Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T07:18:36.093Z Has data issue: false hasContentIssue false

Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils

Published online by Cambridge University Press:  08 April 2016

David Winship Taylor
Affiliation:
Department of Biology, Indiana University Southeast, 4201 Grant Line Road, New Albany, Indiana 47150. E-mail: [email protected]
Hongqi Li
Affiliation:
Department of Biology, Indiana University Southeast, 4201 Grant Line Road, New Albany, Indiana 47150. E-mail: [email protected]
Jeremy Dahl
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305-2115
Fred J. Fago
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305-2115
David Zinniker
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305-2115
J. Michael Moldowan
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305-2115

Abstract

Recent molecular phylogenetic and molecular clock data both suggest a pre-Mesozoic age for the divergence of the angiosperm lineage from other seed plants, greatly predating the confirmed fossil record of the angiosperm crown group. In addition, molecular phylogenetic studies have not supported the morphologically based conclusion that gnetophytes are the extant sister group to angiosperms. We examine these relationships and divergence ages by using a novel approach of examining the presence of oleanane. This includes the development of methods using zeolites to preferentially reduce hopanes that can co-elute with oleanane. The presence of this molecular fossil strongly correlates with angiosperm diversification; in its functionalized form, along with its triterpenoid precursors, it is found in many living angiosperms. Our data show that among non-angiosperm seed plants examined thus far, oleanane is found only in fossil Cretaceous Bennettitales and Permian Gigantopteridales, both of which share characteristics with angiosperms. Previous morphological phylogenetic results indicate Bennettitales could be a sister group to or member of the angiosperm stem lineage, and results of our preliminary phylogenetic analysis including the Gigantopteridales suggests the same. Our data, based on a new pyrolysis method to treat living species, support previous research indicating that oleanane and its precursors are absent in living gnetophytes. If oleanane originated once in seed plants then the angiosperm stem lineage would have diverged from other seed plant lineages by the late Paleozoic.

