Hostname: page-component-7c8c6479df-hgkh8 Total loading time: 0 Render date: 2024-03-19T10:32:08.330Z Has data issue: false hasContentIssue false

Differences in the sexual aposymbiotic phase of the reproductive cycles of Parmelina carporrhizans and P. quercina. Possible implications for their reproductive biology

Published online by Cambridge University Press:  26 April 2019

D. ALORS
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain. Email: d.alors@gmail.com
Y. CENDÓN-FLÓREZ
Affiliation:
Departamento de Biología y Geología (Área de Biodiversidad y Conservación), ESCET, Universidad Rey Juan Carlos, Móstoles, 28933 Madrid, Spain.
P. K. DIVAKAR
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain. Email: d.alors@gmail.com
A. CRESPO
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain. Email: d.alors@gmail.com
N. GONZÁLEZ.BENÍTEZ
Affiliation:
Departamento de Biología y Geología (Área de Biodiversidad y Conservación), ESCET, Universidad Rey Juan Carlos, Móstoles, 28933 Madrid, Spain.
M. C. MOLINA
Affiliation:
Departamento de Biología y Geología (Área de Biodiversidad y Conservación), ESCET, Universidad Rey Juan Carlos, Móstoles, 28933 Madrid, Spain.

Abstract

Our knowledge of ontogenetic development and reproductive biology in lichen-forming fungi is rather poor. Here, we aim to advance our understanding of the reproductive biology of Parmelina carporrhizans and P. quercina for which mycobiont fungi of both species were cultured in aposymbiotic conditions from ascospores. For P. carporrhizans 48 hours were necessary for 98·6% of apothecia to eject spores, while for P. quercina 100% of apothecia ejected spores in the first 24 hours. In P. quercina, large apothecia ejected more spores than smaller ones. In both species the percentage of spores germinating seemed independent of apothecium size. The percentage germination was higher in P. carporrhizans (72·4%) than in P. quercina (14·3%). Moreover, P. carporrhizans was grown more successfully on culture media than P. quercina. These results suggest that these species have different reproductive strategies, given that P. carporrhizans expels larger spores and in greater numbers than P. quercina as well as having different nutritional requirements (since P. carporrhizans grew successfully in the selected media but P. quercina did not). These characteristics may explain the sympatric speciation of these species.

