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The Evolutionary Origin of the Integument in Seed Plants

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The Evolutionary Origin of the Integument in Seed Plants The evolutionary origin of the integument in seed plants Anatomical and functional constraints as stepping stones towards a new understanding DISSERTATION to obtain the degree Doctor Philosophiae (Doctor of Philosophy, PhD) at the Faculty of Biology and Biotechnology RUHR-UNIVERSITÄT BOCHUM International Graduate School of Biosciences Ruhr-Universität Bochum Evolution and Biodiversity of Plants submitted by Xin Zhang from Urad Qianqi (Inner Mongolia, China) Bochum October 2013 First supervisor: Prof. Dr. Thomas Stützel Second supervisor: Prof. Dr. Ralph Tollrian Der evolutionäre Ursprung des Integuments bei den Samenpflanzen Anatomische und funktionale Untersuchungen als Meilensteine für neue Erkenntnisse DISSERTATION zur Erlangung des Grades eines Doktors der Naturwissenschaften an der Fakultät für Biologie und Biotechnologie RUHR-UNIVERSITÄT BOCHUM Internationale Graduiertenschule Biowissenschaften Ruhr-Universität Bochum angefertigt am Lehrstuhl für Evolution und Biodiversität der Pflanzen vorgelegt von Xin Zhang aus Urad Qianqi (Innere Mongolei, China) Bochum Oktober 2013 Referent: Prof. Dr. Thomas Stützel Korreferent: Prof. Dr. Ralph Tollrian Contents I 1 Introduction 1 1.1 The ovule of gymnosperms and angiosperms 1 1.2 The theories about the origin of the integument in the nineteenth century 1 1.3 The theories about the origin of the integument in the twentieth century 1 1.4 The pollination drop 5 1.5 Ovule and pollination in Cycads 6 1.6 Ovule development in Magnolia stellata (Magnoliaceae) 6 1.7 Aril development in Celastraceae 7 1.8 Seed wing in Catha edulis (Vahl) Endl. (Celastraceae) 8 1.9 Ovule development in Homalanthus populifolius Graham (Euphorbiaceae) and differentiation of caruncula and aril 10 2 Material and methods 12 2.1 Material collection and preparation 12 2.2 Scanning Electron Microscopy (SEM) 12 2.3 Anatomical studies 13 3 Results 14 3.1 The morphology of Zamiaceae 14 3.2 Ovule development and seed anatomy in Zamia L. 16 3.3 Ovule morphology and anatomy in Cycas revolutaThunb. 22 3.4 Ovule development, seed morphology and anatomy in Magnolia stellate (Siebold & Zucc.) Maxim. 26 Contents II 3.5 Aril development in Celastraceae 32 3.5.1 Celastrus orbiculatus Thunb. 32 3.5.2 Euonymus europaeus L. 32 3.5.3 Euonymus planipes Koehne 33 3.6 Ontogeny of the ovule and seed wing in Catha edulis (Vahl) Endl. (Celastraceae) 41 3.7 Ovule development in Homalanthus populifolius Graham (Euphorbiaceae) and differentiation of caruncula and aril 45 3.7.1 Homalanthus populifolius Graham 45 3.7.2 Passiflora citrina J.M. MacDougal 46 4 Discussion 52 4.1 Integument and aril or aril-like structure in gymnosperms 52 4.2 Evolution of the (only) integument 53 4.3 The structure of the ovule within angiosperms 55 4.4 The envelope of the ovule within angiosperms 55 4.5 The function of the second envelope of seed plants 57 4.6 Origin of ovule and integument 59 4.7 Ovules in Lyginopteridatae 59 4.8 The pollination drop 60 4.9 Pollination in Cycads 61 4.10 Aril development in Celastraceae 62 Contents III 4.11 Seed wing development in Catha edulis (Vahl) Endl. 64 4.12 Caruncula and aril 67 4.13 Stomata on the outer integument 68 5 Summary 70 6 Zusammenfassung 72 7 Bibliography 74 8 Appendices Curriculum Vitae Published article 9 Acknowledgments List of figures IV Fig.1: Zamia amblyphyllidia D.W. Stev. in the Botanical Garden Bochum 14 Fig. 2: Male strobilus of Zamia amblyphyllidia D. W. Stev. 15 Fig. 3: Female strobilus of Zamia amblyphyllidia D. W. Stev. 15 Fig. 4: Microsporophyll of Zamia amblyphyllidia D. W. Stev. 16 Fig. 5: Ovule development of Zamia amblyphyllidia D. W. Stev. I 18 Fig. 6: Ovule development of Zamia amblyphyllidia D. W. Stev. II 19 Fig. 7: Ovule development of Zamia amblyphyllidia D. W. Stev. III 20 Fig. 8: Seed anatomy of Zamia amblyphyllidia D. W. Stev. 21 Fig. 9: Cycas revoluta Thunb., young leaves and female cone 22 Fig. 10: Megasporophyll and ovule of Cycas revoluta Thunb. 23 Fig. 11: Anatomy of the ovule of Cycas revoluta Thunb. 25 Fig. 12: Magnolia stellata (Siebold & Zucc.) Maxim. in the Botanical Garden Bochum 26 Fig. 13: Flower buds, flower, androecium, young fruit, mature fruit and seeds of Magnolia stellata (Siebold & Zucc.) Maxim. 27 Fig. 14: Ovule development in Magnolia stellata (Siebold & Zucc.) Maxim. 29 Fig. 15: Successive processes of the micropyle development of Magnolia stellata (Siebold & Zucc.) Maxim. 30 Fig. 16: Seed morphology and anatomy of Magnolia stellata (Siebold & Zucc.) Maxim. 