Type
Articles
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Ageta, H., and Arai, Y. 1983. Fern constituents: pentacyclic triterpenoids isolated from Polypodium niponicum and P. formosanum . Phytochemistry 22:18011808.Google Scholar
Angiosperm Phylogeny Group. 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141:399436.Google Scholar
Arai, Y., Hirohara, M., Ogawa, R., Masuda, K., Shiojima, K., Ageta, H., Chang, H.-C., and Chen, Y.-P. 1996. Fern constituents: preoleanatetraene, a novel bicyclic triterpenoid hydrocarbon from Polypodioides formosana . Tetrahedron Letters 37:43814384.CrossRefGoogle Scholar
Baas, W. J. 1985. Naturally occurring Seco-Ring-A-Triterpenoids and their possible biological significance. Phytochemistry 24:18751889.Google Scholar
Bowe, L. M., Coat, G., and de Pamphilis, C. W. 2000. Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. Proceedings of the National Academy of Sciences USA 97:40924097.CrossRefGoogle ScholarPubMed
Brenner, G. J. 1996. Evidence for the earliest stage of angiosperm pollen evolution: a paleoequatorial section from Israel. Pp. 91115 in Taylor, and Hickey, 1996a.Google Scholar
Burleigh, J. G., and Mathews, S. 2004. Phylogenetic signal in nucleotide data from seed plants: implications for resolving the seed plant tree of life. American Journal of Botany 91:15991613.CrossRefGoogle ScholarPubMed
Caveney, S., Charlet, D. A., Freitag, H., Maier-Stolte, M., and Starratt, A. N. 2001. New observations of the secondary chemistry of world Ephedra (Ephedraceae). American Journal of Botany 88:11991208.Google Scholar
Cornet, B. 1996. A new gnetophyte from the Late Carnian (Late Triassic of Texas and its bearing on the origin of the angiosperm carpel and stamen. Pp. 3267 in Taylor, and Hickey, 1996a.CrossRefGoogle Scholar
Crane, P. R. 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanical Garden 72:716793.Google Scholar
Das, M. C., and Mahato, S. B. 1983. Triterpenoids. Phytochemistry 22:10711095.CrossRefGoogle Scholar
Doyle, J. A. 1992. Revised palynological correlations of the Potomac Group (USA) and the Cocobeach sequence of Gabon (Barremian-Aptian). Cretaceous Research 13:337349.CrossRefGoogle Scholar
Doyle, J. A. 1996. Seed plant phylogeny and the relationships of Gnetales. International Journal of Plant Sciences 157(Suppl.):S3S39.Google Scholar
Doyle, J. A. 1998. Molecules, morphology, fossils and the relationship of angiosperms and Gnetales. Molecular Phylogenetics and Evolution 9:448462.Google Scholar
Doyle, J. A., and Donoghue, M. J. 1993. Phylogenies and angiosperm diversification. Paleobiology 19:141167.CrossRefGoogle Scholar
Fensome, R. A., Macrae, R. A., Moldowan, J. M., Taylor, R. J. R., and Williams, G. L. 1996. The early Mesozoic radiation of dinoflagellates. Paleobiology 22:329338.Google Scholar
Goremykin, V., Bobrova, V. V., Pahnke, J., Troitsky, A., Antonov, A., and Martin, W. 1996. Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbcL data do not support gnetalean affinities of angiosperms. Molecular Biology and Evolution 13:383396.Google Scholar
Hickey, L. J., and Taylor, D. W. 1996. Origin of the angiosperm flower. Pp. 176231 in Taylor, and Hickey, 1996a.CrossRefGoogle Scholar
Hostettmann, K., and Marston, A. 1995. Saponins. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Hughes, N. F. 1994. The enigma of angiosperm origins. Cambridge University Press, Cambridge.Google Scholar
Qiang, Ji, Li, H., Bowe, L. M., Liu, Y., and Taylor, D. W. 2004. A new Archaefructus species from Early Cretaceous, China. Acta Geologica Sinica 78:883896.CrossRefGoogle Scholar
Li, H., and Taylor, D. W. 1998. Aculeovinea yunguiensis gen. et sp. nov., a new taxon of gigantopterid axis from the Upper Permian of Guizhou province, China. International Journal of Plant Sciences 159:10231033.CrossRefGoogle Scholar
Li, H., and Taylor, D. W. 1999. Vessel-bearing stems of Vasovinea tianii gen. et sp. nov. (Gigantopteridales) from the Upper Permian of Guizhou province. American Journal of Botany 86:15631675.Google Scholar
Li, H., Taylor, E. L., and Taylor, T. N. 1996. Permian vessel elements. Science 271:188189.CrossRefGoogle Scholar
Li, H., Tian, B., Taylor, E. L., and Taylor, T. N. 1994. Foliage anatomy of Gigantonoclea guizhouensis Gu et Zhi (Gigantopteridales) from the Upper Permian of Guizhou Province, China. American Journal of Botany 81:678689.Google Scholar
Maddison, W. P., and Maddison, D. R. 1992. Analysis of phylogeny and character evolution. Sinauer, Sunderland, Mass. Google Scholar
Magallón, S., and Sanderson, M. J. 2002. Relationships among seed plants inferred from highly conserved genes: sorting conflicting phylogenetic signals among ancient lineages. American Journal of Botany 89:19912006.CrossRefGoogle ScholarPubMed
Martin, W., Gierl, A., and Saedler, H. 1989. Molecular evidence for pre-Cretaceous angiosperm origins. Nature 339:648.CrossRefGoogle Scholar
Martin, W., Lydiate, D., Brinkmann, H., Forkmann, G., Saedler, H., and Cerff, R. 1993. Molecular phylogenies in angiosperm evolution. Molecular Biology and Evolution 10:40162.Google Scholar