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

Ahmadjian, V. (1993) The Lichen Symbiosis. New York: John Wiley & Sons, Inc.Google Scholar
Alors, D., Dal Grande, F., Schmitt, I., Kraichak, E., Lumbsch, H. T., Crespo, A. & Divakar, P. K. (2014) Characterization of fungus-specific microsatellite markers in the lichen-forming fungus Parmelina carporrhizans (Parmeliaceae). Applications in Plant Sciences 2: 1400081.Google Scholar
Alors, D., Dal Grande, F., Cubas, P., Crespo, A., Schmitt, I., Molina, M. C. & Divakar, P. K. (2017) Panmixia and dispersal from the Mediterranean Basin to Macaronesian Islands of a macrolichen species. Scientific Reports 7: 40879.Google Scholar
Argüello, A., del Prado, R., Cubas, P. & Crespo, A. (2007) Parmelina quercina (Parmeliaceae, Lecanorales) includes four phylogenetically supported morphospecies. Biological Journal of the Linnean Society 91: 445467.Google Scholar
Armaleo, D. (1991) Experimental microbiology of lichens: mycelial fragmentation, a novel growth chamber, and the origins of thallus differentiation. Symbiosis 11: 163178.Google Scholar
Barton, K. (2013) MuMin: Multi-Model inference model selection and model averaging based on information criteria (AICc and alike). R package version 1.15.6.Google Scholar
Beck, A., Divakar, P. K., Zhang, N., Molina, M. C. & Struwe, L. (2015) Evidence of ancient horizontal gene transfer between fungi and the terrestrial alga Trebouxia. Organisms Diversity and Evolution 15: 235248.Google Scholar
Brunauer, G. & Stocker-Wörgötter, E. (2005) Culture of lichen fungi for future production of biologically active compounds. Symbiosis 38: 187201.Google Scholar
Brunauer, G., Hager, A., Grube, M., Türk, R. & Stocker-Wörgötter, E. (2007) Alterations in secondary metabolism of aposymbiotically grown mycobionts of Xanthoria elegans and cultured resynthesis stages. Plant Physiology and Biochemistry 45: 146151.Google Scholar
Burnham, K. P. & Anderson, D. R. (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. New York: Springer-Verlag.Google Scholar
Clerc, P. & Truong, C. (2008) The non-sorediate and non-isidiate Parmelina species (lichenized ascomycetes, Parmeliaceae) in Switzerland – Parmelina atricha (Nyl.) P. Clerc reinstated in the European lichen flora. Sauteria 15: 175194.Google Scholar
Cordeiro, L. M. C., Iacomini, M. & Stocker-Wörgötter, E. (2004) Culture studies and secondary compounds of six Ramalina species. Mycological Research 108: 489497.Google Scholar
Dal Grande, F., Alors, D., Divakar, P. K., Bálint, M., Crespo, A. & Schmitt, I. (2014) Insights into intrathalline genetic diversity of the cosmopolitan lichen symbiotic green alga Trebouxia decolorans Ahmadjian using microsatellite markers. Molecular Phylogenetics and Evolution 72: 5460.Google Scholar
Deason, D. R. & Bold, H. C. (1960) Phycological studies. I. Exploratory studies of Texas soil algae. University of Texas Publications 6022: 170.Google Scholar
Deduke, C. & Piercey-Normore, M. D. (2015) Substratum preference of two species of Xanthoparmelia. Fungal Biology 119: 812822.Google Scholar
Degtjarenko, P., Marmor, L., Torra, T., Lerch, M., Saag, A., Randlane, T. & Scheidegger, C. (2016) Impact of alkaline dust pollution on genetic variation of Usnea subfloridana populations. Fungal Biology 120: 11651174.Google Scholar
Easton, L. C. & Kleindorfer, S. (2008 a) Germination in two Australian species of Frankenia L., F. serpyllifolia Lindl. and F. foliosa J. M. Black (Frankeniaceae) – effect of seed age, seed mass, light, and temperature. Transactions of the Royal Society of South Australia 132: 2940.Google Scholar
Easton, L. C. & Kleindorfer, S. (2008 b) Interaction effects of seed mass and temperature on germination in Australian species of Frankenia (Frankeniaceae). Folia Geobotanica 43: 383396.Google Scholar
Eaton, S., Zúñiga, C., Czyzewski, J., Ellis, C., Genney, D. R., Haydon, D., Mirzai, N. & Yahr, R. A. (2018) A method for the direct detection of airborne dispersal in lichens. Molecular Ecology Resources 18: 240250.Google Scholar
Fedrowitz, K., Kuusinen, M. & Snäll, T. (2012) Metapopulation dynamics and future persistence of epiphytic cyanolichens in a European boreal forest ecosystem. Journal of Applied Ecology 49: 493502.Google Scholar
Hawksworth, D. L., Blanco, O., Divakar, P. K., Ahti, T. & Crespo, A. (2008) A first checklist of parmelioid and similar lichens in Europe and some adjacent territories, adopting revised generic circumscriptions and with indications of species distributions. Lichenologist 40: 121.Google Scholar
Honegger, R. & Zippler, U. (2007) Mating systems in representatives of Parmeliaceae, Ramalinaceae and Physciaceae (Lecanoromycetes, lichen-forming ascomycetes). Mycological Research 111: 424432.Google Scholar
Johansson, P., Rydin, H. & Thor, G. (2007) Tree age relationships with epiphytic lichen diversity and lichen life history traits on ash in southern Sweden. Ecoscience 14: 8191.Google Scholar
Johnson, J. B. & Omland, K. S. (2004) Model selection in ecology and evolution. Trends in Ecology and Evolution 19: 101108.Google Scholar