31 Fig. 17: Celastrus orbiculatus Thunb.: Ovule, successive developmental stages 35 Fig. 18: Celastrus orbiculatus Thunb.: Caruncula, successive developmental stages 36 Fig. 19: Euonymus europaeus L.: Ovule, successive developmental stages 37 Fig. 20: Euonymus europaeus L.: Caruncula, successive developmental stages 38 Fig. 21: Euonymus planipes Koehne: Ovule, successive developmental stages 39 Fig. 22: Euonymus planipes Koehne: Caruncula, successive developmental stages 40 Fig. 23: Catha edulis (Vahl) Endl.: Flower and ovule, successive developmental stages 42 Fig. 24: Catha edulis (Vahl) Endl.: Caruncula, successive developmental stages 43 Fig. 25: Catha edulis (Vahl) Endl., younger and mature stage of the fruit 44 Fig. 26: Homalanthus populifolius Graham: Carpel, successive developmental stages 47 List of figures V Fig. 27: Homalanthus populifolius Graham: Ovule, successive developmental stages 48 Fig. 28: Homalanthus populifolius Graham: Caruncula, successive developmental stages 49 Fig. 29: Homalanthus populifolius Graham: Stomata on the outer integument and abaxial side of the leaf 50 Fig. 30: Passiflora citrina J. M. MacDougal: Aril, successive developmental stages 51 Fig. 31: Seed envelopes in gymnosperms. 52 Fig. 32: Ginkgo biloba L.: Ovule. 53 Fig. 33: Pinus parviflora Siebold & Zucc.: Ovule. 53 Fig. 34: Podocarpus macrophyllus (Thunb.) Sweet var. marcophyllus: Ovule. 53 Fig. 35: Structures of angiosperm ovules. 54 Fig. 36: Liriodendron chinense (Hemsl.) Sarg.: Two integuments. 55 Fig. 37: Actinidia arguta (Siebold & Zucc.) Planch. ex Miq.: Unitegmic ovule. 56 Fig. 38: Typical aril and caruncula in Celastraceae. 56 Fig. 39: The telome hypothesis after Andrews (1961). 59 Fig. 40: Structures of the ovules in Lyginopteridatae. 59 Fig. 41: Pollination drops of Zamia amblyphyllidia D.W. Stev. and Cupressus arizonica Greene var. glabra (Sudw.) Little 60 1 1 Introduction 1.1 The ovule of gymnosperms and angiosperms The ovule of gymnosperms and angiosperms is the female structure with at least one or two envelope structures covering the central part called nucellus or megasporangium. Within the nucellus, a megaspore develops into a haploid megagametophyte and produces the egg that is fertilized by the microgamete and forms an embryo. The envelope structure is called integument and surrounds and protects the nucellus. 1.2 The theories about the origin of the integument in the nineteenth century During the later part of the nineteenth century a number of conflicting theories based on anatomical, developmental and teratological evidence from extant plants were put forward but no definite conclusion was reached. Worsdell (1904) discussed the three principal theories for ovule origin advanced during the nineteenth century, namely the axial theory, the foliolar theory and the sui generis theory. The axial theory regards the nucellus as a shoot axis bearing foliar appendages fused to form the integument. This is supported by the morphology of gymnosperms, especially the strobilus structure of conifers. The foliolar theory held the ovule to be morphologically a phyllome; it relates the ovule to a three-lobe leaflet of the female sporophyll (or carpel in the angiosperms); the integument comes from the lateral ones; the nucellus is an emergence borne on the cup-shaped terminal lobe. The foliolar theory has various forms. It is supported by the angiosperm ovule particularly (Eames 1961). The sui generis theory is that the ovule is a new structure which is not homologous to either caulome or phyllome. These three theories generally lost influence. However, one can also find their shadow in some of the botanical text books today. 1.3 The theories about the origin of the integument in the twentieth century In the 20th century, the consideration of the ovule origin has focused largely on Pteridospermophyta, which are generally accepted to include the oldest seed plants. Benson (1904) noticed that the synangium of Telangium scottii Benson and the 2 ovule of Lagenostoma Williamson are very similar to each other. She hypothesized that the integument evolved from a sterile outer ring of sporangia in a radial synangium. This is the first theory of the pteridosperm ovule based on fossil evidence. According to her theory, the number of spores in the central sporangium was reduced to one which finally produced the female gametophyte. Oliver and Scott (1904) hypothesized the evolution of the integument from a cup-like indusium in their monograph on Lagenostoma lomaxii Williamson. With regard to the origin of the ovule they stated that “we have in Lagenostoma Williamson a megasporangium which has been enclosed by two successive, concentric, indusium- like structures of which the inner has become an integral part of a new organ, the seed; the outer is probably of later origin…" It is quite possible that the two enclosures have originated very similarly, i.e. as peltate, lobed structures, and that the present integument was once a comparatively unspecialized, cupule-like indusium”. In the monograph on Lagenostoma Williamson they state “a comparison of the seeds of Cycads with Lagenostoma Williamson is inevitable”. Stopes (1904, 1905) and Matte (1904) supported this idea with their work on the integument structure of the Cycads. They showed independently that the inner vascular system of the cycad ovule supplies the inner part of the integument but not the nucellus as previously thought, and that the integument itself has a double structure in respect to vascularization. Stopes considered that the integumentary vascular system of Lagenostoma is equivalent to the inner system of Cycads and that the cupular system is equivalent to the outer Cycads system.
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