The flying spider-monkey tree fern genome provides insights into fern evolution and arborescence

Huang, Xiong; Wang, Wenling; Gong, Ting; Wickell, David; Kuo, Li-Yaung; Zhang, Xingtan; Wen, Jialong; Kim, Hoon; Lu, Fachuang; Zhao, Hansheng; Chen, Song; Li, Hui; Wu, Wenqi; Yu, Changjiang; Chen, Su; Fan, Wei; Chen, Shuai; Bao, Xiuqi; Li, Li; Zhang, Dan; Jiang, Longyu; Yan, Xiaojing; Liao, Zhenyang; Zhou, Gongke; Guo, Yalong; Ralph, John; Sederoff, Ronald R.; Wei, Hairong; Zhu, Ping; Li, Fay-Wei; Ming, Ray; Li, Quanzi

doi:10.1038/s41477-022-01146-6

Title: The flying spider-monkey tree fern genome provides insights into fern evolution and arborescence

Journal Article · 09 May 2022 · Nature Plants (Online)

DOI: https://doi.org/10.1038/s41477-022-01146-6 · OSTI ID:1876025

Huang, Xiong ^[1]; Wang, Wenling ^[2];

^[3]; Wickell, David ^[4]; Kuo, Li-Yaung ^[5]; Zhang, Xingtan ^[2]; Wen, Jialong ^[6];

^[7];

^[8];

^[9]; Li, Hui ^[10]; Wu, Wenqi ^[6]; Yu, Changjiang ^[11]; Chen, Su ^[9]; Fan, Wei ^[10]; Chen, Shuai ^[2]; Bao, Xiuqi ^[3];

^[3]; Zhang, Dan ^[3] more »

Chinese Academy of Forestry, Beijing (China); University of Illinois at Urbana-Champaign Department of Plant Biology
Chinese Academy of Agricultural Sciences, Shenzhen (China)
Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing (China)
Thompson Inst., Ithaca, NY (United States); Cornell Univ., Ithaca, NY (United States)
National Tsing Hua Univ., Hsinchu (Taiwan)
Beijing Forestry Univ. (China)
Univ. of Wisconsin, Madison, WI (United States)
International Center for Bamboo and Rattan, Beijing (China)
Northeast Forestry Univ., Harbin (China)
Chinese Academy of Forestry, Beijing (China)
Qingdao Agricultural Univ. (China)
Chinese Academy of Sciences (CAS), Beijing (China)
North Carolina State Univ., Raleigh, NC (United States)
Michigan Technological Univ., Houghton, MI (United States)
Univ. of Illinois at Urbana-Champaign, IL (United States)

To date, little is known about the evolution of fern genomes, with only two small genomes published from the heterosporous Salviniales. Here we assembled the genome of Alsophila spinulosa, known as the flying spider-monkey tree fern, onto 69 pseudochromosomes. The remarkable preservation of synteny, despite resulting from an ancient whole-genome duplication over 100 million years ago, is unprecedented in plants and probably speaks to the uniqueness of tree ferns. Our detailed investigations into stem anatomy and lignin biosynthesis shed new light on the evolution of stem formation in tree ferns. We identified a phenolic compound, alsophilin, that is abundant in xylem, and we provided the molecular basis for its biosynthesis. Finally, analysis of demographic history revealed two genetic bottlenecks, resulting in rapid demographic declines of A. spinulosa. The A. spinulosa genome fills a crucial gap in the plant genomic landscape and helps elucidate many unique aspects of tree fern biology.

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Research Organization:: Great Lakes Bioenergy Research Center, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); Fundamental Research Funds of Chinese Academy of Forestry; CAMS Innovation Fund for Medical Sciences; PUMC Disciplinary Development of Synthetic Biology

Grant/Contract Number:: SC0018409

OSTI ID:: 1876025

Journal Information:: Nature Plants (Online), Journal Name: Nature Plants (Online) Journal Issue: 5 Vol. 8; ISSN 2055-0278

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (115)

Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences Tarailo‐Graovac, Maja; Chen, Nansheng Current Protocols in Bioinformatics, Vol. 25, Issue 1 https://doi.org/10.1002/0471250953.bi0410s25	journal	March 2009
Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components Porebski, Sue; Bailey, L. Grant; Baum, Bernard R. Plant Molecular Biology Reporter, Vol. 15, Issue 1 https://doi.org/10.1007/BF02772108	journal	March 1997
New insights into the molecular architecture of hardwood lignins by chemical degradative methods Lapierre, Catherine; Pollet, Brigitte; Rolando, Christian Research on Chemical Intermediates, Vol. 21, Issue 3-5, p. 397-412 https://doi.org/10.1007/BF03052266	journal	March 1995
GCTA: A Tool for Genome-wide Complex Trait Analysis Yang, Jian; Lee, S. Hong; Goddard, Michael E. The American Journal of Human Genetics, Vol. 88, Issue 1 https://doi.org/10.1016/j.ajhg.2010.11.011	journal	January 2011
Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome Bowman, John L.; Kohchi, Takayuki; Yamato, Katsuyuki T. Cell, Vol. 171, Issue 2 https://doi.org/10.1016/j.cell.2017.09.030	journal	October 2017
The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization Nishiyama, Tomoaki; Sakayama, Hidetoshi; de Vries, Jan Cell, Vol. 174, Issue 2 https://doi.org/10.1016/j.cell.2018.06.033	journal	July 2018
Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments Durand, Neva C.; Shamim, Muhammad S.; Machol, Ido Cell Systems, Vol. 3, Issue 1 https://doi.org/10.1016/j.cels.2016.07.002	journal	July 2016
The Evolutionary Origin of a Terrestrial Flora Delwiche, Charles Francis; Cooper, Endymion Dante Current Biology, Vol. 25, Issue 19 https://doi.org/10.1016/j.cub.2015.08.029	journal	October 2015
De Novo Plant Genome Assembly Based on Chromatin Interactions: A Case Study of Arabidopsis thaliana Xie, Ting; Zheng, Jue-Fei; Liu, Sheng Molecular Plant, Vol. 8, Issue 3 https://doi.org/10.1016/j.molp.2014.12.015	journal	March 2015
Genome Analysis of the Ancient Tracheophyte Selaginella tamariscina Reveals Evolutionary Features Relevant to the Acquisition of Desiccation Tolerance Xu, Zhichao; Xin, Tianyi; Bartels, Dorothea Molecular Plant, Vol. 11, Issue 7 https://doi.org/10.1016/j.molp.2018.05.003	journal	July 2018
Evolution of the mutation rate Lynch, Michael Trends in Genetics, Vol. 26, Issue 8 https://doi.org/10.1016/j.tig.2010.05.003	journal	August 2010
A 4000-species dataset provides new insight into the evolution of ferns Testo, Weston; Sundue, Michael Molecular Phylogenetics and Evolution, Vol. 105 https://doi.org/10.1016/j.ympev.2016.09.003	journal	December 2016
A well-resolved fern nuclear phylogeny reveals the evolution history of numerous transcription factor families Qi, Xinping; Kuo, Li-Yaung; Guo, Chunce Molecular Phylogenetics and Evolution, Vol. 127 https://doi.org/10.1016/j.ympev.2018.06.043	journal	October 2018
Nuclear loci developed from multiple transcriptomes yield high resolution in phylogeny of scaly tree ferns (Cyatheaceae) from China and Vietnam Dong, Shiyong; Xiao, Yong; Kong, Hanghui Molecular Phylogenetics and Evolution, Vol. 139 https://doi.org/10.1016/j.ympev.2019.106567	journal	October 2019
Chemical and Spatial Differentiation of Syringyl and Guaiacyl Lignins in Poplar Wood via Time-of-Flight Secondary Ion Mass Spectrometry Zhou, Chuanzhen; Li, Quanzi; Chiang, Vincent L. Analytical Chemistry, Vol. 83, Issue 18 https://doi.org/10.1021/ac200903y	journal	September 2011
Chemical Characterization of Klason Lignin Preparations from Plant-Based Foods Bunzel, Mirko; Schüßler, Anne; Tchetseubu Saha, Gérard Journal of Agricultural and Food Chemistry, Vol. 59, Issue 23 https://doi.org/10.1021/jf2031378	journal	December 2011
