Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-23T11:16:27.967Z Has data issue: false hasContentIssue false

Multiscale 3D Virtual Dissections of 100-Million-Year-Old Flowers Using X-Ray Synchrotron Micro- and Nanotomography

Published online by Cambridge University Press:  07 January 2014

Jean-David Moreau*
Affiliation:
Université Rennes 1, CNRS UMR 6118 Géosciences Rennes, Campus de Beaulieu bât. 15, 263 avenue du Général Leclerc, 35042 Rennes, France European Synchrotron Radiation Facility, 6, rue J.-Horowitz, BP 220, 38043 Grenoble, France
Peter Cloetens
Affiliation:
European Synchrotron Radiation Facility, 6, rue J.-Horowitz, BP 220, 38043 Grenoble, France
Bernard Gomez
Affiliation:
Université Lyon 1 (Claude Bernard), CNRS UMR 5276 LGL-TPE, OSU Lyon, Campus La Doua, Bât. Géode, 43 boulevard du 11 Novembre 1918, 69622 Villeurbanne, France
Véronique Daviero-Gomez
Affiliation:
Université Lyon 1 (Claude Bernard), CNRS UMR 5276 LGL-TPE, OSU Lyon, Campus La Doua, Bât. Géode, 43 boulevard du 11 Novembre 1918, 69622 Villeurbanne, France
Didier Néraudeau
Affiliation:
Université Rennes 1, CNRS UMR 6118 Géosciences Rennes, Campus de Beaulieu bât. 15, 263 avenue du Général Leclerc, 35042 Rennes, France
Tamzin A. Lafford
Affiliation:
European Synchrotron Radiation Facility, 6, rue J.-Horowitz, BP 220, 38043 Grenoble, France
Paul Tafforeau
Affiliation:
European Synchrotron Radiation Facility, 6, rue J.-Horowitz, BP 220, 38043 Grenoble, France
*
*Corresponding author. E-mail: jean.david.moreau@gmail.com
Get access

Abstract

A multiscale approach combining phase-contrast X-ray micro- and nanotomography is applied for imaging a Cretaceous fossil inflorescence in the resolution range from 0.75 μm to 50 nm. The wide range of scale views provides three-dimensional reconstructions from the external gross morphology of the inflorescence fragment to the finest exine sculptures of in situ pollen. This approach enables most of the characteristics usually observed under light microscopy, or with low magnification under scanning and transmission electron microscopy, to be obtained nondestructively. In contrast to previous tomography studies of fossil and extant flowers that used resolutions down to the micron range, we used voxels with a 50 nm side in local tomography scans. This high level of resolution enables systematic affinities of fossil flowers to be established without breaking or slicing specimens.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2014 

