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Phylotranscriptomic analysis of the origin and early diversification of land plants
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Significance: Early branching events in the diversification of land plants and closely related algal lineages remain fundamental and unresolved questions in plant evolutionary biology. Accurate reconstructions of these relationships are critical for testing hypotheses of character evolution: for example, the origins of the embryo, vascular tissue, seeds, and flowers. We investigated relationships among streptophyte algae and land plants using the largest set of nuclear genes that has been applied to this problem to date. Hypothesized relationships were rigorously tested through a series of analyses to assess systematic errors in phylogenetic inference caused by sampling artifacts and model misspecification. Results support some generally accepted phylogenetic hypotheses, while rejecting others. This work provides a new framework for studies of land plant evolution.
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“In addition to our analyses, all the supermatrices have also been previously extensively analyzed using either RAxML or ExaML (e.g., Jarvis et al. 2014; Misof et al. 2014; Wickett et al. 2014).”
From Evaluating fast maximum likelihood-based phylogenetic programs using empirical phylogenomic data sets (2018) · cites this paper as Wickett et al. 2014
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A genome for gnetophytes and early evolution of seed plants
Wan, T., Liu, Z., Li, L., Leitch, A. R., Leitch, I. J., Lohaus, R., Liu, Z., Xin, H.-P., Gong, Y., Liu, Y., et al. (2018) · Nature Plants · doi:10.1038/s41477-017-0097-2 · Cited by 212
Insights into the Diversification and Evolution of R2R3-MYB Transcription Factors in Plants
Jiang, C., & Rao, G. (2020) · PLANT PHYSIOLOGY · doi:10.1104/pp.19.01082 · Cited by 202
Multiple large-scale gene and genome duplications during the evolution of hexapods
Li, Z., Tiley, G. P., Galuska, S. R., Reardon, C. R., Kidder, T. I., Rundell, R. J., & Barker, M. S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710791115 · Cited by 201
“Large sequencing projects such as 1KP (61), 1KITE (26), and i5K (62) will improve our ability to place these events in the plant and hexapod phylogenies.”
BackgroundSelf-citationPractical considerations for plant phylogenomics
McKain, M. R., Johnson, M. G., Uribe‐Convers, S., Eaton, D. A. R., & Yang, Y. J. (2018) · Applications in Plant Sciences · doi:10.1002/aps3.1038 · Cited by 193
“…sequencing to generate protein coding sequences for phylogenomics, or “phylotranscriptomics,” has the versatility to inform relationships from closely related species (Pease et al., 2016) to ancient relationships with relatively slow- evolving coding sequences (Wickett et al., 2014).”
BackgroundYang, Y. J., Moore, M. J., Brockington, S. F., Soltis, P. S., Wong, G. K., Carpenter, E. J., Zhang, Y., Chen, L., Yan, Z., Xie, Y., et al. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv081 · Cited by 200
“…the genetic and genomic bases of diversification in nonmodel systems (e.g., Barker et al. 2008; Dunn et al. 2008; Lee et al. 2011; Wickett et al. 2011; Delaux et al. 2014; Li et al. 2014; Misof et al. 2014; Sveinsson et al. 2014; Wickett et al. 2014; Cannon et al. 2015; Hollister et al. 2015).”
BackgroundMethodSelf-citationRendón‐Anaya, M., Ibarra‐Laclette, E., Méndez‐Bravo, A., Lan, T., Zheng, C., Carretero‐Paulet, L., Pérez-Torres, C., Chacón-López, A., Hernández-Guzmán, G., Chang, T.-H., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1822129116 · Cited by 198
Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land
Zhao, C., Wang, Y., Chan, K. X., Marchant, D. B., Franks, P. J., Randall, D., Tee, E. E., Chen, G. J., Ramesh, S. A., Phua, S. Y., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1812092116 · Cited by 193
“Using two methods, we conducted a comparative genetic similarity analysis (15, 30) of predicted sequences from 61 protein families from 31 species representing the major clades (31, 32) of land plants, streptophyte algae, and chlorophyte algae (Fig.”
