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Reinvestigation of the occurrence of cutan in plants: implications for the leaf fossil record

  • Neal S. Gupta (a1) (a2), Margaret E. Collinson (a3), Derek E. G. Briggs (a4), Richard P. Evershed (a5) and Richard D. Pancost (a6)...

Cutan, a resistant non-hydrolyzable aliphatic biopolymer, was first reported in the cuticle of Agave americana and has generally been considered ubiquitous in leaf cuticles along with the structural biopolyester cutin. Because leaves and cuticles in the fossil record almost always have an aliphatic composition, it was argued that selective preservation of cutan played an important role in leaf preservation. However, the analysis of leaves using chemical degradation techniques involving hydrolysis to test for the presence of cutan reveals that it is absent in 16 of 19 taxa (angiosperm and gymnosperm), including many previously reported to contain cutan on the basis of pyrolysis data. Cutan is clearly much less widespread in leaves than previously thought, and its presence or absence does not exert any major bias on the preservation of leaves in the fossil record. In the absence of cutan, other constituents—cutin, plant waxes, and internal plant lipids—are incorporated into the geomacromolecule and contribute to the formation of a resistant aliphatic polymer by in situ polymerization during diagenesis.

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Almendros, G., González-Vila, F. J., Martin, F., Sanz, J., and Álvarez-Ramis, C. 1998. Appraisal of pyrolytic techniques on different forms of organic matter from a Cretaceous basement in Central Spain. Organic Geochemistry 28:613623.
Almendros, G., Dorado, J., González-Vila, F. J., Martin, F., Sanz, J., Álvarez-Ramis, J. C., and Stuchlik, L. 1999a. Molecular characterization of fossil organic matter in Glyptostrobus europaeus remains from the Orawa basin (Poland): comparison of pyrolytic techniques. Fuel 78:745752.
Almendros, G., Dorado, J., Sanz, J., Alvarez-Ramis, C., Fernández-Marrón, M. T., and Archangelsky, S. 1999b. Compounds released by sequential chemolysis from cuticular remains of the Cretaceous gymnosperm Squamastrobus tigrensis (Patagonia, the Argentine). Organic Geochemistry 30:623634.
Ambwani, K. 1991. Leaf impressions belonging to the Tertiary age of Northeast India. Phytomorphology 41:139146.
Baas, M., Briggs, D. E. G., van Heemst, J. D. H., Kear, A. J., and de Leeuw, J. W. 1995. Selective preservation of chitin during the decay of shrimp. Geochimica et Cosmochimica Acta 59:945951.
Bland, H. A., van Bergen, P. F., Carter, J. F., and Evershed, R. P. 1998. Early diagenetic transformations of proteins and polysaccharides in archaeological plant remains. In Stankiewicz, B. A. and van Bergen, P. F., eds. Nitrogen-containing macromolecules in the bio- and geosphere. ACS Symposium Series 707:113131. Oxford University Press, New York.
Boom, A., Sinninghe Damsté, J. S., and de Leeuw, J. W. 2005. Cutan, a common aliphatic biopolymer in cuticles of drought-adapted plants. Organic Geochemistry 36:595601.
Briggs, D. E. G. 1999. Molecular taphonomy of animal and plant cuticles: selective preservation and diagenesis. Philosophical Transactions of the Royal Society of London B 354:716.
Briggs, D. E. G., Evershed, R. P., and Lockheart, M. J. 2000. The biomolecular paleontology of continental fossils. In Erwin, D. H. and Wing, S. L., eds. Deep time: Paleobiology's perspective. Paleobiology 26(Suppl. to No. 4):169193.
Burnham, R. J. 1993. Reconstructing richness in the plant fossil record. Palaios 8:376384.
Burnham, R. J., Wing, S. L., and Parker, G. G. 1999. The reflection of deciduous forest communities in leaf litter—implications for autochthonous litter assemblages from the fossil record. Paleobiology 18:3049.
Challinor, J. M. 1989. A pyrolysis-derivatization-gas chromatograph technique for the elucidation of some synthetic polymers. Journal of Analytical and Applied Pyrolysis 16:323333.