Single-molecule sequencing of the desiccation-tolerant grass Oropetium thomaeum VanBuren, Robert; Bryant, Doug; Edger, Patrick P. Nature, Vol. 527, Issue 7579 https://doi.org/10.1038/nature15714	journal	November 2015
Full-length transcriptome assembly from RNA-Seq data without a reference genome Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran Nature Biotechnology, Vol. 29, Issue 7 https://doi.org/10.1038/nbt.1883	journal	May 2011
Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism Chen, Wei; Gao, Yanqiang; Xie, Weibo Nature Genetics, Vol. 46, Issue 7 https://doi.org/10.1038/ng.3007	journal	June 2014
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
HISAT: a fast spliced aligner with low memory requirements Kim, Daehwan; Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 12, Issue 4 https://doi.org/10.1038/nmeth.3317	journal	March 2015
Evolutionary patterns of genic DNA methylation vary across land plants Takuno, Shohei; Ran, Jin-Hua; Gaut, Brandon S. Nature Plants, Vol. 2, Issue 2 https://doi.org/10.1038/nplants.2015.222	journal	January 2016
Whole plant cell wall characterization using solution-state 2D NMR Mansfield, Shawn D.; Kim, Hoon; Lu, Fachuang Nature Protocols, Vol. 7, Issue 9 https://doi.org/10.1038/nprot.2012.064	journal	August 2012
A genome for gnetophytes and early evolution of seed plants Wan, Tao; Liu, Zhi-Ming; Li, Ling-Fei Nature Plants, Vol. 4, Issue 2 https://doi.org/10.1038/s41477-017-0097-2	journal	January 2018
Fern genomes elucidate land plant evolution and cyanobacterial symbioses Li, Fay-Wei; Brouwer, Paul; Carretero-Paulet, Lorenzo Nature Plants, Vol. 4, Issue 7 https://doi.org/10.1038/s41477-018-0188-8	journal	July 2018
The biosynthetic origin of psychoactive kavalactones in kava Pluskal, Tomáš; Torrens-Spence, Michael P.; Fallon, Timothy R. Nature Plants, Vol. 5, Issue 8 https://doi.org/10.1038/s41477-019-0474-0	journal	July 2019
The hornwort genome and early land plant evolution Zhang, Jian; Fu, Xin-Xing; Li, Rui-Qi Nature Plants, Vol. 6, Issue 2 https://doi.org/10.1038/s41477-019-0588-4	journal	February 2020
Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts Li, Fay-Wei; Nishiyama, Tomoaki; Waller, Manuel Nature Plants, Vol. 6, Issue 3 https://doi.org/10.1038/s41477-020-0618-2	journal	March 2020
Charting the genomic landscape of seed-free plants Szövényi, Péter; Gunadi, Andika; Li, Fay-Wei Nature Plants, Vol. 7, Issue 5 https://doi.org/10.1038/s41477-021-00888-z	journal	April 2021
The nearly complete genome of Ginkgo biloba illuminates gymnosperm evolution Liu, Hailin; Wang, Xiaobo; Wang, Guibin Nature Plants, Vol. 7, Issue 6 https://doi.org/10.1038/s41477-021-00933-x	journal	June 2021
Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Zhang, Jisen; Zhang, Xingtan; Tang, Haibao Nature Genetics, Vol. 50, Issue 11 https://doi.org/10.1038/s41588-018-0237-2	journal	October 2018
The C-Fern (Ceratopteris richardii) genome: insights into plant genome evolution with the first partial homosporous fern genome assembly Marchant, D. Blaine; Sessa, Emily B.; Wolf, Paul G. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-53968-8	journal	December 2019
Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5 Kim, Hoon; Ralph, John Org. Biomol. Chem., Vol. 8, Issue 3 https://doi.org/10.1039/B916070A	journal	January 2010
Demography of Cyathea hornei (Cyatheaceae), a Tropical Tree-Fern in Fiji Ash, J. Australian Journal of Botany, Vol. 35, Issue 3 https://doi.org/10.1071/BT9870331	journal	January 1987
On the origin and evolutionary consequences of gene body DNA methylation Bewick, Adam J.; Ji, Lexiang; Niederhuth, Chad E. Proceedings of the National Academy of Sciences, Vol. 113, Issue 32 https://doi.org/10.1073/pnas.1604666113	journal	July 2016
