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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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Self-citationPhylogeny of the Rosidae: A dense taxon sampling analysis
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BackgroundHaufler, C. H., Pryer, K. M., Schuettpelz, E., Sessa, E. B., Farrar, D. R., Moran, R. C., Schneller, J., Watkins, J. E., & Windham, M. D. (2016) · BioScience · doi:10.1093/biosci/biw108 · Cited by 147
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A Phylogenomic Supertree of Birds
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Self-citationAbiotic Stress Tolerance of Charophyte Green Algae: New Challenges for Omics Techniques
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Plastome Phylogenetics: 30 Years of Inferences Into Plant Evolution
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Genomes of multicellular algal sisters to land plants illuminate signaling network evolution
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InfluentialThe Expansion and Diversification of Pentatricopeptide Repeat RNA-Editing Factors in Plants
Gutmann, B., Royan, S., Schallenberg‐Rüdinger, M., Lenz, H., Castleden, I. R., McDowell, R., Vacher, M. A., Tonti‐Filippini, J., Bond, C. S., Knoop, V., et al. (2019) · Molecular Plant · doi:10.1016/j.molp.2019.11.002 · Cited by 117
Field Guide to Plant Model Systems
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Nuclear protein phylogenies support the monophyly of the three bryophyte groups (Bryophyta Schimp.)
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Microbial-type terpene synthase genes occur widely in nonseed land plants, but not in seed plants
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“However, increased availability of transcriptomes across angiosperms (Wickett et al., 2014) and lowered sequencing costs allow access to more genomic resources useful in non-model groups.”
BackgroundPhytochrome evolution in 3D: deletion, duplication, and diversification
Rockwell, N. C., & Lagarias, J. C. (2019) · New Phytologist · doi:10.1111/nph.16240 · Cited by 118
“, 1997), as did phytochrome from a member of the sister clade to all other known streptophytes, the streptophyte Mesostigma viride (Wickett et al., 2014; Rockwell et al., 2017).”
BackgroundMethodInfluentialWhole-genome microsynteny-based phylogeny of angiosperms
Zhao, T., Zwaenepoel, A., Xue, J.-Y., Kao, S.-M., Li, Z., Schranz, M. E., & Van de Peer, Y. (2021) · Nature Communications · doi:10.1038/s41467-021-23665-0 · Cited by 117
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“Support for Zygnematophyceae as sister to land plants is strengthened by recent phylogenomic analyses (Zhong et al. 2013, 2015; Wickett et al. 2014; Cheng et al. 2019; One Thousand Plant Transcriptomes Initiative 2019; Jiao et al. 2020), but the relationships among the four major groups of land plants— mosses, liverwo…”
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Phylogenomic Insights into Deep Phylogeny of Angiosperms Based on Broad Nuclear Gene Sampling
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“The angiosperm phylogeny has been greatly improved in recent years (e.g., Moore et al., 2007; Soltis et al., 2011; Ruhfel et al., 2014; Wickett et al., 2014; Zeng et al., 2014; Byng et al., 2016; Zhong and Betancur-R, 2017; Gitzendanner et al., 2018; Leebens-Mack et al., 2019; Li et al., 2019), but the branching order…”
BackgroundSingle-Copy Genes as Molecular Markers for Phylogenomic Studies in Seed Plants
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“Compared with the chloroplast, nuclear sequences can be more effective in resolving phylogeny (Wickett et al. 2014; Zeng et al. 2014); however, large nuclear data sets have been limited in Arundinarieae largely due to the difficulties of identifying sufficient unambiguous single or low copy nuclear loci and their orth…”
BackgroundThe Evolution of Cell Division: From Streptophyte Algae to Land Plants
Buschmann, H., & Zachgo, S. (2016) · Trends in Plant Science · doi:10.1016/j.tplants.2016.07.004 · Cited by 111
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“Introduction Land plants evolved from within the higher streptophyte algae (Lewis and McCourt 2004, Wickett et al. 2014, Delwiche and Cooper 2015, de Vries et al. 2016).”
BackgroundAn open and continuously updated fern tree of life
Nitta, J. H., Schuettpelz, E., Ramírez‐Barahona, S., & Iwasaki, W. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.909768 · Cited by 114
“…of publicly available DNA sequence data, and several pipeline tools exist that can leverage such data to automatically generate phylogenies (Pearse and Purvis, 2013; Xu et al., 2015; Antonelli et al., 2016; Bennett et al., 2018b; Drori et al., 2018; Smith and Walker, 2019; Portik and Wiens, 2020).”