Challinor, J. M. 1991a. Structure determination of alkyd resins by simultaneous pyrolysis methylation. Journal of Analytical and Applied Pyrolysis 18:233244.
Challinor, J. M. 1991b. The scope of pyrolysis methylation reactions. Journal of Analytical and Applied Pyrolysis 20:1524.
Chefetz, B. 2003. Sorption of phenanthrene and atrazine by plant cuticular fractions. Environmental Toxicology and Chemistry 22:24922498.
Collinson, M. E. 1992. The early fossil history of Salicaceae: a brief review. Proceedings of the Royal Society of Edinburgh B 98:155167.
Collinson, M. E., and Hooker, J. J. 2003. Paleogene vegetation of Eurasia: framework for mammalian faunas. Deinsea 10:4183.
Collinson, M. E., Boulter, M. C., and Holmes, P. R. 1993. Magnoliophyta (“Angiospermae”). Pp. 809841in Benton, M. J., ed. The fossil record 2. Chapman and Hall, London.
Collinson, M. E., Mösle, B., Finch, P., Scott, A. C., and Wilson, R. 1998. The preservation of plant cuticle in the fossil record: a chemical and microscopical investigation. Ancient Biomolecules 2:251265.
Collinson, M. E., Mösle, B., Finch, P., Wilson, R., and Scott, A. C. 2000. Preservation of plant cuticles. Acta Palaeobotanica 2(Suppl.):629632.
Crane, P. R. 1989. Early fossil history and evolution of the Betulaceae. In Crane, P. R. and Blackmore, S., eds. Evolution, systematics and fossil history of the Hamamelidae, Vol. 2. ‘Higher’ Hamamelidae. Systematics Association Special Volume 40B:86116. Clarendon, Oxford.
Crepet, W. L., and Nixon, K. C. 1998. Fossil Clusiaceae from the Late Cretaceous (Turonian) of New Jersey and implications regarding the history of bee pollination. American Journal of Botany 85:11221133.
Daghlian, C. P., and Crepet, W. L. 1983. Oak catkins, leaves and fruits from the Oligocene Catahoula Formation and their evolutionary significance. American Journal of Botany 70:639649.
de Leeuw, J. W., and Baas, M. 1993. The behavior of esters in the presence of tetramethylammonium salts at elevated temperatures; flash pyrolysis or flash chemolysis? Journal of Analytical and Applied Pyrolysis 26:175184.
de Leeuw, J. W., and Largeau, C. 1993. A review of macromolecular organic compounds that comprise living organisms and their role in kerogen, coal and petroleum formation. Pp. 2372in Engel, M. H. and Macko, S. A., eds. Organic geochemistry: principles and applications. Plenum, New York.
Deshmukh, A. P., Simpson, A. J., and Hatcher, P. G. 2003. Evidence for cross-linking in tomato cutin using HR-MAS NMR spectroscopy. Phytochemistry 64:11631170.
Eglinton, G., and Hamilton, R. J. 1967. Leaf epicuticular waxes. Science 156:13221334.
Ewbank, G., Edwards, D., and Abbott, G. D. 1996. Chemical characterization of Lower Devonian vascular plants. Organic Geochemistry 25:461473.
Finch, P., and Freeman, G. 2001. Simulated diagenesis of plant cuticles—implications for organic fossilisation. Journal of Analytical and Applied Pyrolysis 58:229235.
Fotyanova, L. I. 1997. Lobed-dentate oaks from the Eocene of eastern Asia. Paleontological Journal 31:225234.
Glasspool, I. J., Hilton, J., Collinson, M. E., and Wang, Shi-Jun 2003. Foliar herbivory in Late Palaeozoic Cathaysian gigantopterids. Review of Palaeobotany and Palynology 127:125132.
Glasspool, I. J., Hilton, J., Collinson, M. E., Wang, Shi-Jun, and Li, Cheng-Sen 2004. Foliar physiognomy in Cathaysian gigantopterids and the potential to track Palaeozoic climates using extinct plant groups. Palaeogeography, Palaeoclimatology, Palaeoecology 205:69110.
