Advertisement
No access
Reports

Molecular Evidence for the Early Colonization of Land by Fungi and Plants

Science
10 Aug 2001
Vol 293, Issue 5532
pp. 1129-1133

Abstract

The colonization of land by eukaryotes probably was facilitated by a partnership (symbiosis) between a photosynthesizing organism (phototroph) and a fungus. However, the time when colonization occurred remains speculative. The first fossil land plants and fungi appeared 480 to 460 million years ago (Ma), whereas molecular clock estimates suggest an earlier colonization of land, about 600 Ma. Our protein sequence analyses indicate that green algae and major lineages of fungi were present 1000 Ma and that land plants appeared by 700 Ma, possibly affecting Earth's atmosphere, climate, and evolution of animals in the Precambrian.

Get full access to this article

View all available purchase options and get full access to this article.

REFERENCES AND NOTES

1
Gray J., Shear W., Am. Sci. 80, 444 (1992).
2
Horodyski R. J., Knauth L. P., Science 263, 494 (1994).
3
Pirozynski K. A., Malloch D. W., Biosystems 6, 153 (1975).
4
Selosse M.-A., LeTacon F., Trends Ecol. Evol. 13, 15 (1998).
5
Remy W., Taylor T. N., Hass H., Kerp H., Proc. Natl. Acad. Sci. U.S.A. 91, 11841 (1994).
6
Redecker D., Kodner R., Graham L. E., Science 289, 1920 (2000).
7
Taylor T. N., Hass H., Remy W., Kerp H., Nature 378, 244 (1995).
8
Retallack G. J., Paleobiology 20, 523 (1994).
9
M. L. Berbee, J. W. Taylor, in The Mycota, vol. VIIB, Systematics and Evolution, D. J. McLaughlin, E. McLaughlin, Eds. (Springer-Verlag, New York, 2000), pp. 229–246.
10
Sequences were aligned with Clustal W (38), and upon visual inspection of the alignments, highly divergent prokaryote sequences were omitted. Neighbor-joining trees were constructed from the alignments with MEGA (39) (complete-deletion, gamma distance), and only orthologous groups were used in subsequent analyses. Paralogous groups were identified by branching orders suggesting gene duplication, and omitted. If available, eukaryotic taxa basal to the divergence of plants, animals, and fungi were used as outgroups in rate tests. If eukaryotic sequences were unavailable, prokaryotes were used as outgroups.
11
C. J. Alexopoulos, C. W. Mims, M. Blackwell, Introductory Mycology (Wiley, New York, ed. 4, 1996).
12
James T. Y., Porter D., Leander C. A., Vilgalys R., Longcore J. E., Can. J. Bot. 78, 336 (2000).
13
For the green algal and bryophyte divergences, 48 proteins averaging 292 amino acids, and 54 proteins averaging 103 amino acids, respectively, were obtained for analyses. The Physcomitrella sequences (Leeds/Wash U. Moss EST Project) were trimmed by 10% at the 3′ end before analysis, and all alignments were checked visually to guard against expressed sequence tag (EST)–related sequence errors. Available tracheophytes were used, including Arabidopsis, Brassica, Nicotiana, Oryza, Pisum, Solanum, and Zea.
14
Wang D. Y.-C., Kumar S., Hedges S. B., Proc. R. Soc. London B. 266, 163 (1999).
15
We estimated divergence times using the animal-plant-fungus divergence (1576 Ma), the nematode-chordate and nematode-arthropod divergence (1177 Ma), and the arthropod-chordate divergence (993 Ma) as calibration points (14).
16
Hedges S. B., Parker P. H., Sibley C. G., Kumar S., Nature 381, 226 (1996).
17
Kumar S., Hedges S. B., Nature 392, 917 (1998).
18
Nei M., Xu P., Glazko G., Proc. Natl. Acad. Sci. U.S.A. 98, 2497 (2001).
19