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

Angiosperm Phylogeny Group (APG III). (2009). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants; APG III. Bot J Linn Soc 161, 105121.Google Scholar
Bench, G., Saint, A., Cholewa, M. & Legge, G.J.F. (1992). STIM tomography: A three-dimensional high resolution imaging tool. Nucl Instr Meth Phys Res 68, 481490.Google Scholar
Brenner, G.J. (1996). Evidence for the earliest stage of angiosperm pollen evolution: Palaeoequatorial section from Israel. In Flowering Plant Origin, Evolution and Phylogeny, Taylor, D.W. & Hickey, L.J. (Eds.), pp. 91115. New York: Chapman & Hall.Google Scholar
Cloetens, P., Baruchel, J., Van Dyck, D., Van Landuyt, J., Guigay, J.-P. & Schlenker, M. (1999). Holotomography: Quantitative phase tomography with micrometer resolution using hard synchrotron radiation X rays. Appl Phys Lett 75, 29122914.CrossRefGoogle Scholar
Cloetens, P., Mache, R., Schlenker, M. & Lerbs-Mache, S. (2006). Quantitative phase tomography of Arabidopsis seeds reveals intercellular void network. Proc Natl Acad Sci USA 103, 1462614630.Google Scholar
Dettmann, M.E., Clifford, H.T. & Peters, M. (2009). Lovellea wintonensis gen. et sp. nov.—Early Cretaceous (late Albian), anatomically preserved, angiospermous flowers and fruits from the Winton Formation, western Queensland, Australia. Cretac Res 30, 339355.CrossRefGoogle Scholar
DeVore, M.L., Kenrick, P., Pigg, K.B. & Ketcham, R.A. (2006). Utility of high resolution X-ray computed tomography (HRXCT) for palaeobotanical studies: An example using London clay fruits and seeds. Am J Bot 93, 18481851.Google Scholar
Dhondt, S., Vanhaeren, H., Van Loo, D., Cnuddle, V. & Inzé, D. (2010). Plant structure visualization by high-resolution X-ray computed tomography. Trends in Plant Sci 15, 419422.Google Scholar
Ducreux, J.L. (1982). Recherche des concentrations métallifères en domaine paralique et limnique. Le cas des formations du Crétacé supérieur gardois, du Paléogène de Manosque (Alpes-de-Haute-Provence) et de Saint-Martin-de-Palins (Puy-de-Dômes). PhD Thesis, Université Claude Bernard Lyon 1, France (unpublished). Google Scholar
Ducreux, J.L. & Gaillard, M.G. (1986). Le Cénomanien moyen à lignite de Saint-Laurent-de-Carnols (Gard). Données palynologiques et sédimentologiques. Implications paléoécologiques. Géol Fr 2, 189196.Google Scholar
Endress, P.K. & Friis, E.M. (1991). Archamamelis, hamamelidalean flowers from the upper Cretaceous of Sweden. Plant Syst Evol 175, 101114.Google Scholar
Feist, M., Liu, J. & Tafforeau, P. (2005). New insights into Paleozoic charophyte morphology and phylogeny. Am J Bot 92, 11521160.Google Scholar
Friis, E.M., Crane, P.R. & Pedersen, K.R. (2011). The Early Flowers and Angiosperm Evolution. Cambridge, UK: Cambridge University Press.Google Scholar
Friis, E.M., Crane, P.R., Pedersen, K.R., Bengtson, S., Donoghue, P.C.J., Grimm, G.W. & Stampanoni, M. (2007). Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature 450, 549552.Google Scholar
Friis, E.M. & Pedersen, K.R. (2011). Canrightia resinifera gen. et sp. nov., a new extinct angiosperm with Retimonocolpites-type pollen from the Early Cretaceous of Portugal: Missing link in the eumagnoliid tree? Grana 50, 329.CrossRefGoogle Scholar
Friis, E.M., Pedersen, K.R. & Crane, P.R. (2010). Cretaceous diversification of angiosperms in the western part of the Iberian Peninsula. Rev Palaeobot Palynol 162, 341361.Google Scholar
Friis, E.M., Pedersen, K.R. & Endress, P.K. (2013). Floral structure of extant Quintinia (Paracryphiales, campanulids) compared with the Late Cretaceous Silvianthemum and Bertilanthus . Int J Pl Sci 174, 647664.Google Scholar
Friis, E.M., Pedersen, K.R., Von Balthazar, M., Grimm, G.W. & Crane, P.R. (2009). Monetianthus mirus gen. et sp. nov., a nymphaealean flower from the Early Cretaceous of Portugal. Int J Pl Sci 17, 10861101.Google Scholar
Gamisch, A., Staedler, Y.M., Schönenberger, J., Fischer, G.A. & Comes, H.P. (2013). Histological and micro-CT evidence of stigmatic Rostellum receptivity promoting auto-pollination in the Madagascan orchid Bulbophyllum bicoloratum . PLoS One 8, e72688. Google Scholar
Heřmanová, Z., Kvaček, J. & Friis, E.M. (2011). Budvaricarpus serialis Knobloch & Mai, an unusual new member of the Normapolles complex from the Late Cretaceous of the Czech Republic. Int J Pl Sci 172, 285293.Google Scholar
