Abstract
Morphologically similar damage to carpels of two Friisicarpus species (Platanaceae), F. kubaensis (Western Siberia, Albian–Cenomanian) and F. sarbaensis (Western Kazakhstan, Cenomanian–Turonian) induced by micromycetes, is described for the first time. Fruiting bodies of the micromycetes are developed within the tissues, forming tubercles on the carpel surfaces. The morphology of the fruiting bodies, their distribution on the substrate, as well as dropping out of the substrate after maturation, link them with some modern representatives of Pleosporales. A possible role of insects in the transfer of fungal spores, and participation of arthropods in the pollination of early Platanaceae, are discussed.
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REFERENCES
Crane, P.R., Friis, E.M., and Pedersen, K.R., Lower Cretaceous angiosperm flowers: fossil evidence on early radiation of dicotyledons, Science, New Ser., 1986, vol. 232 (4752), pp. 852–854.
Crane, P.R., Pedersen, K.R., Friis, E., and Drinnan, A.N., Early Cretaceous (Early to Middle Albian) platanoid inflorescences associated with Sapindopsis leaves from the Potomac Group of Eastern North America, Syst. Bot., 1993, vol. 18, pp. 328–344.
Crous, P.W., Lombard, L., Sandoval-Denis, M., et al., Fusarium: more than a node or a foot-shaped basal cell, Stud. Mycol., 2021, vol. 98, no. 1, pp. 1–184.
Crous, P.W., Wingfield, M.J., Burgess, T.I., et al., Fungal Planet Description Sheets: 469–557, Persoonia: Mol. Phylog. Evol. Fungi, 2016, vol. 37, pp. 218−403.
Deb, D., Khan, A., and Dey, N., Phoma diseases: Epidemiology and control, Plant Pathol. 2020, vol. 69, no. 7, pp. 1203–1217.
Fakir, G.A., Welty, R.E., and Cowling, E.B., Prevalence and pathogenicity of fungi associated with achenes of sycamore in the field and in storage, Phytopathology, 1971, vol. 61, pp. 660–668.
Friis, E.M., Crane, P.R., and Pedersen, K.R., Reproductive structures of Cretaceous Platanaceae, Det Kong. Danske Vidensk. Selskab Biol. Skrift, 1988, vol. 31, pp. 1–55.
Golovneva, L.B., Genus Ettingshausenia (Platanaceae) in the Cenomanian-Turonian floras of Eurasia, in Paleobotany, vol. 2, Golovneva, L.B., Ed., St. Petersburg: Marafon, 2011, pp. 127–163.
Dyakov, Yu.T., Fungi and plants, Priroda, 2003, no. 5, pp. 73–78.
Golovneva, L.B., The morphology, taxonomy, and occurrence of the genus Pseudoprotophyllum Hollick (Platanaceae) in Late Cretaceous floras of Northern Asia, Paleontol. J., 2009, vol. 43, no. 10, pp. 1230–1244.
Hitchcock, L.A. and Cole, A.L.J., Gnomonia platani, the ascogenous state of Gloeosporium platani, found in New Zealand, N. Z. J. Bot., 1978, vol. 16, no. 3, pp. 411–411.
Horst, R.K., Westcott’s Plant Disease Handbook, Dordrecht: Springer, 2013.
Hou, L.W., Groenewald, J.Z., Pfenning, L.H., et al., The Phoma-like dilemma, Stud. Mycol. 2020, vol. 96, pp. 309–396.
Hu, S.S., Dilcher, D.L., Jarzen, D.M., and Taylor, D.W., Early steps of angiosperm-pollinator coevolution, Proc. Nat. Acad. Sci. USA, 2008, vol. 105, no. 1, pp. 240–245.
Huegele, I.B. and Manchester, S.R., Newly recognized reproductive structures linked with Langeria from the Eocene of Washington, USA, and their affinities with Platanaceae, Int. J. Plant Sci., 2022, vol. 183, no. 5.
Huegele, I.B. and Wang, H., An unusual plane tree from the Early Cretaceous of Kansas, USA, Rev. Palaeobot. Palynol., 2023, vol. 309, no. 104815.
Huegele, I.B., Spielbauer, R.J., and Manchester, S.R., Morphology and systematic affinities of Platanus dissecta Lesquereux (Platanaceae) from the Miocene of western North America, Int. J. Plant Sci., 2019, vol. 181, no. 3, pp. 324–341.
Hughes, D.P., Wappler, T., and Labandeira, C.C., Ancient death-grip leaf scars reveal ant–fungal parasitism, Biol. Lett., 2011, no. 7, pp. 67–70.
Jamali, S. and Yalveh, S., The first report of Libertella platani on Platanus orientalis in Iran, Mycol. Iranica, 2017, vol. 4, no. 2, pp. 133–134.
