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Taphonomic Constraints on Preservation of Cuticles In Taphonomic constraints on preservation of cuticles in . compression fossils: fungi induced ultrastructural changes in cuticular membranes UshaBajpai Bajpai Usha 1997. Taphonomic conslraints on preservation of cuticles in compression fossils: fungi induced ultrastructural changes in cuticular membranes. Palaeobolanisl 46 (3): 31-34. A comparative investigation has been made of the ultrastructure of the cuticular membrane recovered from healthy and fungal-infected leaves of Tbinnfeldia indica Feistmantel, a fossil taxon to understand lhe nature of changes brought about in the cuticular membrane by the fungi. In general, the structural configuration of both the cuticular membranes is similar. In the infected leaf, precursors of cutin acc.;::ions are irregularly present at the sub-cuticular surface. These accrelions are interpreted as possible results of breakdown of the cutin due to the secretion of an enzyme by the fungi infecting the leaf. It thus seems that the fungi, besides edaphic factors, do playa role in the break-down of the cutin and thus constrain the preservation of the cuticular membranes. Key-words - Cuticular membrane, Ultrastructure, Taphonomy, Tbinnfeldia. Usha Bajpai, Birbal Sahni Inslilule ofPalaeobolany, 53 Universiry Road, GPO Box 106, Lucknow 226001, India. ~ ~ ~ ~ ~ ~ ]i"yLu"ii~ ctt mwur it J'HiIFC::<6hl : f$lR"il<il it lJU ;:....h1D.. Utilzj"'P]"If'iJ&~ ~ "3itIT ~ ~ ~ ~ ~ ~ ~ ~ 'h1~~4'02:(1 ~ ~ It WU qir cf; fc;rQ: {0.q,(8s3fT 1llfcli ~Cflfcn ~ ~ ~ ~ ~~ ~ ~I ~: ~ <fit m it <fit Q{j{i(Cl11 cnT :g(11Iiii'fi fcf;<rr 'l'f<IT m ~ ~ ~ ~ ~I ~ ~ ~ ~ ~ ~"3"lf~ It {iN1IWfi m 'l'f<IT fcfi l:filt It $ CfiB qyR ~ ~ ~ ~ ~I ~ ~~: ~ ~ ~ ~ 1R it m- l:filt qir CfiB qyR WU cf; CfiRUT $ cf;~~itOfit~1 ~~milcrr~fcfi$cf;~lt, ~mcf;~, ~<fit~~~alR~ ~~~mm%itl THE remarkable resistance of cutin, the major expressed the opinion that cutan is not necessarily component of the plant cuticles, to most inorganic present in the cuticle of all the species, and this may and organic chemicals under normal conditions has be a reason for potential bias in the preservation of enabled the plant cuticles to persist through the the cuticular membranes of leaf fossils. The plant aeons, right from Late Devonian (375 million years surface mostly carries a microflora which grows in approximately) to Recent. The stability of the 'cutin' the environment provided by the leaf surface, Le., is due to the presence of 'cutan', a highly aliphatic 'phyllosphere' (Last, 1955). The phyllosphere is non-saponifiable biomacromolecule, that has a high colonised by bacteria and fungi which penetrate the fossilisation potential (Nip et at., 1986). However, plant tissue either through natural openings in the not all the fossil leaves have a cuticle preserved, and cuticle, Le., stomata, or through openings caused by in many a case the preservation of the cuticle is wounds. Many fungi penetrate directly through the highly unsatisfactory. Tegelaar et at. (991) have cuticle by release of enzyme cutinase which weak- 32 TI-IE PALAEOBOTANIST ens the thick cutin layer and helps the entry of the OBSERVATIONS hyphae. Though the process of fungal colonisation Transmission electron micrographs ofthe ultrathin of the leaf tissue is understood to some extent, yet sections of an uninfected leaf of Thtnnfeldta tndtca no study, more so onthe fossil leaves, has been made reveal that the leaf, atthe air-leaf interface, is covered to know if any changes are brought about in the with remnants of the epicuticular wax (PI. 1, fig. 6). ultrastructure of the cuticular membranes by the Beneath the epicuticular wax is the cuticular mem­ fungal infection. An attempt has been made here to brane proper which is amorphous in composition document differences in the ultrastructure ofhealthy and is structurally homogeneous (PI. 1, figs 6, 7). The andfungi-infected cuticular membranesof Thtnnfeldta thickness of the cuticular membrane is not uniform tndtca Feistmantel 1876. allover. This cuticle conformsto Type-6 ofHolloway's classification of the cuticle types in the leaves of MATERIAL AND MElHOD modern plants. The inner face of the cuticular membrane that is in contact with the epidermis The cuticular membranes were recovered by develops cuticular pegs or anticlinal flanges (PI. 1, acid-alkali processing of specimens of Thtnnfeldta figs 6, 7). These pegs/flanges are pointed at the tips tndtca Feistmantel, a presumed pteridospermous and have wide bases. The cuticular flanges are leaf collected from the Early Cretaceous Sivaganga located between the walls of adjacent epidermal Formation exposed in a water-well near Naicolam, cells (Cutter, 1978). Cuticular flanges have also been Tiruchirapalli District, Tamil Nadu (Maheshwari, reported in another fossil leaf, Ttcaa harrlstt from 1986). Epiphyllous microthyriaceous fungal re­ the Early Cretaceous of Argentina (Archangelsky, mains on these leaves have been earlier reported Taylor & Kurmann, 1986). Several ovoid gaps are and studied under the light microscope (Bajpai & seen in the matrix of the cuticular