BackgroundMethodSelf-citationThe evolutionary history of ferns inferred from 25 low‐copy nuclear genes
Rothfels, C. J., Li, F., Sigel, E. M., Huiet, L., Larsson, A. O., Bürge, D. O., Ruhsam, M., Deyholos, M. K., Soltis, P. S., Stewart, C. N., et al. (2015) · American Journal of Botany · doi:10.3732/ajb.1500089 · Cited by 194
“…of ferns ( Bierhorst, 1977 ; Lugardon and Piquemal, 1993 ; Renzaglia et al., 2000 ; Renzaglia et al., 2001 ), and by other recent molecular phylogenies ( Rai and Graham, 2010 ; Kuo et al., 2011 ; Lehtonen, 2011 ; Grewe et al., 2013 ; Wickett et al., 2014 ; Zhong et al., 2014 ; Knie et al., 2015 ).”
InfluentialSelf-citationEvolution of the Stomatal Regulation of Plant Water Content
Brodribb, T. J., & McAdam, S. A. M. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.00078 · Cited by 191
Embryophyte stress signaling evolved in the algal progenitors of land plants
de Vries, J., Curtis, B. A., Gould, S. B., & Archibald, J. M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1719230115 · Cited by 193
“We have shown that Zygnema and, to some degree, Coleochaete, the algae phylogenetically closest to land plants (42), have many of the stress-signaling factors until now only known from land plants.”
BackgroundThe evolutionary emergence of land plants.
Donoghue, P., Harrison, C. J., Paps, J., & Schneider, H. (2021) · Current Biology · doi:10.1016/j.cub.2021.07.038 · Cited by 153
“Use of site-homogeneous models to analyse an initial 1KP dataset of 852 nuclear protein coding genes recovered bryophyte paraphyly, while a coalescent analysis of amino acid gene trees recovered monophyletic bryo-phytes 32 .”
MethodHarris, B. J., Clark, J. W., Schrempf, D., Szöllősi, G. J., Donoghue, P. C. J., Hetherington, A. M., & Williams, T. A. (2022) · Nature Ecology & Evolution · doi:10.1038/s41559-022-01885-x · Cited by 187
“Indeed, outgroup-rooting analyses using different models 20,33 , datasets and molecules (that is, chloroplast, mitochondrial or nuclear sequences 22,28 ) have provided support for conflicting hypotheses about the earliest-branching lineages and the nature of the ancestral land plant.”
MethodBrockington, S. F., Yang, Y. J., Gandía‐Herrero, F., Covshoff, S., Hibberd, J. M., Sage, R. F., Wong, G. K., Moore, M. J., & Smith, S. A. (2015) · New Phytologist · doi:10.1111/nph.13441 · Cited by 190
Self-citationHuang, C., Zhang, C., Liu, M., Hu, Y., Gao, T., Qi, J., & Mā, H. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw157 · Cited by 185
“…chloroplast sequences, nuclear genes provide genetic information from both parents and are known to be highly effective in resolving phylogeny (Zhang et al. 2012; Wickett et al. 2014; Zeng et al. 2014; Huang et al. 2015; Yang et al. 2015); however, large datasets for Asteraceae are quite limited.”
BackgroundMethodInfluentialCai, L., Xi, Z., Lemmon, E. M., Lemmon, A. R., Mast, A., Buddenhagen, C. E., Liu, L., & Davis, C. “. (2020) · Systematic Biology · doi:10.1093/sysbio/syaa083 · Cited by 184
Phytochrome diversity in green plants and the origin of canonical plant phytochromes
Li, F., Melkonian, M., Rothfels, C. J., Villarreal, J. C., Stevenson, D. W., Graham, S. W., Wong, G. K., Pryer, K. M., & Mathews, S. (2015) · Nature Communications · doi:10.1038/ncomms8852 · Cited by 191
Self-citationEstimating phylogenetic trees from genome‐scale data
Liu, L., Xi, Z., Wu, S., Davis, C. “., & Edwards, S. V. (2015) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12747 · Cited by 188
Using nuclear gene data for plant phylogenetics: Progress and prospects II. Next‐gen approaches
Zimmer, E. A., & Wen, J. (2015) · Journal of Systematics and Evolution · doi:10.1111/jse.12174 · Cited by 184
“Most studies published using RNASeq were exploring deep divergences (e.g., Timme et al., 2012; Wickett et al., 2014; Zeng et al., 2014), and a few also studied family-level or lower-level relationships (Wen et al., 2013; Ma et al., 2015).”
