Summary
Anabaena azollae is associated with two types of multicellular epidermal trichomes inAzolla leaf cavities, the simple and branched hairs. The observation of transfer cell ultrastructure in some hair cells led to speculation that the cavity hairs might participate in metabolite exchange between the symbionts. The developmental ontogeny of cavity trichomes is described here, using transmission electron microscopy, with a goal of improving our understanding of possible functions of these structures in the symbiosis. The observations have established that all cells of simple and branched hairs develop the structural characteristics of transfer cells, but not simultaneously. Rather, there is an acropetal succession of transfer cell ultrastructure beginning in terminal cells, moving to body cells where present, and ending in stalk cells. The transfer cell stage is followed immediately by senescence in all hair cells. The timing of transfer cell differentiation, considered together with information from other studies, suggests that branched hairs may be involved in exchange of fixed nitrogen between the symbionts, while simple hairs may participate in exchange of fixed carbon fromAzolla toAnabaena.
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Barnabas, A. D., Butler, V., Steinke, T. D., 1977:Zostera capensis Setchell. I. Observations of the fine structure of the leaf epidermis. Z. Pflanzenphysiol.85, 417–427.
Briarty, L. G., 1978: The development of root nodule xylem transfer cells inTrifolium repens. J. exp. Bot.29, 735–747.
Calvert, H. E., Peters, G. A., 1981: TheAzolla-Anabaena azollae relationship. IX. Morphological analysis of leaf cavity hair populations. New Phytol.89, 327–335.
—,Perkins, S. K., Peters, G. A., 1983: Sporocarp structure in the heterosporous water fernAzolla mexicana Presl. Scanning Electron Microsc.III, 1499–1510.
Cronshaw, J., 1981: Phloem structure and function. Ann. Rev. Plant Physiol.32, 465–484.
Duckett, J. G., Toth, R., Soni, S. L., 1975: An ultrastructural study of theAzolla, Anabaena azollae relationship. New Phytol.75, 111–118.
Fahn, A., 1979: Secretory structures in plants. Academic Press: London.
—,Benouaiche, P., 1979: Ultrastructure development and secretion in the nectary of bananaMusa paradisiaca var.sapientum flowers. Ann. Bot. (Lond.)44, 85–94.
Fineran, B. A., 1980: Ontogeny of external glands in the bladderwortUtricularia monanthos. Protoplasma105, 9–25.
—,Lee, M. S, L., 1975: Organization of quadrified and bifid hairs in the trap ofUtricularia monanthos. Protoplasma84, 43–70.
Gunning, B. E. S., Pate, J. S., 1969: “Transfer cells” plant cells with wall ingrowths, specialized in relation to short distance transport of solutes—their occurrence, structure, and development. Protoplasma68, 107–133.
Heslop-Harrison, Y., Knox, R. B., 1971: A cytochemical study of the leaf-gland enzymes of insectivorous plants of the genusPinguicula. Planta96, 183–211.
Hill, D. J., 1975: The pattern of development ofAnabaena in theAzolla-Anabaena symbiosis. Planta133, 237–242.
Jones, M. G. K., Northcote, D. H., 1972: Multinucleate transfer cells induced inColeus roots by the root-knot nematode,Meloidogyne arenaria. Protoplasma75, 381–395.
Kaplan, D., Peters, G. A., 1981: TheAzolla-Anabaena azollae relationship. X. 15 N2 fixation and transport in main stem axes. New Phytol.89, 337–346.
Morrison, I. N., O'Brien, T. P., Kuo, J., 1978: Initial cellularization of the aleurone cells in the ventral region of the developing wheat grain. Planta141, 19–30.
Pate, J. S., Gunning, B. E. S., 1972: Transfer cells. Ann. Rev. Plant Physiol.23, 173–196.
Peters, G. A., 1975: TheAzolla-Anabaena azollae relationship. III. Studies of metabolic capabilities and a further characterization of the symbiont. Arch. Microbiol.103, 113–122.
—,Calvert, H. E., 1983: TheAzolla-Anabaena azollae symbiosis. In: Algal symbiosis (Goff, L. J., ed.), pp. 109–145. New York: Cambridge University Press.
—,Mayne, B. C., 1974: TheAzolla, Anabaena azollae relationship. I. Initial characterization of the association. Plant Physiol.53, 813–819.
—,Toia, Jr., R. E., Raveed, D., Levine, N. J., 1978: TheAzolla-Anabaena azollae relationship. VI. Morphological aspects of the association. New Phytol.80, 583–593.
—,Ray, T. B., Mayne, B. C., Toia, Jr., R. E., 1980:Azolla-Anabaena association: morphological and physiological studies. In: Nitrogen fixation, Vol. 2 (Newton, W. E., Orme-Johnson, W. H., eds.), pp. 293–309. Baltimore: University Park Press.
—,Toia, Jr., R. E., Evans, W. R., Crist, D. K., Mayne, B. C., Poole, R. E., 1980: Characterization and comparisons of five N2-fixingAzolla-Anabaena associations. I. Optimization of growth conditions for biomass increase and N content in a controlled environment. Plant Cell Environ.3, 261–269.
—,Kaplan, D., Meeks, J. C., Buzby, K. M., Marsh, B. H., Corbin, J. L., 1985: Aspects of nitrogen and carbon interchange in theAzolla-Anabaena symbiosis. In: Nitrogen fixation and CO2 metabolism (Ludden, P. L., Burris, J. E., eds.), pp. 213–222. New York: Elsevier.
Ray, T. B., Peters, G. A., Toia, Jr., R. T., Mayne, B. C., 1978:Azolla-Anabaena relationship. VII. Distribution of ammonia-assimilating enzymes, protein, and chlorophyll between host and symbiont. Plant Physiol.62, 463–467.
—,Mayne, B. C., Toia, Jr., R. T., Peters, G. A., 1979:Azolla-Anabaena relationship. VIII. Photosynthetic characterization of the association and individual partners. Plant Physiol.64, 791–795.
Reynolds, E. S., 1963: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol.17, 208–213.
Schnepf, E., 1960: Zur Feinstructur der Drüsen vonDrosophyllum lusitanicum. Planta54, 641–675.
—, 1961: Licht- und elektronenmikroskopische Beobachtungen an Insektivorendrüsen über die Sekretion des Fangschleims. Flora151, 73–87.
—, 1974: Gland cells. In: Dynamic aspects of plant ultrastructure (Robards, A. W., ed.), pp. 331–357. Maidenhead, UK: McGraw-Hill.
—,Pross, E., 1976: Differentiation and redifferentiation of a transfer cell: Development of sepal nectaries ofAloe andGasteria. Protoplasma89, 105–115.
Smith, G. M., 1955: Cryptogamic botany, Vol. 2, 2nd ed. New York: McGraw-Hill.
Spurr, A. R., 1969: A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res.26, 31–43.
Wiencke, C., Schulz, D., 1977: The development of transfer cells in the haustorium of theFunaria hygrometrica sporophyte. Bryoph. Biblio.13, 147–167.
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Contribution no. 869 from the Battelle-C. F. Kettering Research Laboratory.
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Calvert, H.E., Pence, M.K. & Peters, G.A. Ultrastructural ontogeny of leaf cavity trichomes inAzolla implies a functional role in metabolite exchange. Protoplasma 129, 10–27 (1985). https://doi.org/10.1007/BF01282301
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DOI: https://doi.org/10.1007/BF01282301