The timescale of early land plant evolution Morris, Jennifer L.; Puttick, Mark N.; Clark, James W. Proceedings of the National Academy of Sciences, Vol. 115, Issue 10 https://doi.org/10.1073/pnas.1719588115	journal	February 2018
RepeatModeler2 for automated genomic discovery of transposable element families Flynn, Jullien M.; Hubley, Robert; Goubert, Clément Proceedings of the National Academy of Sciences, Vol. 117, Issue 17 https://doi.org/10.1073/pnas.1921046117	journal	April 2020
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe The American Journal of Human Genetics, Vol. 81, Issue 3 https://doi.org/10.1086/519795	journal	September 2007
Slowly but surely: gradual diversification and phenotypic evolution in the hyper-diverse tree fern family Cyatheaceae Loiseau, Oriane; Weigand, Anna; Noben, Sarah Annals of Botany, Vol. 125, Issue 1 https://doi.org/10.1093/aob/mcz145	journal	September 2019
r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock Sanderson, M. J. Bioinformatics, Vol. 19, Issue 2 https://doi.org/10.1093/bioinformatics/19.2.301	journal	January 2003
CAFE: a computational tool for the study of gene family evolution De Bie, T.; Cristianini, N.; Demuth, J. P. Bioinformatics, Vol. 22, Issue 10 https://doi.org/10.1093/bioinformatics/btl097	journal	March 2006
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications Krueger, Felix; Andrews, Simon R. Bioinformatics, Vol. 27, Issue 11 https://doi.org/10.1093/bioinformatics/btr167	journal	April 2011
The variant call format and VCFtools Danecek, P.; Auton, A.; Abecasis, G. Bioinformatics, Vol. 27, Issue 15 https://doi.org/10.1093/bioinformatics/btr330	journal	June 2011
CD-HIT: accelerated for clustering the next-generation sequencing data Fu, Limin; Niu, Beifang; Zhu, Zhengwei Bioinformatics, Vol. 28, Issue 23 https://doi.org/10.1093/bioinformatics/bts565	journal	October 2012
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
SOAPdenovo-Trans: de novo transcriptome assembly with short RNA-Seq reads Xie, Y.; Wu, G.; Tang, J. Bioinformatics, Vol. 30, Issue 12 https://doi.org/10.1093/bioinformatics/btu077	journal	February 2014
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv351	journal	June 2015
Minimap2: pairwise alignment for nucleotide sequences Li, Heng Bioinformatics, Vol. 34, Issue 18 https://doi.org/10.1093/bioinformatics/bty191	journal	May 2018
ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R Paradis, Emmanuel; Schliep, Klaus Bioinformatics, Vol. 35, Issue 3 https://doi.org/10.1093/bioinformatics/bty633	journal	July 2018
wgd—simple command line tools for the analysis of ancient whole-genome duplications Zwaenepoel, Arthur; Van de Peer, Yves Bioinformatics, Vol. 35, Issue 12 https://doi.org/10.1093/bioinformatics/bty915	journal	November 2018
RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference Kozlov, Alexey M.; Darriba, Diego; Flouri, Tomáš Bioinformatics, Vol. 35, Issue 21 https://doi.org/10.1093/bioinformatics/btz305	journal	May 2019
Two New Fern Chloroplasts and Decelerated Evolution Linked to the Long Generation Time in Tree Ferns Zhong, B.; Fong, R.; Collins, L. J. Genome Biology and Evolution, Vol. 6, Issue 5 https://doi.org/10.1093/gbe/evu087	journal	April 2014
The Huperzia selago Shoot Tip Transcriptome Sheds New Light on the Evolution of Leaves Evkaikina, Anastasiia I.; Berke, Lidija; Romanova, Marina A. Genome Biology and Evolution, Vol. 9, Issue 9 https://doi.org/10.1093/gbe/evx169	journal	August 2017
Evolution of plant conducting cells: perspectives from key regulators of vascular cell differentiation Ohtani, Misato; Akiyoshi, Nobuhiro; Takenaka, Yuto Journal of Experimental Botany, Vol. 68, Issue 1 https://doi.org/10.1093/jxb/erw473	journal	December 2016
Allopolyploid Speciation Accompanied by Gene Flow in a Tree Fern Wang, Jing; Dong, Shiyong; Yang, Lihua Molecular Biology and Evolution, Vol. 37, Issue 9 https://doi.org/10.1093/molbev/msaa097	journal	April 2020