Gene-specific rates of sequence change were estimated by linear regression (y intercept fixed through the origin) from one or more of these calibrations and applied to the intergroup distance estimations (40) to produce gene-specific time estimates. Single-gene time estimates were averaged to obtain multigene times (16, 17). Where sufficient numbers of proteins (>35) were available, modes were used rather than means to reduce possible error from paralogous comparisons (17). For the average-distance method, time estimates were made by weighting individual gene distances and rates by sequence length, and dividing summed distances by summed rates (18).
20
Gene-specific gamma parameters were calculated and used for distance and time estimation (41). Gamma parameters averaged 1.25 and 1.19 (all genes, rate-constant genes) for the fungal alignments, 2.51 and 2.73 for the green algal alignments, and 1.58 and 1.63 for the land-plant alignments. Relative rate tests (42) were conducted with PHYLTEST (40). Analyses were performed for constant-rate genes and all genes. Sequence alignments, accession numbers, gene-specific gamma parameters, and other supplementary data are available at www.evogenomics.org/publications/data/fungi/.
21
Simon L., Bousquet J., Levesque R. C., Lalonde M., Nature 363, 67 (1993).
22
Doolittle R. F., Feng D.-F., Tsang S., Cho G., Little E., Science 271, 470 (1996).
23
Feng D.-F., Cho G., Doolittle R. F., Proc. Natl. Acad. Sci. U.S.A. 94, 13028 (1997).
24
Taylor T. N., Hass H., Kerp H., Nature 399, 648 (1999).
25
Butterfield N. J., Paleobiology 26, 386 (2000).
26
Moreira D., LeGuyader H., Philippe H., Nature 405, 69 (2000).
27
Goremykin V. V., Hansmann S., Martin W. F., Plant Syst. Evol. 206, 337 (1997).
28
Gehrig H., Schubler A., Kluge M., J. Mol. Evol. 43, 71 (1996).
29
Evans R. D., Johansen J. R., Crit. Rev. Plant Sci. 18, 183 (1999).
30
Watanabe Y., Martini J. E. J., Ohmoto H., Nature 408, 574 (2000).
31
D. Schwartzman, Life, Temperature, and the Earth (Columbia Univ. Press, New York, 1999).
32
Kenrick P., Crane P. R., Nature 389, 33 (1997).
33
Hoffman P. F., Kaufman A. J., Halverson G. P., Schrag D. P., Science 281, 1342 (1998).
34
Knoll A. H., Science 256, 622 (1992).
35
Crowley T. J., Berner R. A., Science 292, 870 (2001).
36
Kroken S., Graham L., Cook M., Am. J. Bot. 83, 1241 (1996).
37
Kump L. R., Nature 335, 152 (1988).
38
Thompson J. D., Higgins D. G., Gibson T. J., Nucleic Acids Res. 22, 4673 (1994).
39
S. Kumar, K. Tamura, M. Nei, MEGA: Molecular Evolutionary Genetic Analysis (Pennsylvania State University, University Park, PA, 1993).
40
S. Kumar, Phyltest: A Program for Testing Phylogenetic Hypotheses (Institute of Molecular Evolutionary Genetics, Pennsylvania State University, University Park, PA, ed. 2.0, 1996).
41
Yang Z., CABIOS (Comput. Appl. Biosci.) 13, 555 (1997).
42
Takezaki N., Rzhetsky A., Nei M., Mol. Biol. Evol. 12, 823 (1995).
43
We thank M. Ray for assistance with data collection and L. E. Graham, J. F. Kasting, A. H. Knoll, L. R. Kump, and D. Schwartzman for comments or discussion. N.L.K. was supported by Women in Science and Engineering Research (NASA Space Grant to Penn State). Supported by grants from the NASA Astrobiology Institute (to S.B.H.).

(0)eLetters

eLetters is a forum for ongoing peer review. eLetters are not edited, proofread, or indexed, but they are screened. eLetters should provide substantive and scholarly commentary on the article. Embedded figures cannot be submitted, and we discourage the use of figures within eLetters in general. If a figure is essential, please include a link to the figure within the text of the eLetter. Please read our Terms of Service before submitting an eLetter.

Log In to Submit a Response

No eLetters have been published for this article yet.