BackgroundGreat moments in evolution: the conquest of land by plants
Rensing, S. A. (2018) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2018.02.006 · Cited by 184
A comparative study of SVDquartets and other coalescent-based species tree estimation methods
Chou, J., Gupta, A., Yaduvanshi, S., Davidson, R., Nute, M., Mirarab, S., & Warnow, T. J. (2015) · BMC Genomics · doi:10.1186/1471-2164-16-s10-s2 · Cited by 184
“Since summary methods are able to analyze large datasets (some are sufficiently fast that they can analyze datasets with 1000 species and 1000 genes [6]), most coalescent-based analyses of biological datasets have been performed using summary methods [18,19].”
MethodSelf-citationChang, Y., Wang, S., Sekimoto, S., Aerts, A. L., Choi, C., Clum, A., LaButti, K. M., Lindquist, E. A., Ngan, C. Y., Ohm, R. A., et al. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv090 · Cited by 185
Liu, Y., Johnson, M. G., Cox, C. J., Medina, R., Devos, N., Vanderpoorten, A., Hedenäs, L., Bell, N., Shevock, J. R., Aguero, B., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09454-w · Cited by 180
Self-citationEvo-physio: on stress responses and the earliest land plants
Fürst‐Jansen, J. M. R., de Vries, S., & de Vries, J. (2020) · Journal of Experimental Botany · doi:10.1093/jxb/eraa007 · Cited by 180
Zhou, X., Shen, X.-X., Hittinger, C. T., & Rokas, A. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msx302 · Cited by 164
Koenen, E. J. M., Ojeda, D. I., Steeves, R., Migliore, J., Bakker, F. T., Wieringa, J. J., Kidner, C. A., Hardy, O. J., Pennington, R. T., Bruneau, A., et al. (2019) · New Phytologist · doi:10.1111/nph.16290 · Cited by 176
Zeng, L., Zhang, N., Zhang, Q., Endress, P. K., Huang, J., & Mā, H. (2017) · New Phytologist · doi:10.1111/nph.14503 · Cited by 172
An overview of extant conifer evolution from the perspective of the fossil record
Leslie, A. B., Beaulieu, J. M., Holman, G., Campbell, C. S., Mei, W., Raubeson, L. R., & Mathews, S. (2018) · American Journal of Botany · doi:10.1002/ajb2.1143 · Cited by 173
Self-citationPrigge, M. J., Platre, M. P., Kadakia, N., Zhang, Y., Greenham, K., Szutu, W., Pandey, B. K., Bhosale, R., Bennett, M. J., Busch, W., et al. (2020) · eLife · doi:10.7554/elife.54740 · Cited by 173
“The sources for the amino-acid sequences (Figure 1—figure supplement 1A) and CDS (Figure 1— figure supplement 1C) are listed in Supplementary file 3 (Jiao et al., 2011; Goodstein et al., 2012; Johnson et al., 2012; Matasci et al., 2014; Wickett et al., 2014; Xie et al., 2014; One Thousand Plant Transcriptomes Initiati…”
BackgroundSelf-citationFoster, C. S. P., Sauquet, H., van der Merwe, M. M., McPherson, H., Rossetto, M., & Ho, S. Y. W. (2016) · Systematic Biology · doi:10.1093/sysbio/syw086 · Cited by 172
“There has also been uncertainty about whether Amborella or Amborella + Nymphaeales is the sister lineage to all other angiosperms (Wickett et al. 2014; Xi et al. 2014).”
BackgroundOrigins and Evolution of Stomatal Development
Chater, C., Caine, R. S., Fleming, A. J., & Gray, J. E. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.00183 · Cited by 172
“Althoughwe discuss the origins of stomatal function in the context of these new discoveries, the evolution of guard cell signaling and stomatal behavior has recently been reviewed (Assmann and Jegla, 2016; Chen et al., 2017; Xu et al., 2016).”
