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Ultrastructure and Cytochemistry of Miocene Angiosperm Leaf Tissues (Angiosperm Paleobotany/Cytology/Electron Microscopy/Histochemistry/Evolution) KARL J

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Ultrastructure and Cytochemistry of Miocene Angiosperm Leaf Tissues (Angiosperm Paleobotany/Cytology/Electron Microscopy/Histochemistry/Evolution) KARL J Proc. Nati. Acad. Sci. USA Vol. 75, No. 7, pp. 13263-3267, July 1978 Botany Ultrastructure and cytochemistry of Miocene angiosperm leaf tissues (angiosperm paleobotany/cytology/electron microscopy/histochemistry/evolution) KARL J. NIKLAS*, R. MALCOLM BROWN, JR.t, RICHARD SANTOSt, AND BRIGITTE VIANt * The Harding Research Laboratory, New York Botanical Garden, Bronx, New York 10458; t Department of Botany, University of North Carolina, Chapel Hill, North Carolina 27514; and * Laboratoire de Biologie Vegetale, Cytologie Experimentale, University Paris VI, Paris, France Communicated by Elso S. Barghoorn, April 20,1978 ABSTRACT Angiosperm leaf fossils (16.7-25 X 106 years high level of phytochemical congruence between fossil taxa and by potassium/argon dating) referable to Zelkova were isolated their respective nearest living representative (20), while con- from pyroclastic deposits in the Succor Creek Formation, Ore- siderations of geochemical profiles indicate that relatively mild gon. These fossils reveal a three-dimensional structure in me- sophyll cell layers and vascular bundles, while transmission physiochemical factors attended post-depositional maturation electron microscopy of fixed tissues reveals well-preserved of associated sediments (21). chloroplasts with grana stacks and starch, as well as nuclei with condensed chromatin. Transmission electron microscopy in- MATERIALS AND METHODS dicates that cell walls retain a cellulosic microfibrillar archi- tecture, while ultrastructural and cytochemical confirmation The fossil material investigated in this and previous reports was is presented for chloroplast starch and the presence of native collected from the Succor Creek Formation, late Heming- cellulose. The preservation of cell walls and cytologic structures fordian or early Barstovian stage, of the Middle Miocene, Or- in fossil materials of this age indicates an unusually mild egon. Potassium/argon (K/A) dating of the Succor Creek flora fossilization process attending the post-depositional maturation and fauna by Evernden and James (22) gave an age of 16.7 X of associated sediments. The preservation observed appears to more recent on our material be associated with rapid physical dehydration coupled with 106 K/A years, while K/A datings endogenous fixation by organic acids (possibly tannins and/or give a range of ages (36-25 X 106 K/A years). Rubidium/ chlorophyll derivatives). strontium dates for the same locality average 22 X 106 R/S years. The incorporation of foreign materials into welded tufts Certain physiochemical conditions may permit the preservation is a major factor in the discrepancies observed in radiogenic of cytoplasmic remnants in fossil materials of extreme age if datings. On the basis of isotopic and stratigraphic data, the autolytic or necrotic processes can be sufficiently reduced or Succor Creek materials used in this study are considered Mio- temporarily stopped. In at least a few well-documented cases, cene in age and are at the minimum between 25 and 16.7 mil- the preservation of very delicate cytologic structures has been lion years old. The specimens used in this report were collected demonstrated in very ancient plant fossils (1-9). Physical factors approximately 13.2 miles from Jordan Valley along Interstate attending fossilization may also be sufficiently mild to permit 95, and some 3.7 mile from Interstate 95 towards Davisville the preservation of biochemical markers that have heretofore (reference map: Rockville, Oregon-Idaho N4315-W 11700). been thought too labile so as to preclude their presence in fossil Leaf tissues appearing a vivid green in color were excavated sediments (10-15). While biochemical fidelity in fossils has from lenticular tufts and tuffaceous siltstone and are thought prompted immunological investigations of problematic fossil to have been buried as a result of rapidly falling, relatively cool taxa,§ there are no reliable reports of biochemically intact volcanic ash. membranes preserved in situ. Speculation as to the nature of A leaf was carefully removed from the ash sediment and geochemical factors favoring the preservation of living plant placed under nitrogen. The upper portion was maintained for structures indicates that the gradual infiltration of mineral- scanning electron microscope analysis: the specimen was glued charged fluids over relatively short time spans may permit the to a stub and then carbon,gold-palladium coated. The lower fixation of intracellular structures (16). Few histologic exami- part of the leaf was fixed and embedded for transmission nations of