Hernández-Castillo, G.R. & Cevallos-Ferriz, S.R.S. (1999). Reproductive and vegetative organs with affinities to Haloragaceae from the Upper Cretaceous Huepac Chert Locality of Sonora, Mexico. Am J Bot 86, 17171734.Google Scholar
Hughes, N.F. (1994). The Enigma of Angiosperm Origins. Cambridge: Cambridge University Press.Google Scholar
Kovacik, L., Plitzko, J.M., Grote, M. & Reichelt, R. (2009). Electron tomography of structures in the wall of hazel pollen grains. J Struct Biol 166, 263271.Google Scholar
Kradaglić, D. & Wilson, T. (2007). Image formation in structured illumination wide-field fluorescence microscopy. Micron 39, 808818.Google Scholar
Labiche, J.-C., Mathon, O., Pascarelli, S., Newton, M.A., Fere, G.G., Curfs, C., Vaughan, G., Homs, A. & Carreiras, D.F. (2007). The fast readout low noise camera as a versatile X-ray detector for time resolved dispersive extended X-ray absorption fine structure and diffraction studies of dynamic problems in materials science, chemistry, and catalysis. Rev Sci Instrum 78, 091301. Google Scholar
Lak, M., Néraudeau, D., Nel, A., Cloetens, P., Perrichot, V. & Tafforeau, P. (2008). Phase contrast X-ray synchrotron imaging: Opening access to fossil inclusions in opaque amber. Microsc Microanal 14, 251259.Google Scholar
Langer, M., Pacureanu, A., Suhonen, H., Grimal, Q., Cloetens, P. & Peyrin, F. (2012). X-ray phase nanotomography resolves the 3D human bone ultrastructure. PLoS One 7, e35691. Google Scholar
Little, S.A., Stockey, R.A. & Penner, B. (2009). Anatomy and development of fruits of Lauraceae from the Middle Eocene Princeton Chert. Am J Bot 96, 637651.Google Scholar
Maslova, N.P. & Tekleva, M.V. (2012). Infructescences of Friisicarpus sarbaensis sp. nov. (Platanaceae) from the Cenomanian-Turonian of Western Kazakhstan. Paleontol J 46, 433443.Google Scholar
Maslova, N.P., Tekleva, M.V. & Remizowa, M.V. (2012). Krassilovianthus gen. nov., a new staminate inflorescence with similarities to Platanaceae and Hamamelidaceae from the Cenomanian–Turonian of western Kazakhstan. Rev Palaeobot Palynol 180, 114.Google Scholar
Maslova, N.P., Tekleva, M.V., Sokolova, A.B., Broushkin, A.B. & Gordenko, N.V. (2011). Platanoid infructescences of Friisicarpus kubaensis sp. nov., and leaves of Ettingshausenia kubaensis sp. nov., from the Albian-Cenomanian of Chulym-Yenisei depression, Russia. The Palaeobotanist 60, 209236.Google Scholar
Matzke-Karasz, R., Smith, R.J., Symonova, R., Miller, C.G. & Tafforeau, P. (2009). Sexual intercourse involving giant sperm in Cretaceous ostracode. Science 324, 1535. Google Scholar
Mendes, M.M., Pais, J., Pedersen, K.R. & Friis, E.M. (2010). Erdtmanitheca portucalensis, a new pollen organ from the Early Cretaceous (Aptian–Albian) of Portugal with Eucommiidites-type pollen. Grana 49, 2636.Google Scholar
Michelet, C. & Moretto, P. (1999). STIM tomography at the cell level. Nucl Instr Meth Phys Res 158, 361367.Google Scholar
Mokso, R., Cloetens, P., Maire, E., Ludwig, W. & Buffière, J.-Y. (2007). Nanoscale zoom tomography with hard X rays using Kirkpatrick-Baez optics. Appl Phys Lett 90, 144104. CrossRefGoogle Scholar
Paganin, D., Mayo, S.C., Gureyev, T.E., Miller, P.R. & Wilkins, S.W. (2002). Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J Microsc 206, 3340.Google Scholar
Parron, C. (1975). Contribution à l'étude des paléoaltérations des grès du Crétacé supérieur du Gard. Conséquences stratigraphiques et paléogéographiques. PhD Thesis, Université de Marseille, France. Google Scholar
Perrichot, V., Marion, L., Néraudeau, D., Vullo, R. & Tafforeau, P. (2008). The early evolution of feathers: Fossil evidence from Cretaceous amber of France. P Roy Soc Lond B Bio 275, 11971202.Google Scholar
Peyrot, D., Barrón, E., Comas-Rengifo, M.J., Thouand, E. & Tafforeau, P. (2007). A confocal laser scanning and conventional wide field light microscopy study of Classopolis from the Toarcian-Aalenian of the Fuentelsaz section (Spain). Grana 46, 217226.Google Scholar
Pradel, A., Langer, M., Maisey, J., Geffard-Kuriyama, D., Cloetens, P., Janvier, P. & Tafforeau, P. (2009). Skull and brain of a 300 million-year-old chimaeroid fish revealed by synchrotron holotomography. P Natl Acad Sci 106, 52245228.Google Scholar
Punt, W., Hoen, P.P., Blackmore, S., Nilsson, S. & Le Thomas, A. (2007). Glossary of pollen and spore terminology. Rev Palaeobot Palynol 143, 181.Google Scholar
Renneberger, O., Schultz, E. & Burkhardt, H. (2002). Automated pollen recognition using 3D volume images from fluorescence microscopy. Aerobiologia 18, 107115.Google Scholar
