Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-22T12:56:31.836Z Has data issue: false hasContentIssue false

Cell wall dynamics under conditions of diffuse growth in the thick-walled cortical tissue (prosoplectenchyma) of Ramalina usnea

Published online by Cambridge University Press:  17 June 2019

William B. SANDERS
Affiliation:
Department of Biological Sciences, Florida Gulf Coast University, 10501 FGCU Blvd, Ft. Myers, Florida 33965-6565, USA. Email: [email protected]
Asunción DE LOS RÍOS
Affiliation:
Museo Nacional de Ciencias Naturales (CSIC), Departamento de Biogeoquímica y Ecología Microbiana, Serrano 115 dpdo, Madrid 28006, Spain.

Abstract

A recent field study indicated that thalli of the beard lichen Ramalina usnea undergo diffuse (“intercalary”) growth throughout their length. We examined thallus sections with TEM to better understand how the highly thickened cell walls of the prosoplectenchymatous cortex behave under conditions of continued expansion. Cell protoplasts were surrounded by massive accumulations of structured electron-dense wall layers interspersed with amorphous, electron-transparent substances, visible as concentric rings in transverse section. Nearest the protoplast, electron-dense wall layers were distinct and more or less alternated with irregular deposits of electron-transparent material. With increasing distance from the protoplast, the electron-dense wall layers were increasingly disrupted and intermixed among the electron-transparent materials. New cell branches grew through the accumulated wall materials, interrupting the layers they penetrated while producing their own concentric wall layers. The differing amounts of cell wall material accumulated was further indication of the different relative ages of such neighbouring cells. These observations suggest that cell walls are disrupted by diffuse tissue expansion and continually replaced by new walls and wall materials deposited to their interior at the interface with the protoplast. This pattern of development, documented previously in R. menziesii and U. longissima, suggests that component cells of lichen prosoplectenchyma behave quite differently from those of diffusely expanding filaments studied in non-lichen-forming fungi, where a single, discrete cell wall is maintained throughout growth.

Type
Articles
Copyright
Copyright © British Lichen Society 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Boissière, J. C. (1987) Ultrastructural relationship between the composition and the structure of the cell wall of the mycobiont of two lichens. Bibliotheca Lichenologica 38: 395409.Google Scholar
Bowman, S. M. & Free, S. J. (2006) The structure and synthesis of the fungal cell wall. BioEssays 28: 799808.Google Scholar
Brandt, T. (1906) Beiträge zur anatomischen Kenntnis der Flechtengattung Ramalina. Hedwigia 45: 124158.Google Scholar
Christensen, M. J., Bennett, R. J., Ansari, H. A., Koga, H., Johnson, R. D., Bryan, G. T., Simpson, W. R., Koolaard, J. P., Nickless, E. M. & Voisey, C. R. (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genetics and Biology 45: 8493.Google Scholar
Craig, G. D., Gull, K. & Wood, D. A. (1977) Stipe elongation in Agaricus bisporus. Journal of General Microbiology 102: 337347.Google Scholar
de los Ríos, A. & Ascaso, C. (2002) Preparative techniques for transmission electron microscopy and confocal laser scanning microscopy of lichens. In Protocols in Lichenology (Kranner, I. C., Beckett, R. P. & Varma, A. K., eds): 87117. Berlin and Heidelberg: Springer-Verlag.Google Scholar
Galun, M., Braun, A., Frensdorf, A. & Galun, E. (1976) Hyphal walls of isolated lichen fungi. Archives of Microbiology 108: 916.Google Scholar
Gooday, G. W. (1995) The dynamics of hyphal growth. Mycological Research 99: 385394.Google Scholar
Hafellner, J. & Bellemère, A. (1981) Elektronoptische Untersuchungen an Arten der Flechtengattung Brigantiaea. Nova Hedwigia 35: 237261.Google Scholar
Henssen, A. & Dobelmann, A. (1987) Development of the spongiostratum in Anzia and Pannoparmelia. Bibliotheca Lichenologica 25: 103108.Google Scholar
Honegger, R. & Bartnicki-García, S. (1991) Cell wall structure and composition of cultured mycobionts from the lichens Cladonia macrophylla, Cladonia caespiticia, and Physcia stellaris (Lecanorales, Ascomycetes). Mycological Research 95: 905914.Google Scholar
Honegger, R. & Haisch, A. (2001) Immunocytochemical location of the (1→3)(1→4)-β-glucan lichenin in the lichen-forming ascomycete Cetraria islandica (Icelandic moss). New Phytologist 150: 739746.Google Scholar
Kärenlampi, L. (1970) Morphological analysis of the growth and productivity of the lichen Cladonia alpestris. Reports of the Kevo Subarctic Research Station 7: 915.Google Scholar
Kashiwadani, H. (1990) Some Chilean species of the genus Ramalina (lichens). Bulletin of the National Science Museum, Tokyo, Series B 16(1): 112.Google Scholar
Marchant, R. (1979) Wall growth during spore differentiation and germination. In Fungal Wall and Hyphal Growth (Burnett, J. H. & Trinci, A. P. J., eds): 115148. Cambridge: Cambridge University Press.Google Scholar
Pérez-Ortega, S., Fernández-Mendoza, F., Raggio, J., Vivas, M., Ascaso, C., Sancho, L. G., Printzen, C. & de los Ríos, A. (2012) Extreme phenotypic variation in Cetraria aculeata (lichenized Ascomycota): adaptation or incidental modification? Annals of Botany 109: 11331148.Google Scholar
Read, N. (2011) Exocytosis and growth do not occur only at hyphal tips. Molecular Microbiology 81: 47.Google Scholar
Rolstad, J. & Rolstad, E. (2008) Intercalary growth causes geometric length expansion in Methuselah's beard lichen (Usnea longissima). Botany 86: 12241232.Google Scholar
Sanders, W. B. (1989) Growth and development of the reticulate thallus in the lichen Ramalina menziesii. American Journal of Botany 76: 666678.Google Scholar
Sanders, W. B. (1992) Comparative in situ studies of thallus net development in morphologically distinct populations of the lichen Ramalina menziesii. Bryologist 95: 192204.Google Scholar
Sanders, W. B. & Ascaso, C. (1995) Reiterative production and deformation of cell walls in expanding thallus nets of the lichen Ramalina menziesii (Lecanorales, Ascomycetes). American Journal of Botany 82: 13581366.Google Scholar
Sanders, W. B. & de los Ríos, A. (2012) Development of thallus axes in Usnea longissima (Parmeliaceae, Ascomycota), a fruticose lichen showing diffuse growth. American Journal of Botany 99: 9981009.Google Scholar
Sanders, W. B. & Tokamov, S. A. (2015) Diffuse growth in the fruticose beard lichen Ramalina usnea (L.) R. Howe. Lichenologist 47: 5158.Google Scholar
Schlarmann, G., Peveling, E. & Tenberge, K. (1990) The occurrence of chitin in the cell walls of ascomycetes mycobionts. Bibliotheca Lichenologica 38: 395409.Google Scholar
Schwendener, S. (1860) Untersuchungen über den Flechtenthallus. Beiträge zur Wissenschaftlichen Botanik (von Carl Nägeli) 2: 109186 (+ Tables I–IV).Google Scholar
Voisey, C. R. (2010) Intercalary growth in hyphae of filamentous fungi. Fungal Biology Reviews 24: 123131.Google Scholar
Wessels, J. G. H. (1994) Developmental regulation of fungal cell wall development. Annual Review of Phytopathology 32: 413437.Google Scholar