Khorsandy, S., Nikbakht, A., Sabzalian, M.R., and Pessarakli, M, Effect of fungal endophytes on morphological characteristics, nutrients content and longevity of plane trees (Platanus orientalis L.), J. Plant Nutrit., 2016, vol. 39, no. 8, pp. 1156–1166.
Kodrul, T.M., Maslova, N.P., Tekleva, M.V., and Golovneva, L.B., Platanaceous reproductive structures and leaves from the Cretaceous locality Kundur, Amur region, Russia, Palaeobotanist, 2013, vol. 62, no. 1, pp. 123–148.
Krassilov, V.A. and Shilin, P.V., New platanoid staminate heads from the Mid–Cretaceous of Kazakhstan, Rev. Palaeobot. Palynol., 1995, vol. 85, pp. 207–211.
Labandeira, C.C., Wilf, P., Johnson, K.R., and Marsh, F., Guide to Insect (and Other) Damage Types on Compressed Plant Fossils. Version 3.0, Washington, D.C.: Smithson. Inst., 2007.
Li, Q., Su, T., Deng, W., et al., High frequency of arthropod herbivore damage in the Miocene Huaitoutala flora, Qaidam Basin, northern Tibetan Plateau, Rev., Palaeobot. Palynol., 2022, vol. 298, no. 104569.
Mamikonyan, T.O. and Manasyan, G.G., Fungal diseases of Platanus L. species in the conditions of Armenia, in Aktual’nyye problemy botaniki v Armenii (Actual Problems of Botany in Armenia), Yerevan: UGU, 2008, pp. 226–228.
Maslova, N.P., Extinct and extant Platanaceae and Hamamelidaceae: morphology, systematics, and phylogeny, Paleontol. J., 2003, vol. 37, Suppl. 5, pp. 467–589.
Maslova, N.P., New genus Sarbaicarpa gen. nov. (Hamamelidales) from the Cenomanian–Turonian of Western Kazakhstan, Paleontol. J., 2009, vol. 43, no. 10, pp. 1281–1297.
Maslova, N.P., Systematics of fossil platanoids and hamamelids, Paleontol. J., 2010, vol. 44, no. 11, pp. 1379–1466.
Maslova, N.P. and Herman, A.B., Infructescences of Friisicarpus nom. nov. (Platanaceae) and associated foliage of the platanoid type from the Cenomanian of Western Siberia, Paleontol. J., 2006, vol. 40, no. 1, pp. 109–113.
Maslova, N.P. and Tekleva, M.V., Infructescences of Friisicarpus sarbaensis sp. nov. (Platanaceae) from the Cenomanian–Turonian of Western Kazakhstan, Paleontol. J., 2012, vol. 46, no. 4, pp. 433–443.
Maslova, N.P., Tekleva M.V., Sokolova, A.B. et al., Infructescences of Friisicarpus kubaensis sp. nov. and leaves of Ettingshausenia kubaensis sp. nov. from the Albian–Cenomanian of Chulym–Yenisei depression, Russia, Palaeobotanist, 2011, vol. 60, no. 2, pp. 209–236.
Maslova, N.P., Tekleva, M.V., and Remizowa, M.V., Krassilovianthus gen. nov., a new staminate inflorescence with similarities to Platanaceae and Hamamelidaceae from the Cenomanian–Turonian of western Kazakhstan, Rev. Palaeobot. Palynol., 2012, vol. 180, pp. 1–14.
Maslova, N.P., Kodrul, T.M., and Vasilenko, D.V., First record of bacteriomorphic organisms in platanoid infructescences from the Campanian Kundur locality, Amur Region, Paleontol. J., 2014, vol. 48, no. 5, pp. 563–570.
Maslova, N.P., Sokolova, A.B., Kodrul, T.M., and Tobias, A.V., Consortia of conifers and fungi in the Paleocene of the Amur Region, Russia, Paleontol. J., 2021, vol. 55, no. 12, pp. 1525–1553.
Maslova, N.P., Tobias, A.V., and Kodrul, T.M., Recent Studies of co-evolutionary relationships of fossil plants and fungi: success, problems, prospects, Paleontol. J., 2021, vol. 55, no. 1, pp. 1–17.
Maslova, N.P, Sokolova, A.B., Vasilenko, D.V., et al., Endophytic micromycetes on the leaves of the genus Taxodium Richard (Cupressaceae) from the Lower Paleocene of the Amur Region, Paleontol. J., 2018, vol. 52, no. 12, pp. 1473–1479.
Pastirčáková, K. and Pastirčák, M., The anamorph of Erysiphe platani on Platanus hispanica in Slovakia, Mycotaxon, 2006, vol. 97, pp. 189–194.