BackgroundWalker, J. F., Yang, Y. J., Feng, T., Timoneda, A., Mikenas, J. D., Hutchison, V., Edwards, C., Wang, N., Ahluwalia, S., Olivieri, J. E., et al. (2018) · American Journal of Botany · doi:10.1002/ajb2.1069 · Cited by 108
A phylogenomically informed five-order system for the closest relatives of land plants
Hess, S., Williams, S. K., Busch, A., Irisarri, I., Delwiche, C. F., de Vries, S., Darienko, T., Roger, A. J., Archibald, J. M., Buschmann, H., et al. (2022) · Current Biology · doi:10.1016/j.cub.2022.08.022 · Cited by 111
Phylogenomic analyses of bat subordinal relationships based on transcriptome data
Lei, M., & Dong, D. (2016) · Scientific Reports · doi:10.1038/srep27726 · Cited by 109
“Transcriptome data are often used in the phylogenomic analyses studies for those non-model organisms without genome information 17–19 .”
Kriegshauser, L., Knosp, S., Grienenberger, E., Tatsumi, K., Gütle, D. D., Sørensen, I., Herrgott, L., Zumsteg, J., Rose, J. K. C., Ralf Reski, A., et al. (2021) · The Plant Cell · doi:10.1093/plcell/koab044 · Cited by 110
Weighted Statistical Binning: Enabling Statistically Consistent Genome-Scale Phylogenetic Analyses
Bayzid, M. S., Mirarab, S., Boussau, B., & Warnow, T. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129183 · Cited by 110
“ubset of the data. ASTRAL estimates species trees given unrooted gene trees, and can analyze very large datasets (such as the plant 8 transcriptome dataset with approximately 100 species and 600 loci [35]); hence, ASTRAL can analyze larger datasets than MP-EST, and so understanding the impact of binning on ASTRAL’s ac…”
MethodSelf-citationRuhlman, T. A., Chang, W., Chen, J. J. W., Huang, Y., Chan, M., Zhang, J., Liao, D., Blazier, J. C., Jin, X., Shih, M.-C., et al. (2015) · BMC Plant Biology · doi:10.1186/s12870-015-0484-7 · Cited by 109
“gnepine, gnetifer, anthopyte, gnetophytes sister to all other gymnosperms) [40-45].”
BackgroundRooting the tree of life: the phylogenetic jury is still out
Gouy, R., Baurain, D., & Philippe, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0329 · Cited by 96
Self-citationFragmentary Gene Sequences Negatively Impact Gene Tree and Species Tree Reconstruction
Sayyari, E., Whitfield, J. B., & Mirarab, S. (2017) · Molecular Biology and Evolution · doi:10.1093/molbev/msx261 · Cited by 112
Self-citationQin, L., Hu, Y., Wang, J., Wang, X., Zhao, R., Shan, H., Li, K., Xu, P., Wu, H., Yan, X., et al. (2021) · Nature Plants · doi:10.1038/s41477-021-00990-2 · Cited by 109
Self-citationEdwards, D., Kenrick, P., & Dolan, L. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0489 · Cited by 106
Ethylene, ACC, and the Plant Growth-Promoting Enzyme ACC Deaminase
Gamalero, E., Lingua, G., & Glick, B. R. (2023) · Biology · doi:10.3390/biology12081043 · Cited by 113
Evolution in the Cycles of Life
Bowman, J. L., Sakakibara, K., Furumizu, C., & Dierschke, T. (2016) · Annual Review of Genetics · doi:10.1146/annurev-genet-120215-035227 · Cited by 107
Stevenson, S. R., Kamisugi, Y., Trinh, C. H., Schmutz, J., Jenkins, J. W., Grimwood, J., Muchero, W., Tuskan, G. A., Rensing, S. A., Lang, D., et al. (2016) · The Plant Cell · doi:10.1105/tpc.16.00091 · Cited by 105
Self-citationDarwin review: angiosperm phylogeny and evolutionary radiations
Soltis, P. S., Folk, R. A., & Soltis, P. S. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.0099 · Cited by 104
Self-citationde Souza, W. R., Martins, P. K., Freeman, J., Pellny, T. K., Michaelson, L. V., Sampaio, B. L., Vinecky, F., Ribeiro, A. P., da Cunha, B. A. D. B., Kobayashi, A. K., et al. (2018) · New Phytologist · doi:10.1111/nph.14970 · Cited by 102
Perianth symmetry changed at least 199 times in angiosperm evolution
Reyes, E., Sauquet, H., & Nadot, S. (2016) · Taxon · doi:10.12705/655.1 · Cited by 102
Chen, F., Ludwiczuk, A., Wei, G., Chen, X., Crandall‐Stotler, B., & Bowman, J. L. (2018) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2018.1482397 · Cited by 105
Baggs, E. L., Monroe, J. G., Thanki, A. S., O’Grady, R., Schudoma, C., Haerty, W., & Krasileva, K. V. (2020) · The Plant Cell · doi:10.1105/tpc.19.00903 · Cited by 101
Catarino, B., Hetherington, A. J., Emms, D., Kelly, S. L., & Dolan, L. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw155 · Cited by 100
Plasmodesmata and intercellular molecular traffic control
Tee, E. E., & Faulkner, C. R. (2024) · New Phytologist · doi:10.1111/nph.19666 · Cited by 98
Abscisic acid controlled sex before transpiration in vascular plants
McAdam, S. A. M., Brodribb, T. J., Banks, J. A., Hedrich, R., Lanman, N. A., Cai, C. Y. L., Geringer, M. A., Lind, C., Nichols, D. S., Stachowski, K., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1606614113 · Cited by 97
“Questions about a lack of functional homology between the stomata of bryophytes and vascular plants (27, 28) arise; given the recent revelation that mosses are sister to liverworts (29).”