fossil animal tissues have been attempted (17) other electron microscopy as follows: The light-brown leaf was placed than in cases of cryologic permeation, as in frozen Pleistocene into a fixative containing 2% (vol/vot) glutaraldehyde, 1% deposits (18, 19). Rehydration of frozen tissue samples taken (wt/vol) tannic acid, and 50 mM cacodylate buffer at pH 7.2. from the "mummified" remains of mammals dated at from At first the leaf floated, so it was swirled gently and intermit- 15,000 to 25,000 years old reveals that muscle and liver tissues tently for the first 15 min. At the end of this period, sufficient may retain some ultrastructural fidelity; however, most tissues fixative had penetrated the tissue so that the leaf settled to the are completely or partly replaced by bacterial masses. bottom of the fixation vial. The leaf was in the fixative for 45 The present study attempts to document the preservation of min at 250, then transferred to 40 for 20 hr. After washes in cell ultrastructure in angiosperm leaf tissues. Correlated light buffer, the sample was postfixed in 2% OS04 in 50 mM caco- and scanning and transmission electron microscopy of in situ dylate buffer, pH 7.2, for 3 hr at 4°. Then the sample was rinsed leaf fossils indicate that some regions of leaf tissues are virtually once in buffer as described above, then once in deionized water. unaltered and show little or no three-dimensional distortion due The sample was dehydrated with ethanol and infiltrated with to compression. Previous analyses of these specimens reveal a Abbreviations: K/A years, years by potassium/argon dating; PATAG, The costs of publication of this article were defrayed in part by the periodic acid-thiocarbohydrazide silver-staining method (23). payment of page charges. This article must therefore be hereby marked § Schmid, R. S., Wolniak, M. & Vreeland, V. J. (1976) Electron Mi- "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate croscopy and Immunochemistry of Prototaxites (Botanical Society this fact. of America, Lawrence, KA), p. 31 (abstr.). 3263 Downloaded by guest on October 2, 2021 32643NProc.Botany: Niklas et al. Nati. Acad. Sci. USA 75 (1978) ISoil" VIC A' L... A I L I - I >- s. A PA -S. .&- . FIG. 1. (Legend appears at bottom of the following page.) Downloaded by guest on October 2, 2021 Botany: Niklas et al. Proc. Nati. Acad. Sci. USA 75 (1978) 3265 Spurr's Epoxy resin. Sections were made: with a Reilf A cCasei *Y OM-U2 Ultramicrotome and transferred to copper grids for Solvent extractions, spectral characteristics, and cytochemistry conventional examination and to stainless steel grids for cyto- permit the identification and localization of various organic chemical tests. Material on the grids was post-stained with 2% constituents and confirm previously reported chemical profiles. aqueous uranyl acetate followed by Reynolds lead citrate. For X-ray diffractograms of pulverized and washed leaves show cytochemical analysis of carbohydrates the periodic acid- 20' Bragg peaks at 22, 17, and 15, and are identical to spectra thiocarbohydrazide silver-staining (PATAG) method was used of cellulose standards. Similarly, Raman spectra of fossil ma- (see ref. 23). Vouchers of in situ fossils and scanning and terial, as well as fresh leaf preparations, show AV(cm'1) shifts transmission electron microscopy specimens are stored at The at 1100 and between 500 and 300. Leaf tissues placed in New York Botanical Garden and the Department of Botany, cuprammonium solutions break apart; however, the quantity University of North Carolina, Chapel Hill, NC. of fossil material available for study precluded a viscometric determination. Optical birefringence, spectral characteristics, RESULTS and chemical properties of fossil leaves confirm the presence Morphology and ultrastructure of a cellulose or cellulose-like component in cell walls, and are In situ fossil leaves were mechanically removed from associated consistent with ultrastructural observations. PATAG staining rock matrices (Fig. 1 A-C) and prepared for scanning electron and 12KI reactions of the fossil material also indicate the pres- microscopy (Fig. I D-F) and transmission electron microscopy ence of true starch localized in cytoplasmic residues. (Figs. 1 H-K and 2). A typical angiosperm leaf anatomy is Thin-layer chromatography on silica gel (40:10:1, vol/vol, discernable at both the light and electron microscopy levels with hexane/ether/methanol) of the ether-soluble acids released by a cuticle external to the epidermis (Figs. 1 D-G and 2 C and methanolic KOH hydrolysis indicates the presence of mono-, D). Fractured leaves show tracheids and pallisade/spongy di-, and trihydroxy acids (20). Two series of monohydroxy acids mesophyll (Fig. 1 E and F), while correlated light and trans- were detected; the high molecular weight hydroxy acids, mission electron microscopy reveals exceptionally well-pre- 10,16-dihydroxyhexadecanoic acid and 9,10,18-trihydroxy-
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