membrane which Maheshwari, 1988). Ultrastructure of the fungi­ are the result of not very higWy satisfactory impreg­ infected cuticular membrane has been studied by nation of the embedding medium. Maheshwari and Bajpai (996). Here we document the ultrastructure of the cuticular membranes recov­ The cuticular membrane of T. tndtca leaf that is ered from a healthy (Le., uninfected) leaf and infected with epiphyllous fungi is also covered by remnants of the epicuticular wax at the leaf-air compare it with that of the infected leaf to under­ interface (PI. 1, fig. 5). The matrix of the cuticular stand the taphonomic changes in the cuticular membrane is amorphous (PI. 1, figs 1, 2); at certain membrane. places electron dense spots are seen which in all For processing the cuticular membranes for probability are particles of the stain uranyl acetate ultrastructural studies, the method described in (PI. 1, fig. 4). The inner region of the cuticular Maheshwari and Bajpai (997) was followed in membrane appears to have been formed ofaggrega­ general. A variety of staining techniques was em­ tions ofirregu:ar bodies (PI. 1, fig. 3), which have the ployed to attain good contrast. A large number of same density as the other region (PI. 1, fig. 4). This sections of the cuticular membrane have been cut region is termed here as the 'disturbed zone'. These and were picked on uncoated Copper grids for irregular bodies were possibly formed by the break examination underthe Transmission Electron Micro­ down ofcutin at the sub-cuticular surface due to the scope. action of some enzyme (?cutinase) released by the PLATE 1 1-3. Thinnjeldia indica Feistmantel. micrographs of cross-section level, x 21000. of an infected cuticular membrane shOWing 'disturbed: sub- cuticular layer. I, x 4400; 2, x 7100; 3, x 7100. 5. Epicuticular wax on the infected cuticular membrane, x 21000. 4. A part of the same enlarged further to show the amorphous 6-7. Micrograph of the cuticular membrane of an uninfecled leaf matrix and aggregatiOns of irregular bodies at the sub-cuticular shOWing the amorphous matrix and cuticular pegs, x 8800. ~ ~ z 8 u ~ oz o :r: ~ I :( Q., co<- 34 THE PALAEOBOTANIST infecting fungi. Certain other structural deformities epiphyllous fungi and bacteria have been reported of the amorphous matrix are also seen in the on certain Permian and younger leaves. It has been disturbed zone as discussed by Maheshwari and found that such leaves invariably do not have a Bajpai (996). sufficiently well-preserved cuticle. In such cases the initial breakdown of the cuticle by cutinase is REMARKS probably followed by a bacterial arrack as has recently been observed in a Glossopteris leaf from a As a result of the available information on the grey shale associated with a Late Permian coal fine structure of uninfected and infected cuticular (Bajpai & Tewari, 1990). It would thus seem that membranes of Thtnnfeldta tndtca, it has been clas­ degradation of the cuticle in compression fossils is sified under the Holloway's Type-6. Both the induced by fungi , and in later stages is taken over cuticular membranes described here possess an by bacteria. amorphous homogeneousregion ofsignificant thick­ ness. The well-developed anticlinal flanges indicate a machinery to minimise water loss from the leaf ACKNOWLEDGEMENT surface, but whether this information supports the I thank Dr H.K. Maheshwari, Deputy Director, views that the climate of the region during the Early Birbal Sahni Institute of Palaeobotany for kindly Cretaceous was warm tropical is open to question. placing the compression material of Thtnnfeldta at From the palaeogeographical maps of that period it my disposal for study, and for initial review of the is evident that India lay in the sub-temperate zone, manuscript and constructive suggestions. south of the palaeoequator. REFERENCES Degradation of the epicuticular waxes may be Archangelsky S, Taylor TN & Kurmann MH 1986. Ultrastructural due to burial and diagenesis. The consistency in the studies of fossil plant cuticles: Ticoa harrisii from the early fine structure of both the normal and infected Cretaceous of Argentina. Bot.]. Linn. ·Soc. 92: 101-116. cuticular membranes demonstrates that diagenetic Bajpai U & Maheshwari HK 1988. Epiphyllous fungi from the Gondwana. In: Venkatachala BS & Maheshwari HK (Editors).­ factor did not disturb the structural identity but the Concepts, limits and extension of the Indian Gondwana. fungal infection did result in degradation of the Palaeobotanist 36: 21 0- 213. cuticular membrane on the inner surface. Fungi are Bajpai U & Tewari R 1990. Plant fossils from upper beds of Raniganj known to secrete cutin-hydrolysing enzymes, such Formation in Jharia Coalfield. Palaeobotanist 38: 43-48. Cuner EG 1982. Plant anatomy. Pan I. Cells and tissues. Edward as, cutinase (Kolarrukudy, 1980). Arnold, London, 1978. The most common plant fossils are compression Holloway PJ 1982. Structure and histochemistry of plant cuticular membranes: an overview. In: Cutler OF, Alvin KL & Price CE fossils of leaves that have lost their carbonified crust.
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