Gupta, N. S., and Pancost, R. D. 2004. Biomolecular and physical taphonomy of angiosperm leaf in early decay: implications for fossilisation. Palaios 19:428440.
Gupta, N. S., Briggs, D. E. G., Collinson, M. E., Evershed, R. P., Michels, R., Jack, K. S., and Pancost, R. D.In press a. Evidence for the in situ polymerization of labile aliphatic organic compounds during the preservation of fossil leaves: implications for organic matter preservation. Organic Geochemistry.
Gupta, N. S., Briggs, D. E. G., Collinson, M. E., Evershed, R. P., Michels, R., and Pancost, R. D.In press b. Molecular preservation of plant and insect cuticles from the Oligocene Enspel Formation, Germany: evidence against derivation of aliphatic polymer from sediment. Organic Geochemistry.
Hably, L., Kvaček, Z., and Manchester, S. R. 2000. Shared taxa of land plants in the Oligocene of Europe and North America in context of Holarctic phytogeography. Acta Universitatis Carolinae, Geologica 44:5974.
Herendeen, P. S., and Crane, P. R. 1995. The fossil history of the monocotyledons. Pp. 121in Rudall, P. J., Cribb, P. J., Cutler, D. F., and Humphries, C. J., eds. Monocotyledons: systematics and evolution. Royal Botanic Gardens, Kew.
Herzog, B., Hoffmann, S., Hartung, W., and Lüttge, U. 1999. Comparison of photosynthetic responses of the sympatric tropical species Clusia multiflora H.B.K. and the C3-CAM intermediate species Clusia minor L. to irradiance and drought stress in a phytotron. Plant Biology 1:460470.
Hill, R. S., ed. 1994. History of the Australian vegetation Cretaceous to Recent. Cambridge University Press, Cambridge.
Hill, R. S. 2004. Origins of the southeastern Australian vegetation. Philosophical Transactions of the Royal Society of London B 359:15371549.
Jacobs, B. F. 2002. Estimation of low latitude palaeoclimates using fossil angiosperm leaves: an example from the Miocene Tugen Hills, Kenya. Paleobiology 28:399421.
Jones, T. P., and Rowe, N. P., eds. 1999. Fossil plants and spores: modern techniques. Geological Society, London.
Kolattukudy, P. E. 1980. Biopolyester membranes of plants: cutin and suberin. Science 208:9901000.
Kowalski, E. A. 2002. Mean annual temperature estimation based on leaf morphology: a test from tropical South America. Palaeogeography, Palaeoclimatology, Palaeoecology 188:141165.
Kowalski, E. A., and Dilcher, D. L. 2003. Warmer paleotemperatures for terrestrial ecosystems. Proceedings of the National Academy of Sciences USA 100:167170.
Kvaček, Z., and Rember, W. C. 2000. Shared Miocene conifers of the Clarkia flora and Europe. Acta Universitatis Carolinae, Geologica 44:7585.
Kvaček, Z., and Walther, H. 1989. Paleobotanical studies in Fagaceae of the European Tertiary. Plant Systematics and Evolution 162:213229.
Kvaček, Z., and Walther, H. 1998. The Oligocene volcanic flora of Kundratice near Litomerice, ceske Stredohori volcanic complex (Czech Republic)—a review. Acta Musei Nationalis Prague, ser. B, Historia Naturalis 54:142.
Lee, S., and Wen, J. 2001. A phylogenetic analysis of Prunus and the Amygdaloideae (Rosaceae) using ITS sequences of nuclear ribosomal DNA. American Journal of Botany 88:150160.
LePage, B. A., Williams, C. J., and Yang, H. 2005. The geobiology and ecology of Metasequoia. Kluwer Academic, Dordrecht.
Liang, M.-M., Bruch, A., Collinson, M., Mosbrugger, V., Li, C.-S., Sun, Q.-G., and Hilton, J. 2003. Testing the climatic estimates from different palaeobotanical methods: an example from the Middle Miocene Shanwang flora of China. Palaeogeography, Palaeoclimatology, Palaeoecology 198:279301.