Pelleteret, P., Crovadore, J., Cochard, B., et al., Urban London plane tree dieback linked to fungi in the Botryosphaeriaceae, Urban Forest. Urban Green., 2017, vol. 22, pp. 74–83.
Perera, R.H., Hyde, K.D., Maharachchikumbura, S.S.N., et al., Fungi on wild seeds and fruits, Mycosphere, 2020, vol. 11, no. 1, pp. 2108–2480.
Robles, C.A., Lopez, S.E., McCargo, P.D., and Carmarán, C.C., Relationships between fungal endophytes and wood-rot fungi in wood of Platanus acerifolia in urban environments, Canad. J. Forest Res., 2015, vol. 45, no. 7, pp. 929–936.
Saccardo, P.A., Sylloge Fungorum Omnium Hucusque Cognitorum. Vol. II. Pyrenomycologiae universae. Continuatio et finis. Berlin: Iterum Impressum apud R. Friedländer, 1883.
Saccardo, P.A., Sylloge Fungorum Omnium Hucusque Cognitorum. Vol. XI. Supplementum universale. Pars III. Berlin: Iterum impressum apud R. Friedländer, 1895.
Saccardo, P.A., Saccardo, D., Traverso, J.B., Trotter, A., Sylloge Fungorum Omnium Hucusque Cognitorum. Vol. XXV. Supplementum Universale. Pars X. Berlin: Iterum Impressum apud R. Friedländer, 1931.
Scattolini, A., Coelho, A., Torrano, C., et al., Fungi associated to Platanus x acerifolia in Uruguay and failure indicators, Agrociencia, 2023, vol. 27, pp. 989.
Schmitt, U., Lüer, B., Dujesiefken, D., and Koch, G., The Massaria disease of plane trees: Its wood decay mechanism, IAWA J., 2014, vol. 35, no. 4, pp. 395–406.
Tekleva, M.V. and Maslova, N.P., A diverse pollen assemblage found on Friisicarpus infructescences (Platanaceae) from the Cenomanian-Turonian of Kazakhstan, Cret. Res., 2016, vol. 57, pp. 131–141.
Tschan, G.F., Denk, T., and von Balthazar, M., Credneria and Platanus (Platanaceae) from the Late Cretaceous (Santonian) of Quedlinburg, Germany, Rev. Palaeobot. Palynol., 2008, vol. 152, no. 3-4, pp. 211–236.
Wainio, W.W. and Forbes, E.B., The chemical composition of forest fruits and nuts from Pennsylvania, J. Agric. Res., 1941, vol. 62, pp. 627–635.
Wang, H., Dilcher, D.L., Schwarzwalder, R.N., and Kvaček, J., Vegetative and reproductive morphology of an extinct Early Cretaceous member of Platanaceae from the Braun’s Ranch Locality, Kansas, U.S.A., Int. J. Plant Sci., 2011, vol. 172, no. 1, pp. 139–157.
Wang, X., Mesofossils with platanaceous affinity from the Dakota Formation (Cretaceous) in Kansas, USA, Palaeoworld, 2008, vol. 17, pp. 246–255.
Wijayawardene, N.N., Hyde, K.D., Bhat, D.J., et al., Additions to brown spored coelomycetous taxa in Massarinae, Pleosporales: introducing Phragmocamarosporium gen. nov. and Suttonomyces gen. nov., Cryptogam. Mycol., 2015, vol. 2, pp. 213–224.
ACKNOWLEDGMENTS
The authors are grateful to their colleagues from the Borissiak Paleontological Institute, Russian Academy of Sciences (PIN RAS) and the Institute of Biology and Soil Sciences, Far Eastern Branch Russian Academy of Sciences (now the Federal Scientific Center for Biodiversity of Terrestrial Biota of East Asia, FEB RAS—FSC FEB RAS) for collecting and providing the opportunity to study fossils, D.V. Vasilenko (PIN RAS) for constructive discussion of the research results, V.M. Ionov for help in producing the map showing the localities, the reviewers A.B. Herman and M.G. Moiseeva (Geological Institute, Russian Academy of Sciences, GIN RAS) for valuable advice and recommendations.
Funding
The work was carried out within the framework of the theme of the state assignment of Lomonosov Moscow State University no. 121032300081-7 (E.Yu.B.).
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Maslova, N.P., Tekleva, M.V. & Blagoveshchenskaya, E.Y. First Evidence of Micromycete Damage to Infructescences of the Cretaceous Genus Friisicarpus N. Maslova et Herman (Platanaceae). Paleontol. J. 57, 692–703 (2023). https://doi.org/10.1134/S0031030123060072
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DOI: https://doi.org/10.1134/S0031030123060072