BackgroundRippin, M., Becker, B., & Holzinger, A. (2017) · Plant and Cell Physiology · doi:10.1093/pcp/pcx136 · Cited by 103
“In contrast to Klebsormidiophyceae, which are located closer to the basis of the Streptophyta (Becker and Marin 2009), Zygnematophyceae are the sister lineage of the land plants (Wickett et al. 2014).”
ResultThe origin and early evolution of plants
Bowles, A. M. C., Williamson, C. J., Williams, T. A., Lenton, T. M., & Donoghue, P. C. J. (2022) · Trends in Plant Science · doi:10.1016/j.tplants.2022.09.009 · Cited by 95
“However, a diversity of phylogenomic methods and datasets place the simple Zygnematophyceae as a sister group to land plants [3,29,30].”
Wang, H.-C., Susko, E., & Roger, A. J. (2019) · Systematic Biology · doi:10.1093/sysbio/syz021 · Cited by 85
Generative Cell Specification Requires Transcription Factors Evolutionarily Conserved in Land Plants
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Phylogenomic discordance suggests polytomies along the backbone of the large genus Solanum
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“…discordance across key nodes in birds (Suh et al., 2015; Suh, 2016), mammals (Morgan et al., 2013; Romiguier et al., 2013; Simion et al., 2017), amphibians (Hime et al., 2021), plants (Wickett et al., 2014; One Thousand Plant Transcriptomes Initiative, 2019), and fungi (Kuramae et al., 2006).”
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Glacier Algae: A Dark Past and a Darker Future
Williamson, C. J., Cameron, K. A., Cook, J. M., Žárský, J. D., Stibal, M., & Edwards, A. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00524 · Cited by 93
Analyzing Contentious Relationships and Outlier Genes in Phylogenomics
Walker, J. F., Brown, J. W., & Smith, S. A. (2018) · Systematic Biology · doi:10.1093/sysbio/syy043 · Cited by 93
The hornworts: morphology, evolution and development
Frangedakis, E., Shimamura, M., Villarreal, J. C., Li, F., Tomaselli, M., Waller, M., Sakakibara, K., RENZAGLIA, K. S., & Szövényi, P. (2020) · New Phytologist · doi:10.1111/nph.16874 · Cited by 95
“…of tracheophytes (lycophytes, ferns, gymnosperms and angiosperms) is well supported, while the interrelationships among bryophyte lineages and tracheophytes have been the subject of a long-standing debate (Nishiyama et al., 2004; Qiu et al., 2006; Wickett et al., 2014; Morris et al., 2018).”
BackgroundSelf-citationThe Welwitschia genome reveals a unique biology underpinning extreme longevity in deserts
Wan, T., Liu, Z., Leitch, I. J., Xin, H., Maggs‐Kölling, G., Gong, Y., Li, Z., Marais, E., Liao, Y., Dai, C., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24528-4 · Cited by 95
Ickert‐Bond, S. M., & Renner, S. S. (2015) · Journal of Systematics and Evolution · doi:10.1111/jse.12190 · Cited by 95
Roch, S., Nute, M., & Warnow, T. J. (2018) · Systematic Biology · doi:10.1093/sysbio/syy061 · Cited by 92
Self-citationThe Trichoptera barcode initiative: a strategy for generating a species-level Tree of Life
Zhou, X. Y., Frandsen, P. B., Holzenthal, R. W., Beet, C. R., Bennett, K. R., Blahnik, R. J., Bonada, N., Cartwright, D. I., Chuluunbat, S., Cocks, G. V., et al. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0025 · Cited by 91
Marden, J. H., Mangan, S. A., Peterson, M. P., Wafula, E. K., Fescemyer, H. W., Der, J. P., dePamphilis, C. W., & Comita, L. S. (2017) · Molecular Ecology · doi:10.1111/mec.13999 · Cited by 92
“…redundancy and potential artefacts, we used a well-validated orthology analysis (Amborella Genome 2013; Honaas et al. 2013; Ming et al. 2013; Wickett et al. 2014) that employs a hidden Markov matrix procedure to detect deep homology and select the best representative gene model from…”
MethodSelf-citationFlores‐Sandoval, E., Eklund, D. M., Hong, S., Alvarez, J. P., Fisher, T. J., Lampugnani, E. R., Golz, J. F., Vázquez‐Lobo, A., Dierschke, T., Lin, S., et al. (2018) · New Phytologist · doi:10.1111/nph.15090 · Cited by 85
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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