Liu, Y. S., Guo, S.-X., and Ferguson, D. K. 1996. Catalogue of Cenozoic megafossil plants in China. Palaeontographica, Abteilung B 238:77139.
Logan, G. A., Boon, J. J., and Eglinton, G. 1993. Structural biopolymer preservation in Miocene leaf fossils from the Clarkia site, Northern Idaho. Proceedings of the National Academy of Sciences USA 90:22462250.
Logan, G. A., Smiley, C. J., and Eglinton, G. 1995. Preservation of fossil leaf waxes in association with their source tissues, Clarkia, northern Idaho, USA. Geochimica et Cosmochimica Acta 59:751763.
Lüttge, U. 1999. One morphotype, three physiotypes: sympatric species of Clusia with obligate C3 photosynthesis, obligate CAM and C3-CAM intermediate behaviour. Plant Biology 1:138148.
Mai, D. H. 1984. Karpologische Untersuchungen der Steinkerne fossiler und rezenter Amygdalaceae (Rosales). Feddes Repertorium 95:299329.
Mai, D. H. 1995. Tertiäre Vegetationsgeschichte Europas. Gustav Fischer, Jena.
Mai, D. H., and Walther, H. 1991. Die Oligozänen und untermiozänen Floren NW-Sachsens und des Bitterfelder Raumes. Abhandlungen Staatlichen Museums für Mineralogie und Geologie zu Dresden 38:1230.
Martin, F., Gonzalez-Vila, F. J., del Río, J. C., and Verdejo, T. 1994. Pyrolysis derivatization of humic substances 1. Pyrolysis of fulvic acids in the presence of tetramethylammonium hydroxide. Journal of Applied and Analytical Pyrolysis 28:7180.
McKinney, D. E., Bortiatynski, J. M., Carson, D. M., Clifford, D. J., de Leeuw, J. W., and Hatcher, P. G. 1996. Tetramethylammonium hydroxide thermochemolysis of the aliphatic biopolymer cutan: insights into the chemical structure. Organic Geochemistry 24:641650.
Mösle, B., Finch, P., Collinson, M. E., and Scott, A. C. 1997. Comparison of modern and fossil plant cuticles by selective chemical extraction monitored by flash pyrolysis-gas chromatography-mass spectrometry and electron microscopy. Journal of Analytical and Applied Pyrolysis 40–41:585597.
Mösle, B., Collinson, M. E., Finch, P., Stankiewicz, B. A., Scott, A. C., and Wilson, R. 1998. Factors influencing the preservation of plant cuticles: a comparison of morphology and chemical composition of modern and fossil examples. Organic Geochemistry 29:13691380.
Mösle, B., Collinson, M. E., Scott, A. C., and Finch, P. 2002. Chemosystematic and microstructural investigations on Carboniferous seed plant cuticles from four North American localities. Review of Palaeobotany and Palynology 120:4152.
Nip, M., Tegelaar, E. W., Brinkhuis, H., de Leeuw, J. W., Schenk, P. A., and Holloway, P. J. 1986a. Analysis of modern and fossil plant cuticles by Curie point Py-GC and Curie point Py-GC-MS: recognition of a new, highly aliphatic and resistant biopolymer. Organic Geochemistry 10:769778.
Nip, M., Tegelaar, E. W., de Leeuw, J. W., and Schenk, P. A. 1986b. A new nonsaponifiable highly aliphatic and resistant biopolymer in plant cuticles. Naturwissenschaften 73:579585.
Palamarev, E. H., and Petkova, A. S. 1987. Les fossiles de Bulgarie VIII. 1. La Macroflore du Sarmatien. Bulgarian Academy of Sciences, Sofia. [In Bulgarian, French summary.]
Poirier, N., Derenne, S., Rouzaud, J.-N., Largeau, C., Mariotti, A., Balesdent, J., and Maquet, J. 2000. Chemical structure and sources of the macromolecular, resistant, organic fraction isolated from a forest soil (Lacadée, south-west France). Organic Geochemistry 31:813827.