BackgroundThe evolution of CHROMOMETHYLASES and gene body DNA methylation in plants
Bewick, A. J., Niederhuth, C. E., Ji, L., Rohr, N. A., Griffin, P. T., Leebens‐Mack, J., & Schmitz, R. J. (2017) · Genome biology · doi:10.1186/s13059-017-1195-1 · Cited by 177
Self-citation
Metadata
- Authors
- Wickett, N. J., Mirarab, S., Nguyen, N., Warnow, T., Carpenter, E., Matasci, N., Ayyampalayam, S., Barker, M. S., Burleigh, J. G., Gitzendanner, M. A., Ruhfel, B. R., Wafula, E., Der, J. P., Graham, S. W., Mathews, S., Melkonian, M., Soltis, D. E., Soltis, P. S., Miles, N. W., Rothfels, C. J., Pokorny, L., Shaw, A. J., DeGironimo, L., Stevenson, D. W., Surek, B., Villarreal, J. C., Roure, B., Philippe, H., dePamphilis, C. W., Chen, T., Deyholos, M. K., Baucom, R. S., Kutchan, T. M., Augustin, M. M., Wang, J., Zhang, Y., Tian, Z., Yan, Z., Wu, X., Sun, X., Wong, G. K.-S., & Leebens-Mack, J.
- Affiliations
- Northwestern University (US)
- The University of Texas at Austin (US)
- University of Alberta (CA)
- University of Arizona (US)
- University of Georgia (US)
- Department of Biology and
- University of Florida (US)
- Eastern Kentucky University (US)
- Pennsylvania State University (US)
- Department of Botany and
- Harvard University (US)
- University of Cologne (DE)
- Florida Museum of Natural History (US)
- University of British Columbia (CA)
- Consejo Superior de Investigaciones Científicas (ES)
- Duke University (US)
- New York Botanical Garden (US)
- Ludwig-Maximilians-Universität München (DE)
- Université de Montréal (CA)
- Centre National de la Recherche Scientifique (FR)
- Chinese Academy of Sciences (CN)
- University of Michigan (US)
- Donald Danforth Plant Science Center (US)
- BGI Group (China) (CN)
- Department of Plant Biology, University of Georgia, Athens, GA 30602;
- ORCID
- Wickett, Norman J.
- Mirarab, Siavash
- Nguyen, Nam
- Warnow, Tandy
- Carpenter, Eric
- Matasci, Naim
- Barker, Michael S.
- Burleigh, J. Gordon
- Gitzendanner, Matthew A.
- Ruhfel, Brad R.
- Wafula, Eric
- Der, Joshua P.
- Graham, Sean W.
- Mathews, Sarah
- Melkonian, Michael
- Rothfels, Carl J.
- Pokorny, Lisa
- Shaw, A. Jonathan
- Stevenson, Dennis W.
- Villarreal, Juan Carlos
- Philippe, Hervé
- dePamphilis, Claude W.
- Chen, Tao
- Deyholos, Michael K.
- Baucom, Regina S.
- Kutchan, Toni M.
- Augustin, Megan M.
- Wang, Jun
- Zhang, Yong
- Yan, Zhixiang
- Wu, Xiaolei
- Sun, Xiao
- Wong, Gane Ka-Shu
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-10-29
- Volume
- 111
- Issue
- 45
- Pages
- E4859-68
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4234587
- OpenAlex
- W2013277649
- Cited by
- 1,252
- References
- 124
- Citations by year
- 2026: 33 · 2025: 56 · 2024: 92 · 2023: 73 · 2022: 98 · 2021: 144 · 2020: 125 · 2019: 139 · 2018: 168 · 2017: 124 · 2016: 116 · 2015: 81 · 2014: 2
- FWCI
- 44.12
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (acceptedVersion)
- Civil War Book Review (submittedVersion)
- HAL (submittedVersion)
- Funders
- National Institute on Drug Abuse (R01DA025197)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant Diversity and Evolution
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- land plant origin, Zygnematophyceae, liverworts, bryophytes, plant phylogeny, nuclear gene phylogeny, phylogenetic robustness, coalescent phylogenetics, supertree, supermatrix
- MeSH terms
- Phylogeny, Sequence Alignment, DNA, Plant, Genome, Plant, Evolution, Molecular, Quantitative Trait, Heritable, Gene Expression Profiling, Streptophyta, Transcriptome
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