PAML 4: Phylogenetic Analysis by Maximum Likelihood Yang, Z. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm088	journal	April 2007
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
SweeD: Likelihood-Based Detection of Selective Sweeps in Thousands of Genomes Pavlidis, Pavlos; Živković, Daniel; Stamatakis, Alexandros Molecular Biology and Evolution, Vol. 30, Issue 9 https://doi.org/10.1093/molbev/mst112	journal	June 2013
Detecting and Locating Whole Genome Duplications on a Phylogeny: A Probabilistic Approach Rabier, Charles-Elie; Ta, Tram; Ané, Cécile Molecular Biology and Evolution, Vol. 31, Issue 3 https://doi.org/10.1093/molbev/mst263	journal	December 2013
ModelTest-NG: A New and Scalable Tool for the Selection of DNA and Protein Evolutionary Models Darriba, Diego; Posada, David; Kozlov, Alexey M. Molecular Biology and Evolution, Vol. 37, Issue 1 https://doi.org/10.1093/molbev/msz189	journal	August 2019
Tandem repeats finder: a program to analyze DNA sequences Benson, G. Nucleic Acids Research, Vol. 27, Issue 2 https://doi.org/10.1093/nar/27.2.573	journal	January 1999
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity Wang, Y.; Tang, H.; DeBarry, J. D. Nucleic Acids Research, Vol. 40, Issue 7 https://doi.org/10.1093/nar/gkr1293	journal	January 2012
Down-regulation of glycosyltransferase 8D genes in Populus trichocarpa caused reduced mechanical strength and xylan content in wood Li, Q.; Min, D.; Wang, J. P. -Y. Tree Physiology, Vol. 31, Issue 2 https://doi.org/10.1093/treephys/tpr008	journal	February 2011
Involvement of VNS NAC-domain transcription factors in tracheid formation in Pinus taeda Akiyoshi, Nobuhiro; Nakano, Yoshimi; Sano, Ryosuke Tree Physiology, Vol. 40, Issue 6 https://doi.org/10.1093/treephys/tpz106	journal	December 2019
Transcription switches for protoxylem and metaxylem vessel formation Kubo, M. Genes & Development, Vol. 19, Issue 16 https://doi.org/10.1101/gad.1331305	journal	August 2005
Fast model-based estimation of ancestry in unrelated individuals Alexander, D. H.; Novembre, J.; Lange, K. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.094052.109	journal	July 2009
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data McKenna, A.; Hanna, M.; Banks, E. Genome Research, Vol. 20, Issue 9 https://doi.org/10.1101/gr.107524.110	journal	July 2010
GeneWise and Genomewise Birney, E. Genome Research, Vol. 14, Issue 5 https://doi.org/10.1101/gr.1865504	journal	May 2004
Canu: scalable and accurate long-read assembly via adaptive k -mer weighting and repeat separation Koren, Sergey; Walenz, Brian P.; Berlin, Konstantin Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.215087.116	journal	March 2017
VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 Effectively Induce Transdifferentiation into Xylem Vessel Elements under Control of an Induction System Yamaguchi, Masatoshi; Goué, Nadia; Igarashi, Hisako Plant Physiology, Vol. 153, Issue 3 https://doi.org/10.1104/pp.110.154013	journal	May 2010
Structural, Functional, and Evolutionary Analysis of the Unusually Large Stilbene Synthase Gene Family in Grapevine Parage, Claire; Tavares, Raquel; Réty, Stéphane Plant Physiology, Vol. 160, Issue 3 https://doi.org/10.1104/pp.112.202705	journal	September 2012
Hydroxystilbenes Are Monomers in Palm Fruit Endocarp Lignins Carlos del Río, José; Rencoret, Jorge; Gutiérrez, Ana Plant Physiology, Vol. 174, Issue 4 https://doi.org/10.1104/pp.17.00362	journal	June 2017
Transcription Factors VND1-VND3 Contribute to Cotyledon Xylem Vessel Formation Tan, Tian Tian; Endo, Hitoshi; Sano, Ryosuke Plant Physiology, Vol. 176, Issue 1 https://doi.org/10.1104/pp.17.00461	journal	November 2017