Information & Authors

Information

Published In

Science
Volume 293 | Issue 5532
10 August 2001

Submission history

Received: 9 April 2001
Accepted: 8 June 2001
Published in print: 10 August 2001

Permissions

Request permissions for this article.

Authors

Affiliations

Daniel S. Heckman
Astrobiology Research Center and Department of Biology,
David M. Geiser
Department of Plant Pathology, Pennsylvania State University, University Park, PA 16802, USA.
Brooke R. Eidell
Astrobiology Research Center and Department of Biology,
Rebecca L. Stauffer
Astrobiology Research Center and Department of Biology,
Natalie L. Kardos
Astrobiology Research Center and Department of Biology,
S. Blair Hedges*
Astrobiology Research Center and Department of Biology,

Notes

*
To whom correspondence should be addressed: Department of Biology, 208 Mueller Laboratory, Pennsylvania State University, University Park, PA 16802, USA; e-mail: [email protected]

Metrics & Citations

Metrics

Article Usage

Altmetrics

Citations

Cite as

Export citation

Select the format you want to export the citation of this publication.

Cited by

  1. Mycorrhizal Symbiosis for Sustainable Optimization of Tropical Agriculture: A Review of Research, Symbiosis in Nature [Working Title], (2023).https://doi.org/10.5772/intechopen.110084
    Crossref
  2. The Hydroponic Rockwool Root Microbiome: Under Control or Underutilised?, Microorganisms, 11, 4, (835), (2023).https://doi.org/10.3390/microorganisms11040835
    Crossref
  3. Re-Evaluating Botryosphaeriales: Ancestral State Reconstructions of Selected Characters and Evolution of Nutritional Modes, Journal of Fungi, 9, 2, (184), (2023).https://doi.org/10.3390/jof9020184
    Crossref
  4. From guest to host: parasite Cistanche deserticola shapes and dominates bacterial and fungal community structure and network complexity, Environmental Microbiome, 18, 1, (2023).https://doi.org/10.1186/s40793-023-00471-3
    Crossref
  5. ATM Activation and Its Recruitment to Damaged DNA Require Binding to the C Terminus of Nbs1, Molecular and Cellular Biology, 25, 13, (5363-5379), (2023).https://doi.org/10.1128/MCB.25.13.5363-5379.2005
    Crossref
  6. Regulation of Ras Localization and Cell Transformation by Evolutionarily Conserved Palmitoyltransferases, Molecular and Cellular Biology, 34, 3, (374-385), (2023).https://doi.org/10.1128/MCB.01248-13
    Crossref
  7. A Stress-Activated, p38 Mitogen-Activated Protein Kinase–ATF/CREB Pathway Regulates Posttranscriptional, Sequence-Dependent Decay of Target RNAs, Molecular and Cellular Biology, 33, 15, (3026-3035), (2023).https://doi.org/10.1128/MCB.00349-13
    Crossref
  8. Coevolutionary legacies for plant decomposition, Trends in Ecology & Evolution, 38, 1, (44-54), (2023).https://doi.org/10.1016/j.tree.2022.07.008
    Crossref
  9. Molecular record of the SPICE event in well YD2, Tarim Basin: Insights from catalytic hydropyrolysis of kerogens, Marine and Petroleum Geology, 148, (106038), (2023).https://doi.org/10.1016/j.marpetgeo.2022.106038
    Crossref
  10. Do all fungi have ancestors with endophytic lifestyles?, Fungal Diversity, (2023).https://doi.org/10.1007/s13225-023-00516-5
    Crossref
  11. See more
Loading...

View Options

Check Access

Log in to view the full text

AAAS ID LOGIN

AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.

Log in via OpenAthens.
Log in via Shibboleth.

More options

Register for free to read this article

As a service to the community, this article is available for free. Login or register for free to read this article.

Purchase this issue in print

Buy a single issue of Science for just $15 USD.

View options

PDF format

Download this article as a PDF file

Download PDF

Full Text

FULL TEXT

Media

Figures

Multimedia

Tables

Share

Share

Share article link

Share on social media