Prochazka, M., and Buzek, C. 1975. Maple leaves from the Tertiary of North Bohemia. Rozpravy Ustredniho Ustavu Geologickeho 41:186.
Ralph, J., and Hatfield, R. D. 1991. Pyrolysis-GC-MS characterization of forage materials. Journal of Agricultural Food Chemistry 39:14261437.
Royer, D. L., Wilf, P., Janesko, D. A., Kowalski, E. A., and Dilcher, D. L. 2005. Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. American Journal of Botany 92:11411151.
Royer, D. L., Wing, S. L., Beerling, D. J., Jolley, D. W., Koch, P. L., Hickey, L. J., and Berner, R. A. 2001. Paleobotanical evidence for near present-day levels of atmospheric CO2 during parts of the Tertiary. Science 292:23102313.
Schmidt, H. W., and Schönherr, J. 1982. Development of plant cuticles: occurrence and role of non-ester bonds in cutin of Clivia miniata Reg. leaves. Planta 156:380384.
Schouten, S., Moerkerken, P., Gelin, F., Baas, M., de Leeuw, J. W., and Sinninghe Damsté, J. S. 1998. Structural characterization of aliphatic, non-hydrolyzable biopolymers in freshwater algae and a leaf cuticle using ruthenium tetroxide degradation. Phytochemistry 49:987993.
Stankiewicz, B. A., Mastalerz, M., Kruge, M. A., van Bergen, P. F., and Sadowska, A. 1997. A comparative study of modern and fossil cone scale and seeds of conifers: a geochemical approach. New Phytologist 135:375393.
Stankiewicz, B. A., Poinar, H. N., Briggs, D. E. G., Evershed, R. P., and Poinar, G. O. Jr. 1998a. Chemical preservation of plants and insects in natural resins. Proceedings of the Royal Society of London B 265:641647.
Stankiewicz, B. A., Scott, A. C., Collinson, M. E., Finch, P., Mösle, B., Briggs, D. E. G., and Evershed, R. P. 1998b. Molecular taphonomy of arthropod and plant cuticles from the Carboniferous of North America: implications for the origin of kerogen. Journal of the Geological Society, London 155:453462.
Stankiewicz, B. A., Briggs, D. E. G., Michels, R., Collinson, M. E., and Evershed, R. P. 2000. Alternative origin of aliphatic polymer in kerogen. Geology 28:559562.
Sun, B. N., Dilcher, D. L., Beerling, D. J., Zhang, C. J., Yan, D., and Kowalski, E. 2003. Variation in Ginkgo biloba L. leaf characters across a climatic gradient in China. Proceedings of the National Academy of Sciences USA 100:71417146.
Tanai, T. 1995. Fagaceous leaves from the Paleogene of Hokkaido, Japan. Bulletin of the National Science Museum, Tokyo, C 21:71101.
Tegelaar, E. W., de Leeuw, J. W., Derenne, S., and Largeau, C. 1989a. A reappraisal of kerogen formation. Geochimica et Cosmochimica Acta 53:31033106.
Tegelaar, E. W., de Leeuw, J. W., and Holloway, P. J. 1989b. Some mechanisms of flash pyrolysis of naturally occurring higher plant polyesters. Journal of Analytical and Applied Pyrolysis 15:289295.
Tegelaar, E. W., de Leeuw, J. W., Largeau, C., Derenne, S., Schulten, H.-R., Muller, R., Boon, J. J., Nip, M., and Sprenkels, J. C. M. 1989c. Scope and limitations of several pyrolysis methods in the structural elucidation of a macromolecular plant constituent in the leaf cuticle of Agave americana L. Journal of Analytical and Applied Pyrolysis 15:2954.
Tegelaar, E. W., Kerp, H., Visscher, H., Schenk, P. A., and de Leeuw, J. W. 1991. Bias of the paleobotanical record as a consequence of variations in the chemical composition of higher vascular plant cuticles. Paleobiology 17:133144.