SND1, a NAC Domain Transcription Factor, Is a Key Regulator of Secondary Wall Synthesis in Fibers of Arabidopsis Zhong, Ruiqin; Demura, Taku; Ye, Zheng-Hua The Plant Cell, Vol. 18, Issue 11 https://doi.org/10.1105/tpc.106.047399	journal	November 2006
Convergent Evolution of Syringyl Lignin Biosynthesis via Distinct Pathways in the Lycophyte Selaginella and Flowering Plants Weng, Jing-Ke; Akiyama, Takuya; Bonawitz, Nicholas D. The Plant Cell, Vol. 22, Issue 4 https://doi.org/10.1105/tpc.109.073528	journal	April 2010
Independent Recruitment of an O -Methyltransferase for Syringyl Lignin Biosynthesis in Selaginella moellendorffii Weng, Jing-Ke; Akiyama, Takuya; Ralph, John The Plant Cell, Vol. 23, Issue 7 https://doi.org/10.1105/tpc.110.081547	journal	July 2011
Detecting the number of clusters of individuals using the software structure: a simulation study Evanno, G.; Regnaut, S.; Goudet, J. Molecular Ecology, Vol. 14, Issue 8 https://doi.org/10.1111/j.1365-294X.2005.02553.x	journal	July 2005
The presence of sinapyl lignin in Ginkgo biloba cell cultures changes our views of the evolution of lignin biosynthesis Uzal, Esther Novo; Gómez Ros, Laura V.; Pomar, Federico Physiologia Plantarum, Vol. 135, Issue 2 https://doi.org/10.1111/j.1399-3054.2008.01185.x	journal	February 2009
Distribution of Lignin Derivatives in Plants Logan, Karen J.; Thomas, Barry A. New Phytologist, Vol. 99, Issue 4 https://doi.org/10.1111/j.1469-8137.1985.tb03685.x	journal	April 1985
Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus Buggs, Richard J. A.; Elliott, Natalie M.; Zhang, Linjing New Phytologist, Vol. 186, Issue 1 https://doi.org/10.1111/j.1469-8137.2010.03205.x	journal	March 2010
Abrupt Deceleration of Molecular Evolution Linked to the Origin of Arborescence in Ferns Korall, Petra; Schuettpelz, Eric; Pryer, Kathleen M. Evolution, Vol. 64, Issue 9 https://doi.org/10.1111/j.1558-5646.2010.01000.x	journal	September 2010
Arabidopsis thaliana NOP10 is required for gametophyte formation: AtNOP10 functions in gametophyte formation Li, Lin-Xiao; Liao, Hong-Ze; Jiang, Li-Xi Journal of Integrative Plant Biology, Vol. 60, Issue 8 https://doi.org/10.1111/jipb.12652	journal	June 2018
A community-derived classification for extant lycophytes and ferns: PPG I Journal of Systematics and Evolution, Vol. 54, Issue 6 https://doi.org/10.1111/jse.12229	journal	November 2016
Genome evolution of ferns: evidence for relative stasis of genome size across the fern phylogeny Clark, James; Hidalgo, Oriane; Pellicer, Jaume New Phytologist, Vol. 210, Issue 3 https://doi.org/10.1111/nph.13833	journal	January 2016
The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution Lang, Daniel; Ullrich, Kristian K.; Murat, Florent The Plant Journal, Vol. 93, Issue 3 https://doi.org/10.1111/tpj.13801	journal	January 2018
Genome-Wide Evolutionary Analysis of Eukaryotic DNA Methylation Zemach, A.; McDaniel, I. E.; Silva, P. Science, Vol. 328, Issue 5980 https://doi.org/10.1126/science.1186366	journal	April 2010
The Selaginella Genome Identifies Genetic Changes Associated with the Evolution of Vascular Plants Banks, J. A.; Nishiyama, T.; Hasebe, M. Science, Vol. 332, Issue 6032 https://doi.org/10.1126/science.1203810	journal	May 2011
Contribution of NAC Transcription Factors to Plant Adaptation to Land Xu, B.; Ohtani, M.; Yamaguchi, M. Science, Vol. 343, Issue 6178 https://doi.org/10.1126/science.1248417	journal	March 2014
De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds Dudchenko, Olga; Batra, Sanjit S.; Omer, Arina D. Science, Vol. 356, Issue 6333 https://doi.org/10.1126/science.aal3327	journal	March 2017
Repbase Update, a database of eukaryotic repetitive elements Jurka, J.; Kapitonov, V. V.; Pavlicek, A. Cytogenetic and Genome Research, Vol. 110, Issue 1-4 https://doi.org/10.1159/000084979	journal	January 2005