Masuda, K., Shiojima, K., and Ageta, H. 1983. Fern constituents: six tetracyclic triterpenoid hydrocarbons having different carbon skeletons, isolated from Lemmaphyllum microphyllum var. obovatum . Chemical and Pharmaceutical Bulletin (Tokyo) 31:25302533.Google Scholar
Moldowan, J. M., and Talyzina, N. M. 1998. Biochemical evidence for dinoflagellate ancestors in the early Cambrian. Science 281:11681170.Google Scholar
Moldowan, J. M., Dahl, J., Huizinga, B. J., Fago, F. J., Hickey, L. J., Peakman, T. M., and Taylor, D. W. 1994. The molecular fossil record of oleanane and its relationship to angiosperms. Science 265:768771.Google Scholar
Moldowan, J. M., Dahl, J., Jacobson, S. R., Huizinga, B. J., Fago, F. J., Shetty, R., Watt, D. S., and Peters, K. E. 1996. Chemostratigraphic reconstruction of biofacies: molecular evidence linking cyst-forming dinoflagellates with pre-Triassic ancestors. Geology 24:159162.Google Scholar
Moldowan, J. M., Jacobson, S. R., Dahl, J., Al-Hajji, A., Huizinga, B. J., and Fago, F. J. 2001. Molecular fossils demonstrate Precambrian origin of dinoflagellates. Pp. 474493 in Zhuravelev, A. and Riding, R., eds. Ecology of the Cambrian radiation. Cambridge University Press, Cambridge.Google Scholar
Murray, A. P., Sosrowidojojo, I. B., Alexander, R., Kagi, R., Norgate, C. M., and Summons, R. E. 1997. Oleananes in oil and sediments: evidence of marine influence during early diagenesis. Geochimica et Cosmochimica Acta 61:12611276.Google Scholar
Nixon, K. C., Crepet, W. L., Stevenson, D., and Friis, E. M. 1994. A reevaluation of seed plant phylogeny. Annals of the Missouri Botanical Garden 81:484533.CrossRefGoogle Scholar
Pant, P., and Rastogi, R. P. 1979. The triterpenoids. Phytochemistry 18:10951108.CrossRefGoogle Scholar
Peters, K. E., and Moldowan, J. M. 1993. The biomarker guide: interpreting molecular fossils in petroleum and ancient sediments. Prentice Hall, Englewood Cliffs, N.J. Google Scholar
Peters, K. E., Clutson, M. J., and Robertson, G. 1999. Mixed marine and lacustrine input to an oil-cemented sandstone breccia from Brora, Scotland. Organic Geochemistry 30:237248.CrossRefGoogle Scholar
Pryer, K. M., Schneider, H., Smith, A. R., Cranfill, R., Wolf, P. G., Hunt, J. S., and Sipes, S. D. 2001. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618622.Google Scholar
Pryer, K. M., Schuettpelz, E., Wolf, P. G., Schneider, H., Smith, A. R., and Cranfill, R. 2004. Phylogeny and evolution of ferns (Monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany 91:15821598.Google Scholar
Rothwell, G. W., and Serbet, R. 1994. Lignophyte phylogeny and the evolution of spermatophytes: a numerical cladistic analysis. Systematic Botany 19:443482.CrossRefGoogle Scholar
Rullkötter, J., Peakman, T. M., and ten Haven, H. L. 1994. Early diagenesis of terrigenous triterpenoids and its implications for petroleum geochemistry. Organic Geochemistry 21:215233.CrossRefGoogle Scholar
Sanderson, M. J., and Doyle, J. A. 2001. Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. American Journal of Botany 88:14991516.Google Scholar
Sanderson, M. J., Thorne, J. L., Wilström, N., Bremer, K. 2004. Molecular evidence on plant divergence times. American Journal of Botany 91:16561665.Google Scholar
Schneider, J., Schuettpelz, E., Pryer, K. M., Cranfill, R., Magallón, S., and Lupia, R. 2004. Ferns diversified in the shadow of angiosperms. Nature 428:553557.Google Scholar
Soltis, D. E., Soltis, P. S., and Zanis, M. J. 2002. Phylogeny of seed plants based on evidence from eight genes. American Journal of Botany 89:16701681.CrossRefGoogle ScholarPubMed
Stewart, W. N., and Rothwell, G. W. 1993. Paleobotany and the evolution of plants, 2d ed. Cambridge University Press, Cambridge.Google Scholar
Sun, G., Dilcher, D. L., Zheng, S., and Zhou, Z. 1998. In search of the first flower: a Jurassic angiosperm, Archaefructus . Science 282:16921695.CrossRefGoogle Scholar
Sun, G., Ji, Q., Dilcher, D. L., Zheng, S., Nixon, K. C., and Wang, X. 2002. Archaefructaceae, a new basal angiosperm family. Science 296:899904.Google Scholar
Swofford, D. L. 2001. PAUP: phylogenetic analysis using parsimony ( and other methods), Version 4. Sinauer, Sunderland, Mass. Google Scholar
Taylor, D. W., and Hickey, L. J. 1996a. Flowering plant origin, evolution and phylogeny. Chapman and Hall, New York.Google Scholar
Taylor, D. W., and Hickey, L. J. 1996b. Evidence for and implications of an herbaceous origin for angiosperms. Pp. 232266 in Taylor, and Hickey, 1996a.CrossRefGoogle Scholar
Trapp, S., and Croteau, R. 2001. Defensive resin biosynthesis in conifers. Annual Review of Plant Physiology and Plant Molecular Biology 52:689724.Google Scholar
Wolfe, K. H., Gouy, J., Yang, Y.-W., Sharp, P. M., and Li, W.-H. 1989. Date of the monocot-dicot divergence estimate from chloroplast DNA sequence data. Proceedings of the National Academy of Sciences USA 86:62016205.Google Scholar