto, Sarah P.; Pannell, John R.; Peichel, Catherine L.
- Trends in Genetics, Vol. 27, Issue 9
Confirmation of Single-Locus Sex Determination and Female Heterogamety in Willow Based on Linkage Analysis
journal, February 2016
- Chen, Yingnan; Wang, Tiantian; Fang, Lecheng
- PLOS ONE, Vol. 11, Issue 2
R/qtl: high-throughput multiple QTL mapping: Fig. 1.
journal, October 2010
- Arends, Danny; Prins, Pjotr; Jansen, Ritsert C.
- Bioinformatics, Vol. 26, Issue 23
Assembly algorithms for next-generation sequencing data
journal, June 2010
- Miller, Jason R.; Koren, Sergey; Sutton, Granger
- Genomics, Vol. 95, Issue 6
A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species
journal, May 2011
- Elshire, Robert J.; Glaubitz, Jeffrey C.; Sun, Qi
- PLoS ONE, Vol. 6, Issue 5, Article No. e19379
Genetic Improvement of Willow for Bioenergy and BiofuelsFree Access
journal, January 2011
- Karp, Angela; Hanley, Steve J.; Trybush, Sviatlana O.
- Journal of Integrative Plant Biology, Vol. 53, Issue 2
PAML 4: Phylogenetic Analysis by Maximum Likelihood
journal, April 2007
- Yang, Z.
- Molecular Biology and Evolution, Vol. 24, Issue 8
Plant contributions to our understanding of sex chromosome evolution
journal, June 2015
- Charlesworth, Deborah
- New Phytologist, Vol. 208, Issue 1
EST data suggest that poplar is an ancient polyploid
journal, March 2005
- Sterck, Lieven; Rombauts, Stephane; Jansson, Stefan
- New Phytologist, Vol. 167, Issue 1
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
Allelic incompatibility can explain female biased sex ratios in dioecious plants
journal, March 2017
- Pucholt, Pascal; Hallingbäck, Henrik R.; Berlin, Sofia
- BMC Genomics, Vol. 18, Issue 1
Harnessing the power of RADseq for ecological and evolutionary genomics
journal, January 2016
- Andrews, Kimberly R.; Good, Jeffrey M.; Miller, Michael R.
- Nature Reviews Genetics, Vol. 17, Issue 2
Sex Chromosomes and the Evolution of Sexual Dimorphism
journal, July 1984
- Rice, William R.
- Evolution, Vol. 38, Issue 4
Works referencing / citing this record:
Genetic variation of biomass recalcitrance in a natural Salix viminalis (L.) population
journal, June 2019
- Ohlsson, Jonas A.; Hallingbäck, Henrik R.; Jebrane, Mohamed
- Biotechnology for Biofuels, Vol. 12, Issue 1
Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion
journal, June 2020
- Almeida, Pedro; Proux-Wera, Estelle; Churcher, Allison
- BMC Biology, Vol. 18, Issue 1
Genetic variation of biomass recalcitrance in a natural Salix viminalis (L.) population
journal, June 2019
- Ohlsson, Jonas A.; Hallingbäck, Henrik R.; Jebrane, Mohamed
- Biotechnology for Biofuels, Vol. 12, Issue 1
Plant sex influences aquatic–terrestrial interactions
journal, January 2020
- LeRoy, Carri J.; Ramstack Hobbs, Joy M.; Claeson, Shannon M.
- Ecosphere, Vol. 11, Issue 1
Genetic diversity and population structure of native, naturalized, and cultivated Salix purpurea
journal, May 2019
- Gouker, Fred E.; DiFazio, Stephen P.; Bubner, Ben
- Tree Genetics & Genomes, Vol. 15, Issue 3
Uneven selection pressure accelerating divergence of Populus and Salix
journal, April 2019
- Hou, Jing; Wei, Suyun; Pan, Huixin
- Horticulture Research, Vol. 6, Issue 1
Genome-wide analysis of Cushion willow provides insights into alpine plant divergence in a biodiversity hotspot
journal, November 2019
- Chen, Jia-hui; Huang, Yuan; Brachi, Benjamin
- Nature Communications, Vol. 10, Issue 1
Evolution of sex determination and heterogamety changes in section Otites of the genus Silene
journal, January 2019
- Balounova, Veronika; Gogela, Roman; Cegan, Radim
- Scientific Reports, Vol. 9, Issue 1
Joint linkage and association mapping of complex traits in shrub willow (Salix purpurea L.)
journal, April 2019
- Carlson, Craig H.; Gouker, Fred E.; Crowell, Chase R.
- Annals of Botany, Vol. 124, Issue 4
Phylogenomics of the genus Populus reveals extensive interspecific gene flow and balancing selection
journal, October 2019
- Wang, Mingcheng; Zhang, Lei; Zhang, Zhiyang
- New Phytologist, Vol. 225, Issue 3
A willow sex chromosome reveals convergent evolution of complex palindromic repeats
journal, February 2020
- Zhou, Ran; Macaya-Sanz, David; Carlson, Craig H.
- Genome Biology, Vol. 21, Issue 1
Genome Wide Associations of Growth, Phenology, and Plasticity Traits in Willow [Salix viminalis (L.)]
journal, June 2019
- Hallingbäck, Henrik R.; Berlin, Sofia; Nordh, Nils-Erik
- Frontiers in Plant Science, Vol. 10