Engineered fungal polyketide biosynthesis in Pichia pastoris: a potential excellent host for polyketide production Gao, Limei; Cai, Menghao; Shen, Wei Microbial Cell Factories, Vol. 12, Issue 1 https://doi.org/10.1186/1475-2859-12-77	journal	September 2013
ANGSD: Analysis of Next Generation Sequencing Data Korneliussen, Thorfinn Sand; Albrechtsen, Anders; Nielsen, Rasmus BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/s12859-014-0356-4	journal	November 2014
Homoeolog expression bias and expression level dominance in resynthesized allopolyploid Brassica napus Wu, Jian; Lin, Li; Xu, Meiling BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4966-5	journal	August 2018
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy Emms, David M.; Kelly, Steven Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0721-2	journal	August 2015
Stairway Plot 2: demographic history inference with folded SNP frequency spectra Liu, Xiaoming; Fu, Yun-Xin Genome Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s13059-020-02196-9	journal	November 2020
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Expression Level Dominance and Homeolog Expression Bias in Recurrent Origins of the Allopolyploid Fern Polypodium hesperium Sigel, Erin M.; Der, Joshua P.; Windham, Michael D. American Fern Journal, Vol. 109, Issue 3 https://doi.org/10.1640/0002-8444-109.3.224	journal	September 2019
Enzyme Promiscuous Activity: How to Define it and its Evolutionary Aspects De Luca, Valentina; Mandrich, Luigi Protein & Peptide Letters, Vol. 27, Issue 5 https://doi.org/10.2174/0929866527666191223141205	journal	April 2020
Antimicrobial activity of ethanolic and aqueous extracts of medicinally used tree ferns Alsophila cuspidata and Cyathea microdonta Longtine, Charlie; Tejedor, Adrian Acta Botanica Malacitana, Vol. 42, Issue 1 https://doi.org/10.24310/abm.v42i1.2885	journal	February 2018
Organelle Genome Inheritance in Deparia Ferns (Athyriaceae, Aspleniineae, Polypodiales) Kuo, Li-Yaung; Tang, Te-Yen; Li, Fay-Wei Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00486	journal	April 2018
Investigation Into Different Wood Formation Mechanisms Between Angiosperm and Gymnosperm Tree Species at the Transcriptional and Post-transcriptional Level Li, Hui; Chen, Guanghui; Pang, Hongying Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.698602	journal	July 2021
Dynamic DNA Methylation in Plant Growth and Development Bartels, Arthur; Han, Qiang; Nair, Pooja International Journal of Molecular Sciences, Vol. 19, Issue 7 https://doi.org/10.3390/ijms19072144	journal	July 2018
On the Recognition of Gymnosphaera As a Distinct Genus in Cyatheaceae Dong, Shi-Yong; Zuo, Zheng-Yu Annals of the Missouri Botanical Garden, Vol. 103, Issue 1 https://doi.org/10.3417/2017049	journal	May 2018
The evolutionary history of ferns inferred from 25 low‐copy nuclear genes Rothfels, Carl J.; Li, Fay‐Wei; Sigel, Erin M. American Journal of Botany, Vol. 102, Issue 7 https://doi.org/10.3732/ajb.1500089	journal	July 2015
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w Cingolani, Pablo; Platts, Adrian; Wang, Le Lily Fly, Vol. 6, Issue 2 https://doi.org/10.4161/fly.19695	journal	April 2012
Genome assembly and Annotation of Alsophila spinulosa Chen, Song figshare https://doi.org/10.6084/m9.figshare.19075346.v4	dataset	January 2022
Phylogenetic trees Chen, Song figshare https://doi.org/10.6084/m9.figshare.19125641.v4	image	January 2022
Expression Level Dominance and Homeolog Expression Bias in Recurrent Origins of the Allopolyploid Fern Polypodium hesperium Sigel, Erin; Der, Joshua P.; Windham, Michael D. figshare https://doi.org/10.6084/m9.figshare.c.4388981.v1	collection	January 2019

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