The DOI matches its Crossref record; 69 of the 69 references it cites were found in a registry or an index.
A one-billion-year-old multicellular chlorophyte
Open accessAbstract
Chlorophytes (representing a clade within the Viridiplantae and a sister group of the Streptophyta) probably dominated marine export bioproductivity and played a key role in facilitating ecosystem complexity before the Mesozoic diversification of phototrophic eukaryotes such as diatoms, coccolithophorans and dinoflagellates. Molecular clock and biomarker data indicate that chlorophytes diverged in the Mesoproterozoic or early Neoproterozoic, followed by their subsequent phylogenetic diversification, multicellular evolution and ecological expansion in the late Neoproterozoic and Palaeozoic. This model, however, has not been rigorously tested with palaeontological data because of the scarcity of Proterozoic chlorophyte fossils. Here we report abundant millimetre-sized, multicellular and morphologically differentiated macrofossils from rocks approximately 1,000 million years ago. These fossils are described as Proterocladus antiquus new species and are interpreted as benthic siphonocladalean chlorophytes, suggesting that chlorophytes acquired macroscopic size, multicellularity and cellular differentiation nearly a billion years ago, much earlier than previously thought.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“More recent analyses have tended to resolve an older LECA, with ages closer to 1 Ga being less plausible on the basis of fossils from that period that can uncontroversially be assigned to crown Archaeplastida.”
From ATP synthase evolution on a cross-braced dated tree of life (2023) · cites this paper as [100]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“and more recently with reports of macroscopic multicellular green algae at ∼1.0 Ga (Tang et al., 2020).”
From Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview (2021) · cites this paper as Tang et al., 2020
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The Evolution of Modern Eukaryotic Phytoplankton
Falkowski, P. G., Katz, M. E., Knoll, A. H., Quigg, A., Raven, J. A., Schofield, O., & Taylor, F. J. R. (2004) · Science · doi:10.1126/science.1095964 · Cited by 1,613
Phylogeny and Molecular Evolution of the Green Algae
Leliaert, F., Smith, D. R., Moreau, H., Herron, M. D., Verbruggen, H., Delwiche, C. F., & Clerck, O. D. (2012) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2011.615705 · Cited by 948
The timescale of early land plant evolution
Morris, J. L., Puttick, M. N., Clark, J., Edwards, D., Kenrick, P., Pressel, S., Wellman, C. H., Yang, Z., Schneider, H., & Donoghue, P. C. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1719588115 · Cited by 926
Estimating the timing of early eukaryotic diversification with multigene molecular clocks
Parfrey, L. W., Lahr, D. J. G., Knoll, A. H., & Katz, L. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110633108 · Cited by 899
The rise of algae in Cryogenian oceans and the emergence of animals
Brocks, J. J., Jarrett, A. J. M., Sirantoine, E., Hallmann, C., Hoshino, Y., & Liyanage, T. (2017) · Nature · doi:10.1038/nature23457 · Cited by 574
The Number, Speed, and Impact of Plastid Endosymbioses in Eukaryotic Evolution
Keeling, P. J. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050312-120144 · Cited by 498
Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin
Betts, H. C., Puttick, M. N., Clark, J. W., Williams, T. A., Donoghue, P. C. J., & Pisani, D. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0644-x · Cited by 437
Morphologie und Biologie der Algen
Oltmanns, F. (1922) · Fischer eBooks · doi:10.5962/bhl.title.44469 · Cited by 395
Paleobiological Perspectives on Early Eukaryotic Evolution
Knoll, A. H. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016121 · Cited by 394
Confidence intervals on stratigraphic ranges
Marshall, C. R. (1990) · Paleobiology · doi:10.1017/s0094837300009672 · Cited by 349
Early photosynthetic eukaryotes inhabited low-salinity habitats
Sánchez‐Baracaldo, P., Raven, J. A., Pisani, D., & Knoll, A. H. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620089114 · Cited by 332
Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen
Butterfield, N. J. F., Knoll, A. H., & Swett, K. (1994) · Lethaia · doi:10.1111/j.1502-3931.1994.tb01558.x · Cited by 316
A shale-hosted Cr isotope record of low atmospheric oxygen during the Proterozoic
Cole, D. B., Reinhard, C. T., Wang, X., Gueguen, B., Halverson, G. P., Gibson, T., Hodgskiss, M. S. W., McKenzie, N. R., Lyons, T. W., & Planavsky, N. J. (2016) · Geology · doi:10.1130/g37787.1 · Cited by 296
Bengtson, S., Sallstedt, T., Belivanova, V., & Whitehouse, M. (2017) · PLOS Biology · doi:10.1371/journal.pbio.2000735 · Cited by 284
Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen
Butterfield, N. J. F., Knoll, A. H., & Swett, K. (1994) · Fossils and strata · doi:10.18261/8200376494-1994-01 · Cited by 283
The Geological Succession of Primary Producers in the Oceans
KNOLL, A. H., SUMMONS, R. E., WALDBAUER, J. R., & ZUMBERGE, J. E. (2007) · Evolution of Primary Producers in the Sea · doi:10.1016/b978-012370518-1/50009-6 · Cited by 249
18. A. Pascher: Über Flagellaten und Algen
(1914) · Berichte der Deutschen Botanischen Gesellschaft · doi:10.1111/j.1438-8677.1914.tb07573.x · Cited by 229
Early evolution of the Eukaryota
Butterfield, N. J. F. (2014) · Palaeontology · doi:10.1111/pala.12139 · Cited by 225
Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis
Gibson, T. M., Shih, P. M., Cumming, V. M., Fischer, W. W., Crockford, P. W., Hodgskiss, M. S. W., Wörndle, S., Creaser, R. A., Rainbird, R. H., Skulski, T. M., et al. (2018) · Geology · doi:10.1130/g39829.1 · Cited by 217
A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record
Berney, C., & Pawlowski, J. (2006) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2006.3537 · Cited by 212
The origins of multicellular organisms
Niklas, K. J., & Newman, S. A. (2013) · Evolution & Development · doi:10.1111/ede.12013 · Cited by 195
Systematics of the Green Algae.
Graham, L. E., Irvine, D. E. G., & John, D. M. (1986) · Systematic Botany · doi:10.2307/2418940 · Cited by 185
Early fungi from the Proterozoic era in Arctic Canada
Loron, C., François, C., Rainbird, R., Turner, E., Borensztajn, S., & Javaux, E. (2019) · Nature · doi:10.1038/s41586-019-1217-0 · Cited by 182
Nuclear and Genome Dynamics in Multinucleate Ascomycete Fungi
Roper, M. L., Ellison, C., Taylor, J. W., & Glass, N. L. (2011) · Current Biology · doi:10.1016/j.cub.2011.06.042 · Cited by 180
A multi-locus time-calibrated phylogeny of the siphonous green algae
Verbruggen, H., Ashworth, M. P., LoDuca, S. T., Vlaeminck, C., Cocquyt, E., Sauvage, T., Zechman, F. W., Littler, D. S., Littler, M. M., & Leliaert, F. (2008) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2008.12.018 · Cited by 177
Actualistic taphonomy of cyanobacteria; implications for the Precambrian fossil record
Bartley, J. K. (1996) · Palaios · doi:10.2307/3515192 · Cited by 177
Green Algae and the Origins of Multicellularity in the Plant KingdomPreprint
Umen, J. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016170 · Cited by 173
The Weng'an biota and the Ediacaran radiation of multicellular eukaryotes
Xiao, S., Muscente, A. D., Chen, L., Zhou, C., Schiffbauer, J. D., Wood, A. D., Polys, N. F., & Yuan, X. (2014) · National Science Review · doi:10.1093/nsr/nwu061 · Cited by 172
Self-citationThe terrestrial biota prior to the origin of land plants (embryophytes): a review of the evidence
Wellman, C. H., & Strother, P. K. (2015) · Palaeontology · doi:10.1111/pala.12172 · Cited by 155
Shih, P. M., & Matzke, N. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305813110 · Cited by 151
Evolution and Cytological Diversification of the Green Seaweeds (Ulvophyceae)
Cocquyt, E., Verbruggen, H., Leliaert, F., & Clerck, O. D. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq091 · Cited by 149
Sterol and genomic analyses validate the sponge biomarker hypothesis
Gold, D. A., Grabenstatter, J., de Mendoza, A., Riesgo, A., Ruiz-Trillo, I., & Summons, R. E. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1512614113 · Cited by 145
Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds
Cortona, A. D., Jackson, C. J., Bucchini, F., Bel, M. V., D’hondt, S., Škaloud, P., Delwiche, C. F., Knoll, A. H., Raven, J. A., Verbruggen, H., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1910060117 · Cited by 134
Yang, D., Xu, W., Xu, Y., Wang, Q., Pei, F., & Wang, F. (2012) · Precambrian Research · doi:10.1016/j.precamres.2012.07.002 · Cited by 121
Proterozoic photosynthesis – a critical review
Butterfield, N. J. F. (2015) · Palaeontology · doi:10.1111/pala.12211 · Cited by 120
Zhang, S., Zhao, Y. J., Hao, Y., & Hu, G. (2015) · Precambrian Research · doi:10.1016/j.precamres.2015.11.005 · Cited by 117
Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals
Zumberge, J. A., Love, G. D., Cárdenas, P., Sperling, E. A., Gunasekera, S., Rohrssen, M., Grosjean, E., Grotzinger, J. P., & Summons, R. E. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0676-2 · Cited by 114
Proterozoic phytoplankton and timing of Chlorophyte algae origins
Moczydłowska, M., Landing, E., Zang, W., & Palacios, T. (2011) · Palaeontology · doi:10.1111/j.1475-4983.2011.01054.x · Cited by 110
Zhao, H., Zhang, S., Ding, J., Chang, L., Ren, Q., Li, H., Yang, T., & Wu, H. (2019) · Geological Society of America Bulletin · doi:10.1130/b35198.1 · Cited by 109
Gueneli, N., Mckenna, A. M., Ohkouchi, N., Boreham, C. J., Beghin, J., Javaux, E., & Brocks, J. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803866115 · Cited by 109
Morphologie und biologie der algen
Oltmanns, F. (1904) · G. Fischer eBooks · doi:10.5962/bhl.title.1660 · Cited by 108
Nagovitsin, K. E., Rogov, V. I., Marusin, V. V., Karlova, G. A., Kolesnikov, A. V., Bykova, N., & Grazhdankin, D. V. (2015) · Precambrian Research · doi:10.1016/j.precamres.2015.09.012 · Cited by 106
New phylogenetic hypotheses for the core Chlorophyta based on chloroplast sequence data
Fučíková, K., Leliaert, F., Cooper, E. D., Kaloud, P. Ĺ., D’hondt, S., Clerck, O. D., Gurgel, C. F. D., Lewis, L. A., Lewis, P. O., Lopez-Bautista, J. M., et al. (2014) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2014.00063 · Cited by 105
Tang, Q., Pang, K., Xiao, S., Yuan, X., Ou, Z., & Wan, B. (2013) · Precambrian Research · doi:10.1016/j.precamres.2013.07.019 · Cited by 103
Self-citationJackson, C., Knoll, A. H., Chan, C. X., & Verbruggen, H. (2018) · Scientific Reports · doi:10.1038/s41598-017-18805-w · Cited by 99
Parial, D., & Pal, R. (2014) · Journal of Applied Phycology · doi:10.1007/s10811-014-0355-x · Cited by 96
Oxygen, animals and aquatic bioturbation: An updated account
Butterfield, N. J. (2018) · Geobiology · doi:10.1111/gbi.12267 · Cited by 89
Cryogenian evolution of stigmasteroid biosynthesis
Hoshino, Y., Stroeva, A. R., Meredith, W., Snape, C. E., Poshibaev, V. V., Versteegh, G. J. M., Kuznetsov, N. B., Leider, A., van Maldegem, L. M., Neumann, M., et al. (2017) · Science Advances · doi:10.1126/sciadv.1700887 · Cited by 77
Self-citationZumberge, J. A., Rocher, D., & Love, G. D. (2020) · Geobiology · doi:10.1111/gbi.12378 · Cited by 73
Komárek, J., & Johansen, J. R. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-385876-4.00004-9 · Cited by 72
Schuster, A., Vargas, S., Knapp, I. S. S., Pomponi, S. A., Toonen, R. J., Erpenbeck, D., & Wörheide, G. (2018) · BMC Evolutionary Biology · doi:10.1186/s12862-018-1230-1 · Cited by 70
Xiao, S., & Tang, Q. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20170165 · Cited by 64
Self-citationPrimary Productivity of Marine Ecosystems
Bunt, J. S. (1975) · Ecological studies · doi:10.1007/978-3-642-80913-2_8 · Cited by 59
Evolution of the Chlorophyta: Insights from chloroplast phylogenomic analyses
Fang, L., Leliaert, F., Zhang, Z., Penny, D., & Zhong, B. (2017) · Journal of Systematics and Evolution · doi:10.1111/jse.12248 · Cited by 59
Ontogenetic diversity of sclerotia of Sclerotinia sclerotiorum and related species
Willetts, H. J., & Wong, A. (1971) · Transactions of the British Mycological Society · doi:10.1016/s0007-1536(71)80066-9 · Cited by 39
Morphogenesis in the red alga, Griffithsia pacifica: Regeneration from single cells
Duffield, E. C. S., Waaland, S. D., & Cleland, R. E. (1972) · Planta · doi:10.1007/bf00385390 · Cited by 35