Lallemant, R. (1985) Le développement en cultures pures in vitro des mycosymbiotes des lichens. Canadian Journal of Botany 63: 681703.Google Scholar
Lilly, V. G. & Barnett, H. L. (1951) Physiology of the Fungi. New York: McGraw-Hill.Google Scholar
Marshall, W. A. (1996) Aerial dispersal of lichen soredia in the maritime Antarctic. New Phytologist 134: 523530.Google Scholar
McDonald, T. R., Dietrich, F. S. & Lutzoni, F. (2012) Multiple horizontal gene transfers of ammonium transporters/ammonia permeases from prokaryotes to eukaryotes: toward a new functional and evolutionary classification. Molecular Biology and Evolution 29: 5160.Google Scholar
Molina, M. C. & Crespo, A. (2000) Comparison of development of axenic cultures of five species of lichen-forming fungi. Mycological Research 103: 595602.Google Scholar
Molina, M. C., Stocker-Wörgötter, E., Türk, R. & Vicente, C. (1997) Axenic culture of the mycobiont of Xanthoria parietina in different nutritive media: effect of carbon source in spore germination. Endocytobiosis and Cell Research 12: 103109.Google Scholar
Molina, M. C., Crespo, A., Blanco, O. & Hawksworth, D. L. (2002) Molecular phylogeny and status of Diploicia and Diplotomma, with observations on Diploicia subcanescens and Diplotomma rivas-martinezii. Lichenologist 34: 509519.Google Scholar
Molina, M. C., Divakar, P. K., Zhang, N., González, N. & Struwe, L. (2013) Non-developing ascospores found in apothecia of asexually reproducing lichen-forming fungi. International Microbiology 16: 145155.Google Scholar
Molina, M. C., Divakar, P. K. & González, N. (2015) Success in the isolation and axenic culture of Anaptychia ciliaris (Physciaceae, Lecanoromycetes) mycobiont. Mycoscience 56: 351358.Google Scholar
Morando, M., Favero-Longo, S. E., Carrer, M., Matteucci, E., Nascimbene, J., Sandrone, S., Appolonia, L. & Piervittori, R. (2017) Dispersal patterns of meiospores shape population spatial structure of saxicolous lichens. Lichenologist 49: 397413.Google Scholar
Nimis, P. L. (1993) The Lichens of Italy: An Annotated Catalogue. Torino: Museo Regionale di Scienze Naturali.Google Scholar
Núñez-Zapata, J., Divakar, P., Del-Prado, R., Cubas, P., Hawksworth, D. L. & Crespo, A. (2011) Conundrums in species concepts: the discovery of a new cryptic species segregated from Parmelina tiliacea (Ascomycota: Parmeliaceae). Lichenologist 43: 603616.Google Scholar
Núñez-Zapata, J., Alors, D., Cubas, P., Divakar, P. K., Leavitt, S. D., Lumbsch, H. T. & Crespo, A. (2017) Understanding disjunct distribution patterns in lichen-forming fungi: insights from Parmelina (Parmeliaceae, Ascomycota). Botanical Journal of the Linnean Society 184: 238253.Google Scholar
Öckinger, E., Niklasson, M. & Nilsson, S. G. (2005) Is local distribution of the epiphytic lichen Lobaria pulmonaria limited by dispersal capacity or habitat quality? Biodiversity and Conservation 14: 759773.Google Scholar
Ott, S. (1987) Sexual reproduction and developmental adaptations in Xanthoria parietina. Nordic Journal of Botany 7: 219228.Google Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1–128.Google Scholar
R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http:// www.R-project.org.Google Scholar
Sanders, W. B. (2014) Complete life cycle of the lichen fungus Calopadia puiggari (Pilocarpaceae, Ascomycetes) documented in situ: propagule dispersal, establishment of symbiosis, thallus development, and formation of sexual and asexual reproductive structures. American Journal of Botany 101: 18361848.Google Scholar
Sanders, W. B. & Lücking, R. (2002) Reproductive strategies, relichenization and thallus development observed in situ in leaf-dwelling lichen communities. New Phytologist 155: 425435.Google Scholar
Sangvichien, E., Hawksworth, D. L. & Whalley, A. J. S. (2011) Ascospore discharge, germination and culture of fungal partners of tropical lichens, including the use of a novel culture technique. IMA Fungus 2: 143153.Google Scholar
Schauer, T. (1965) Ozeanische flechten in Nordalpenraum. Portugaliae Acta Biologica (B) 8: 17229.Google Scholar
Schielzeth, H. & Nakagawa, S. (2012) Nested by design: model fitting and interpretation in a mixed model era. Methods in Ecology and Evolution 4: 1424.Google Scholar
Schuster, G., Ott, S. & Jahns, H. M. (1985) Artificial cultures of lichens in the natural environment. Lichenologist 17: 247253.Google Scholar
Shanmugam, K., Srinivasan, M. & Hariharan, G. N. (2016) Developmental stages and secondary compound biosynthesis of mycobiont and whole thallus cultures of Buellia subsororioides. Mycological Progress 15: 41.Google Scholar
Tibell, L. B. (1994) Distribution patterns and dispersal strategies of Caliciales. Botanical Journal of the Linnean Society 116: 159202.Google Scholar
Westoby, M., Falster, D., Moles, A., Vesk, P. & Wright, I. (2002) Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33: 125159.Google Scholar
Yamamoto, Y., Kinoshita, Y., Takahagi, T., Kroken, S., Kurokawa, T. & Yoshimura, I. (1998) Factors affecting discharge and germination of lichen ascospores. Journal of the Hattori Botanical Laboratory 85: 267278.Google Scholar