Cited by 1,252Protist diversity and phylogenyPlant Diversity and EvolutionGenomics and Phylogenetic Studies

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Phylotranscriptomic analysis of the origin and early diversification of land plants

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Wickett, Norman J., Mirarab, Siavash, Nguyen, Nam, Warnow, Tandy, Carpenter, Eric, Matasci, Naim, Ayyampalayam, Saravanaraj, Barker, Michael S., Burleigh, J. Gordon, Gitzendanner, Matthew A., Ruhfel, Brad R., Wafula, Eric, Der, Joshua P., Graham, Sean W., Mathews, Sarah, Melkonian, Michael, Soltis, Douglas E., Soltis, Pamela S., Miles, Nicholas W., Rothfels, Carl J., Pokorny, Lisa, Shaw, A. Jonathan, DeGironimo, Lisa, Stevenson, Dennis W., Surek, Barbara, Villarreal, Juan Carlos, Roure, Béatrice, Philippe, Hervé, dePamphilis, Claude W., Chen, Tao, Deyholos, Michael K., Baucom, Regina S., Kutchan, Toni M., Augustin, Megan M., Wang, Jun, Zhang, Yong, Tian, Zhijian, Yan, Zhixiang, Wu, Xiaolei, Sun, Xiao, Wong, Gane Ka-Shu, Leebens-Mack, James·2014·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1323926111PMC PMC4234587

