The Pollen Tube Pathway in Tasmannia insipida (Winteraceae): Homology of the Male Gametophyte Conduction Tissue in Angiosperms

Abstract

The pathway of the pollen tube in Tasmannia insipida (Winteraceae), an archaic angiosperm, is described. Visual observations and measurements of percentage sugar content from stigmatic exudate and the calyptra droplet were made. The droplet that forms on the calyptra of unopened flowers was artificially pollinated, but no pollen tubes appeared to grow through it to the gynoecium of female flowers. Calyptra droplets occur on both female and male (having reduced female structures) flowers of this dioecious plant. It is considered unlikely that a drop pollination mechanism, analogous to that found in some gymnosperms, is at work in T. insipida, and it is proposed that one possible droplet function is as a “reward” to potential pollinators in advance of flower opening. Pollen tubes were observed to grow almost exclusively along epidermal cells. Early thoughts on angiosperm transmission tissue are re-examined and built upon. It is proposed that the male gametophyte conduction tissue in angiosperms is homologous with epidermal tissue, and that pollen tube passage occurred originally solely along the surface of specialized epidermal cells, or possibly for short distances along unspecialized regions covered with exudate derived from these cells. Some earlier attempts to explain transmitting tissue homology and evolution are discussed.

Key words

Stigmatic exudate - transmitting tissue - morphology - pollination.

References

• 1 Anderson W. R.. Cryptic self-fertilization in the Malphigiaceae.  Science. (1980);  207 892-893
• 2 Arber A.. The interpretation of the flower: A study of some aspects of morphological interest.  Biological Reviews of the Cambridge Philosophical Society. (1937);  12 157-184
• 3 Bailey I. W., Swamy B. G. L.. The conduplicate carpel of dicotyledons and its initial trends of specialization.  American Journal of Botany. (1951);  38 373-379
• 4 Baker H. G., Baker I., Opler P. A.. Stigmatic exudates and pollination. Brantjes, N. B. M., ed. Pollination and Dispersal. Nijmegen; Department of Botany (1973): 47-60
• 5 Capus G.. Anatomie du tissu conducteur. Annales des Sciences Naturelles.  Botanique et Biologie Vegetale. (1878);  7 209-291
• 6 Doyle J. A., Hotton C. L., Ward J. V.. Early Cretaceous tetrads, zonasulcate pollen, and Winteraceae.  I. Taxonomy, morphology, and ultrastructure. American Journal of Botany. (1990);  77 1544-1557
• 7 Endress P. K.. Diversity and Evolutionary Biology of Tropical Flowers. Cambridge; Cambridge University Press (1994)
• 8 Endress P. K., Igersheim A.. Gynoecium structure and evolution in basal angiosperms.  International Journal of Plant Science. (2000);  161 (Suppl.6) S211-S223
• 9 Frame-Purguy D.. Carpel development in Tasmannia insipida (Winteraceae).  International Journal of Plant Science. (1996);  157 698-702
• 10 Franssen-Verheijen M. A. W., Willemse M. T. M.. Micropylar exudate in Gasteria (Aloaceae) and its possible function in pollen tube growth.  American Journal of Botany. (1993);  80 253-262
• 11 Gottsberger G., Silberbauer-Gottsberger I., Ehrendorfer F.. Reproductive biology in the primitive relic angiosperm Drimys brasiliensis (Winteraceae).  Plant Systematics and Evolution. (1980);  135 11-39
• 12 Hartl D.. Morphologische Studien am Pistell der Scrophulariaceen.  Österreichische Botanische Zeitung. (1956);  103 185-242
• 13 Higashiyama T.. The synergid cell: attractor and acceptor of the pollen tube for double fertilization.  Journal of Plant Research. (2002);  115 149-160
• 14 Igersheim A., Endress P. K.. Gynoecium diversity and systematics of the Magnoliales and winteroids.  Botanical Journal of the Linnean Society. (1997);  124 213-271
• 15 Kaplan D. R.. The science of plant morphology: definition, history, and role in modern biology.  American Journal of Botany. (2001);  88 1711-1741
• 16 Küchmeister H., Silberbauer-Gottsberger I., Gottsberger G.. Flowering, pollination, nectar standing crop, and nectaries of Euterpe precatoria (Arecaceae), an Amazonian rain forest palm.  Plant Systematics and Evolution. (1997);  206 71-97
• 17 Labandeira C. C.. The history of associations between plants and animals. Herrera, C. M. and Pellmyr, O., eds. Plant-Animal Interactions: An Evolutionary Approach. London; Blackwell Science (2002): 26-74
• 18 Lloyd D. G., Wells M. S.. Reproductive biology of a primitive angiosperm, Pseudowintera colorata (Winteraceae), and the evolution of pollination systems in the Anthophyta.  Plant Systematics and Evolution. (1992);  181 77-95
• 19 Martin F. W.. Staining and observing pollen tubes in the style by means of fluorescence.  Stain Technology. (1959);  34 125-128
• 20 Prakash N., Linn A. L., Sampson F. B.. Anther and ovule development in Tasmannia (Winteraceae).  Australian Journal of Botany. (1992);  40 877-885
• 21 Sage T. L., Sampson F. B., Bayliss P., Gordon M. G., Heij E. G.. Self-sterility in Winteraceae. Owens, S. J. and Rudall, P. J., eds. Reproductive Biology in Systematics, Conservation and Economic Botany. Kew; Royal Botanic Gardens (1998): 317-328
• 22 Sampson F. B., Tucker S. C.. Placentation in Exospermum stipitatum (Winteraceae).  Botanical Gazette. (1978);  139 215-222
• 23 Sampson F. B., Williams J. B., Woodland P. S.. The morphology and taxonomic position of Tasmannia glaucifolia (Winteraceae), a new Australian species.  Australian Journal of Botany. (1988);  36 395-413
• 24 Satina S.. Periclinal chimeras in Datura in relation to development and structure (A) of the style and stigma (B) of calyx and corolla.  American Journal of Botany. (1944);  31 493-502
• 25 Scott A. C., Stephenson J., Chaloner W. G.. Interaction and coevolution of plants and arthropods during the Palaeozoic and Mesozoic.  Philosophical Transactions of the Royal Society of London B. (1992);  335 129-165
• 26 Takaso T.. “Pollination drop” time at the Arnold Arboretum.  Arnoldia. (1990);  50 2-7
• 27 Thomas H. H.. The nature and origin of the stigma: a contribution towards a new morphological interpretation of the angiosperm flower.  New Phytologist. (1934);  33 12-198
• 28 Tomlinson P. B., Braggins J. E., Rattenbury J. A.. Pollination drop in relation to cone morphology in Podocarpaceae: a novel reproductive mechanism.  American Journal of Botany. (1991);  78 1289-1303
• 29 Vink W.. Winteraceae of the Old World. I. Pseudowintera and Drimys - morphology and taxonomy.  Blumea. (1970);  18 225-354
• 30 Webb M. C., Williams E. G.. The pollen tube pathway in the pistil of Lycopersicon peruvianum. .  Annals of Botany. (1988);  61 415-423
• 31 Weberling F.. Morphology of flowers and inflorescences. (translated by Pankhurst, R. J.) Cambridge; Cambridge University Press (1989)
• 32 Williams E. G., Sage T. L., Thien L. B.. Functional syncarpy by intercarpellary growth of pollen tubes in a primitive apocarpous angiosperm, Illicium floridanum (Illiciaceae).  American Journal of Botany. (1993);  80 137-142

Section Editor: G. Gottsberger