A revision ofCladophoropsisBørgesen (Siphonocladales, Chlorophyta)
Leliaert, F., & Coppejans, E. (2006) · Phycologia · doi:10.2216/06-07.1 · Cited by 34
Zhao, Z., Zhu, H., Liu, G., & Hu, Z. (2016) · Fottea · doi:10.5507/fot.2015.024 · Cited by 18
Wang, Y., Xu, H., Wang, Y., & Fu, Q. (2018) · Review of Palaeobotany and Palynology · doi:10.1016/j.revpalbo.2018.05.008 · Cited by 18
A discovery of riphean heterotrophs in the Lakhanda group of Siberia
Hermann, T. N., & Podkovyrov, V. N. (2010) · Paleontological Journal · doi:10.1134/s0031030110040027 · Cited by 18
Zhu, H., Zhao, Z., Liu, X., Song, H., Liu, G., & Hu, Z. (2018) · Phycologia · doi:10.2216/16-33.1 · Cited by 16
Zhao, Z., Zhu, H., Hu, Z., & Liu, G. (2014) · Phytotaxa · doi:10.11646/phytotaxa.166.4.3 · Cited by 16
Nowak, H., Harvey, T. H. P., Liu, H. P., McKay, R. M., Zippi, P., Campbell, D. H., & Servais, T. (2017) · Geobios · doi:10.1016/j.geobios.2017.06.005 · Cited by 11
Tsutsui, I., Miyoshi, T., Sukchai, H., Pinphoo, P., Aue-umneoy, D., Meeanan, C., Songphatkaew, J., Klomkling, S., Yamaguchi, I., Ganmanee, M., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0124997 · Cited by 11
Okuda, K., Sekida, S., Hasebe, A., Iwabuchi, M., Kamiya, M., & Hishinuma, T. (2016) · Phycological Research · doi:10.1111/pre.12139 · Cited by 7
Digging deeper: why we need more Proterozoic algal fossils and how to get them
Graham, L. (2018) · Journal of Phycology · doi:10.1111/jpy.12790 · Cited by 3
Akinete Formation in Vaucheria geminata
Randhawa, M. S. (1942) · Botanical Gazette · doi:10.1086/335099 · Cited by 3
Collins, A. G. (2000) · doi:10.1666/0094-8373(2000)026
Research works printed but not linked: 2
- Hermann, T. N. Filamentous microorganisms in the Lakhanda Formation on the Maya River. Paleontol. J. 1981, 100–107 (1981).
- Fryxell, G. A. Survival Strategies of the Algae (Cambrian Univ. Press, 1983).
Cited by
Sorted by citations
Strassert, J. F. H., Irisarri, I., Williams, T. A., & Burki, F. (2021) · Nature Communications · doi:10.1038/s41467-021-22044-z · Cited by 298
Cyanobacteria and biogeochemical cycles through Earth history
Sánchez-Baracaldo, P., Bianchini, G., Wilson, J. D., & Knoll, A. H. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2021.05.008 · Cited by 279
Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview
Lyons, T. W., Diamond, C. W., Planavsky, N. J., Reinhard, C. T., & Li, C. (2021) · Astrobiology · doi:10.1089/ast.2020.2418 · Cited by 211
“…to 1.6 Ga stem eukaryote remains (Zhu et al., 2016), and emergence of the crown group, expressed in simple multicellular red algae, is placed at *1.05 Ga (Butterfield, 2000; Gibson et al., 2018) and more recently with reports of macroscopic multicellular green algae at *1.0 Ga (Tang et al., 2020).”
BackgroundInfluentialHarris, 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
Sedimentary Ce anomalies: Secular change and implications for paleoenvironmental evolution
Zhang, K., & Shields, G. (2022) · Earth-Science Reviews · doi:10.1016/j.earscirev.2022.104015 · Cited by 162
Metadata
- Authors
- Tang, Q., Pang, K., Yuan, X., & Xiao, S.
- Affiliations
- Virginia Tech (US)
- Chinese Academy of Sciences (CN)
- Corresponding author
- Tang, Qing
- Xiao, Shuhai
- Venue
- Nature Ecology & Evolution
- Published
- 2020-02-24
- Volume
- 4
- Issue
- 4
- Pages
- 543-549
- ISSN
- 2397-334X (ISSN-L)
- PMC
- PMC8668152
- OpenAlex
- W3008173880
- Cited by
- 186
- References
- 69
- Citations by year
- 2026: 20 · 2025: 24 · 2024: 26 · 2023: 27 · 2022: 43 · 2021: 35 · 2020: 11
- FWCI
- 16.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature Ecology & Evolution (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Natural Science Foundation of China (41602007)
- National Aeronautics and Space Administration (80NSSC18K1086)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- 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
- Keywords
- Chlorophyta, evolution of multicellularity, benthic algae, cell differentiation, molecular clock, Neoproterozoic, Paleozoic
- MeSH terms
- Fossils, Phylogeny, Diatoms, Ecosystem
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review