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Abstract

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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Self-citation
Adaptation to life on land at high O 2 via transition from ferredoxin-to NADH-dependent redox balance
Gould, S. B., Garg, S. G., Handrich, M. R., Sathi, S. N., Gruenheit, N., Tielens, A. G. M., & Martin, W. F. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.1491 · Cited by 22
“Current findings have shown that the monophyletic origin of land plants, which occurred some 450 Ma [12,13], boosted O2 accumulation to modern levels through massive carbon burial [9,10].”
Background
Multilocus data reveal deep phylogenetic relationships and intercontinental biogeography of the Eurasian-North American genus Corylus (Betulaceae)
Zhao, T., Wang, G., Ma, Q., Liang, L., & Yang, Z. (2019) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2019.106658 · Cited by 20
Supertree Construction: Opportunities and ChallengesPreprint
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“, [61, 140]), leading many systematists to seek alternative approaches to concatenation analysis in constructing species trees.”
BackgroundInfluentialSelf-citation
Phylogenetic Resolution and Conflict in the Species-Rich Flowering Plant Family Leguminosae
Zhang, R., Stull, G. W., Jin, J., Wang, Y., Guo, Y., Yang, Z., Li, H., An, K.-L., Charboneau, J. L. M., Folk, R. A., et al. (2025) · Systematic Biology · doi:10.1093/sysbio/syaf057 · Cited by 19
“However, persistent challenges remain in resolving relationships among lineages that have experienced rapid, successive diversification events (e.g., Steemans et al. 2009 ; Wickett et al. 2014 ; Li, Yi, et al. 2019 ; Zuntini et al. 2024 ).”
Self-citation
Targeted sequencing for high-resolution evolutionary analyses following genome duplication in salmonid fish: Proof of concept for key components of the insulin-like growth factor axis
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“…10K’ (Haussler et al., 2009) and Fish-T1K (Sun et al., 2016) are aiming to characterise vast genomic diversity within eukaryotes, while providing essential data for comparative-genomic, evolutionary and phylogenetic studies (e.g. Wickett et al., 2014; Zhang et al., 2014; Jarvis et al., 2014).”
Background
Reconstructing the phylogeny of new world monkeys (platyrrhini): evidence from multiple non-coding loci
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Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion
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“Furthermore, phylogeny analysis has placed the Zygnematophyceae class as the closest sister group to land plants (Wickett et al., 2014; Delwiche and Cooper, 2015).”
Background
The GENOMES UNCOUPLED1 protein has an ancient, highly conserved role but not in retrograde signalling
Honkanen, S., & Small, I. (2022) · New Phytologist · doi:10.1111/nph.18318 · Cited by 19
“Land plants form a monophyletic group that evolved from the streptophyte algae (Wickett et al ., 2014).”
A diverse group of underappreciated zygnematophytes deserves in-depth exploration
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“It is now well established that the conjugating green algae (Zygnematophyceae , Streptophyta) represent the sister clade of all land plants (Figure 1(a); Cheng et al. (2019); Timme, Bachvaroff, & Delwiche (2012); Wickett et al. (2014); Wodniok et al., 2011).”
Background
Phylotranscriptomics of Swertiinae (Gentianaceae) reveals that key floral traits are not phylogenetically correlated
Chen, C., Ruhfel, B. R., Li, J., Wang, Z., Zhang, L., Zhang, L., Mao, X., Wang, J., He, D., Luo, Y., et al. (2023) · Journal of Integrative Plant Biology · doi:10.1111/jipb.13464 · Cited by 18
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Evolution of ethylene as an abiotic stress hormone in streptophytes
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The cell walls of different Chara species are characterized by branched galactans rich in 3‐O‐methylgalactose and absence of AGPs
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The Genome of the Model Species Anthoceros agrestis
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DRP3 and ELM1 are required for mitochondrial fission in the liverwort Marchantia polymorpha
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“, [34, 47, 48]) none induced terraces having more than one tree.”
Background
Transient genetic transformation of Mougeotia scalaris (Zygnematophyceae) mediated by the endogenous α‐tubulin1 promoter
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Potential of Transcript Editing Across Mitogenomes of Early Land Plants Shows Novel and Familiar Trends
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Treehouse: a user-friendly application to obtain subtrees from large phylogenies
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“Recent phylogenomic studies suggest that bryophytes could be monophyletic and, consequently, the systematics of classes and divisions have undergone changes (Wickett et al., 2014; Leebens-Mack et al., 2019; Bell et al., 2020).”
Background
Functional Conservation of an AGAMOUS Orthologous Gene Controlling Reproductive Organ Development in the Gymnosperm Species Taxus chinensis var. mairei
Liu, Z., Xiong, H.-Y., Li, L., & Fei, Y.-J. (2018) · Journal of Plant Biology · doi:10.1007/s12374-017-0154-4 · Cited by 19
“…of the AG orthologous gene in gymnosperms, we isolated AG-like gene TcAG from Taxus chinensis var. mairei (family Taxaceae, order Coniferales), a member of the last divergant lineage from higher Conifers that sister to Gnetales (Wang and Ran 2014; Wickett et al. 2014; Uddenberg et al. 2015).”
Background
Protist Diversification
Simpson, A. G. B., & Eglit, Y. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-800049-6.00247-x · Cited by 19
Plant terrestrialization: an environmental pull on the evolution of multi-sourced streptophyte phenolics
Kunz, C. F., de Vries, S., & de Vries, J. (2024) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2023.0358 · Cited by 18
“Thus, the last common ancestor (LCA) of land plants and algae was a phragmoplastophyte and all analyses agree that the closest algal relatives of land plants are the Zygnematophyceae [11–14].”
Background
Molecular and Morphological Evidence Challenges the Records of the Extant Liverwort Ptilidium pulcherrimum in Eocene Baltic Amber
Heinrichs, J., Scheben, A., Lee, G. E., Váňa, J., Schäfer‐Verwimp, A., Krings, M., & Schmidt, A. R. (2015) · PLoS ONE · doi:10.1371/journal.pone.0140977 · Cited by 18
Biases of tree-independent-character-subsampling methods
Simmons, M. P., & Gatesy, J. (2016) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2016.04.022 · Cited by 18
Ephedra as a gymnosperm evo‐devo model lineage
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“Gnetales include a reference genome for Gnetum montanum (Wan et al., 2018), and transcriptomic resources for Welwitschia mirabilis and Ephedra sinica (1 KP project, Wickett et al., 2014).”
Background
The Saururus chinensis genome provides insights into the evolution of pollination strategies and herbaceousness in magnoliids
Xue, J., Li, Z., Hu, S., Kao, S., Zhao, T., Wang, J., Wang, Y., Chen, M., Qiu, Y., Fan, H., et al. (2023) · The Plant Journal · doi:10.1111/tpj.16097 · Cited by 18
“…and other mesangiosperm lineages, also using molecular data, despite many attempts employing a large amount of data from nuclear, plastid, and mitochondrial genomes (Gitzendanner et al., 2018; Li et al., 2019; One Thousand Plant Transcriptomes, 2019; Wickett et al., 2014; Xue et al., 2022).”
BackgroundSelf-citation
Incomplete lineage sorting and long-branch attraction confound phylogenomic inference of Pancrustacea
Yu, H. Y., Chu, K. H., Tsang, L. M., & Ma, K. Y. (2024) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2024.1243221 · Cited by 23
Marine genomics: News and views
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ANGUSTIFOLIA contributes to the regulation of three-dimensional morphogenesis in the liverwort Marchantia polymorpha
Furuya, T., Hattori, K., Kimori, Y., Ishida, S., Nishihama, R., Kohchi, T., & Tsukaya, H. (2018) · Development · doi:10.1242/dev.161398 · Cited by 18
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Method
One Upward, Two Steps Down: Order of Floral Organ Initiation
Remizowa, M. V. (2019) · Russian Journal of Developmental Biology · doi:10.1134/s1062360419060080 · Cited by 18
The Complete Moss Mitochondrial Genome in the Angiosperm Amborella Is a Chimera Derived from Two Moss Whole-Genome Transfers
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Background
Divide-and-Conquer Tree Estimation: Opportunities and Challenges
Warnow, T. J. (2019) · Computational biology · doi:10.1007/978-3-030-10837-3_6 · Cited by 18
Self-citation
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“Based on the inferred phylogenetic relationships, it was often unclear whether the sister clade of extant angiosperms is Amborellales alone (e.g., [5, 6, 33–36]) or Amborellales + Nymphaeales (e.g., [20, 30, 32, 37–40]).”
Mutually exclusive phylogenomic inferences at the root of the angiosperms: Amborella is supported as sister and Observed Variability is biased
Simmons, M. P. (2016) · Cladistics · doi:10.1111/cla.12177 · Cited by 17
“This phylogenetic hypothesis also has been supported by other workers’ analyses of still larger genomic data matrices (Ruhfel et al., 2014; Wickett et al., 2014).”
Result
Introgression is widespread in the radiation of carnivorous Nepenthes pitcher plants
Scharmann, M., Wistuba, A., & Widmer, A. (2021) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2021.107214 · Cited by 20
Asteroid: a new algorithm to infer species trees from gene trees under high proportions of missing data
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Genome-wide identification of the N6-methyladenosine regulatory genes reveals NtFIP37B increases drought resistance of tobacco (Nicotiana tabacum L.)
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Comparative transcriptomics elucidates the cellular responses of an aeroterrestrial zygnematophyte to UV radiation
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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
DOI: 10.1073/pnas.1323926111
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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Phylotranscriptomic analysis of the origin and early diversification of land plants

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