Sanchez, S., Ahlberg, P.E., Trinajstic, K., Mirone, A. & Tafforeau, P. (2012). Three dimensional synchrotron virtual paleohistology: A new insight into the world of fossil bone microstructures. Microsc Microanal 18, 10951105.Google Scholar
Schönenberger, J. (2005). Rise from the ashes—The reconstruction of charcoal fossil flowers. Trends Plant Sci 10, 436443.Google Scholar
Schönenberger, J. & Friis, E.M. (2001). Fossil flowers of Ericalean affinity from the Late Cretaceous of southern Sweden. Am J Bot 88, 467480.Google Scholar
Schönenberger, J., Friis, E.M., Matthews, M.L. & Endress, P.K. (2001). Cunoniaceae in the Cretaceous of Europe: Evidence from fossil flowers. Ann Bot 88, 423437.Google Scholar
Schönenberger, J., Von Balthazar, M., Takahashi, M., Xia, X., Crane, P.R. & Herendeen, P.S. (2012). Glandulocalyx upatoiensis, a fossil flower of Ericales (Actinidiaceae/Clethraceae) from the Late Cretaceous (Santonian) of Georgia, USA. Ann Bot 109, 921936.Google Scholar
Scott, A.C., Galtier, J., Gostling, N.J., Smith, S.Y., Collinson, M.E., Stampanoni, M., Marone, F., Donoghue, P.C.J. & Bengton, S. (2009). Scanning electron microscopy and synchrotron radiation X-ray tomographic microscopy of 330 million year old charcoalified seed fern fertile organs. Microsc Microanal 15, 166173.Google Scholar
Smith, S.Y., Collinson, M.E., Rudall, P.J., Simpson, D.A., Marone, F. & Stampanoni, M. (2009). Virtual taphonomy using synchrotron tomographic microscopy reveals cryptic features and internal structure of modern and fossil plants. P Natl Acad Sci 106, 1201312018.Google Scholar
Smith, S.Y. & Stockey, R. (2007). Establishing a fossil record for the perianthless Piperales: Saururus tuckerae sp. nov. (Saururaceae) from the Middle Eocene Princeton Chert. Am J Bot 94, 16421657.Google Scholar
Smith, T.M. & Tafforeau, P. (2008). New visions of dental tissue research: Tooth development, chemistry, and structure. Evol Anthropol 17, 213226.CrossRefGoogle Scholar
Smith, T.M., Tafforeau, P., Reid, D.J., Pouech, J., Lazzari, V., Zermeno, J.P., Guatelli-Steinberg, D., Olejniczak, A.J., Hoffman, A., Radovcic, J., Makaremi, M., Tousaint, M., Stringer, C. & Hublin, J.-J. (2010). Dental evidence for ontogenetic differences between modern humans and Neanderthals. P Natl Acad Sci 107, 2092320928.Google Scholar
Sornay, J. (1950). Etude stratigraphique sur le Crétacé supérieur de la vallée du Rhône entre Valence et Avignon et des régions voisines. Trav Lab Géol Fac Sci Grenoble 27, 35270.Google Scholar
Staedler, Y.M., Masson, D. & Schönenberger, J. (2013). Plant tissues in 3D via X-ray tomography: Simple contrasting methods allow high resolution imaging. PLoS One 8, e75295. CrossRefGoogle ScholarPubMed
Stuppy, W.H., Maisano, J.A., Colbert, M.W., Rudall, P.J. & Rowe, T.B. (2003). Three-dimensional analysis of plant structure using high-resolution X-ray computed tomography. Trends Plant Sci 8, 26.Google Scholar
Tafforeau, P., Boistel, R., Boller, E., Bravin, A., Brunet, M., Chaimanee, Y., Cloetens, P., Feist, M., Hoszowska, J., Jaeger, J.-J., Kay, R.F., Lazzari, V., Marivaux, L., Neil, A., Nemoz, C., Thibault, X., Vignaud, P. & Zabler, S. (2006). Applications of X-ray synchrotron microtomography for nondestructive 3D studies of paleontological specimens. Appl Phys A-Mater 83, 195202.Google Scholar
Tafforeau, P. & Smith, T.M. (2008). Nondestructive imaging of hominoid dental microstructure using phase contrast X-ray synchrotron microtomography. J Hum Evol 54, 272278.Google Scholar
Tekleva, M.V. & Denk, T. (2012). Sporoderm ultrastructure of Platanus quedlinburgensis Pacltová emend. Tschan, Denk et von Balthazar from the Late Cretaceous of Germany. Acta Palaeobotanica 52, 177191.Google Scholar
Von Balthazar, M., Pedersen, K.R., Crane, P.R., Stampanoni, M. & Friis, E.M. (2007). Potomacanthus lobatus gen. et sp. nov, a new flower of probable Lauraceae from the Early Cretaceous (early to middle Albian) of Eastern North America. Am J Bot 94, 20412053.Google Scholar
Wang, X. (2008). Mesofossils with platanaceous affinity from the Dakota Formation (Cretaceous) in Kansas, USA. Palaeoworld 17, 246255.Google Scholar
Zhang, Y.-Y. (1999). The evolutionary succession of Cretaceous angiosperm pollen in China. Acta Palaeontologica Sinica 38, 435453 (in Chinese with English abstract).Google Scholar
Zhou, Z.K., Crepet, W.L. & Nixon, K.C. (2001). The earliest fossil evidence of the Hamamelidaceae: Late Cretaceous (Turonian) inflorescences and fruits of Altingioideae. Am J Bot 88, 753766.Google Scholar