Tegelaar, E. W., Wattendorff, J., and de Leeuw, J. W. 1993. Possible effects of chemical heterogeneity in higher land plant cuticles on the preservation of its ultrastructure upon fossilization. Review of Palaeobotany and Palynology 77:149170.
van Bergen, P. F. 1999. Pyrolysis and chemolysis of fossil plant remains: applications to palaeobotany. Pp. 143148in Jones, T. P. and Rowe, N. P., eds. Fossil plants and spores: modern techniques. Geological Society, London.
van Bergen, P. F., Scott, A. C., Barrie, P. J., de Leeuw, J. W., and Collinson, M. E. 1994. The chemical composition of Upper Carboniferous pteridosperm cuticles. Organic Geochemistry 21:107117.
van Bergen, P. F., Collinson, M. E., Briggs, D. E. G., de Leeuw, J. W., Scott, A. C., Evershed, R. P., and Finch, P. 1995. Resistant biomacromolecules in the fossil record. Acta Botanica Neerlandica 44:319342.
van Bergen, P. F., Flannery, M. B., Poulton, P. R., and Evershed, R. P. 1998. Organic geochemical studies of soils from Rothamsted Experimental Station: III Nitrogen-containing organic matter in soil from Geescroft Wilderness. In Stankiewicz, B. A. and van Bergen, P. F., eds. Nitrogen-containing macromolecules in the bio- and geosphere. ACS Symposium Series 707:321338. Oxford University Press, New York.
Villena, J. F., Dominguez, E., Stewart, D., and Heredia, A. 1999. Characterization and biosynthesis of non-degradable polymers in plant cuticles. Planta 208:181187.
Walther, H. 1999. Die Tertiärflora von Kleinsaubernitz bei Bautzen. Palaeontographica, Abteilung B 249:63174.
Walton, T. J. 1990. Waxes, cutin and suberin. Pp. 105159in Dey, P. M. and Harborne, J., eds. Methods in plant biochemistry, Vol. 4. Lipids, membranes and aspects of photobiology. Academic Press, San Diego.
Wiemann, M. C., Manchester, S. R., Dilcher, D. L., Hinojosa, L. F., and Wheeler, E. A. 1998. Estimation of temperature and precipitation from morphological characters of dicotyledon leaves. American Journal of Botany 85:17961802.
Wijninga, V. M. 1996. Paleobotany and palynology of Neogene sediments from the high plain of Bogota (Colombia), Chapter 2. Geochemical characterisation of Neogene Organic deposits from Colombia. Ph.D. thesis. University of Amsterdam, Amsterdam. Printed in Wageningen. Published by the author. ISBN 90-9009414–8.
Wilf, P. 1997. When are leaves good thermometers? A new case for Leaf Margin Analysis. Paleobiology 23:373390.
Wilf, P., Cuneo, N. R., Johnson, K. R., Hicks, J. F., Wing, S. L., and Obradovich, J. D. 2003. High plant diversity in Eocene South America: evidence from Patagonia. Science 300:122125.
Wing, S. L., Harrington, G. J., Smith, F. A., Bloch, J. I., Boyer, D. M., and Freeman, K. H. 2005. Transient floral change and rapid global warming at the Paleocene-Eocene boundary. Science 310:993996.
Wolfe, J. A. 1995. Paleoclimatic estimates from Tertiary leaf assemblages. Annual Review of Earth and Planetary Sciences 23:119142.
Wolfe, J. A., and Tanai, T. 1987. Systematics, phylogeny and distribution of Acer (maples) in the Cenozoic of western North America. Journal of the Faculty of Sciences Hokkaido University 22:1246.
Xiao, F.-M., Goodwin, S. M., Xiao, Y., Sun, Z., Baker, D., Tang, X., Jenks, M. A., and Zhou, J.-M. 2004. Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. The EMBO (European Molecular Biology Organisation) Journal 23:29032913.
Yang, H., Huang, Y., Leng, Q., LePage, B. A., and Williams, C. J. 2005. Biomolecular preservation of Tertiary Metasequoia fossil lagerstätten revealed by comparative pyrolysis analysis. Review of Palaeobotany and Palynology 134:237256.
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