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PLOS ONE  2012 

Genetic Basis of Self-Incompatibility in the Lichen-Forming Fungus Lobaria pulmonaria and Skewed Frequency Distribution of Mating-Type Idiomorphs: Implications for Conservation

DOI: 10.1371/journal.pone.0051402

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Abstract:

Fungal populations that reproduce sexually are likely to be genetically more diverse and have a higher adaptive potential than asexually reproducing populations. Mating systems of fungal species can be self-incompatible, requiring the presence of isolates of different mating-type genes for sexual reproduction to occur, or self-compatible, requiring only one. Understanding the distribution of mating-type genes in populations can help to assess the potential of self-incompatible species to reproduce sexually. In the locally threatened epiphytic lichen-forming fungus Lobaria pulmonaria (L.) Hoffm., low frequency of sexual reproduction is likely to limit the potential of populations to adapt to changing environmental conditions. Our study provides direct evidence of self-incompatibility (heterothallism) in L. pulmonaria. It can thus be hypothesized that sexual reproduction in small populations might be limited by an unbalanced distribution of mating-type genes. We therefore assessed neutral genetic diversity (using microsatellites) and mating-type ratio in 27 lichen populations (933 individuals). We found significant differences in the frequency of the two mating types in 13 populations, indicating a lower likelihood of sexual reproduction in these populations. This suggests that conservation translocation activities aiming at maximizing genetic heterogeneity in threatened and declining populations should take into account not only presence of fruiting bodies in transplanted individuals, but also the identity and balanced representation of mating-type genes.

References

[1]  Bell G (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality. Berkeley: University of California Press. 635 p.
[2]  Whittle CA, Nygren K, Johannesson H (2011) Consequences of reproductive mode on genome evolution in fungi. Fungal Genet Biol 48: 661–667.
[3]  Scarascia-Mugnozza GT, Perrino P (2002) The history of ex-situ conservation and use of plant genetic resources. In: Engels JMM, Ramanatha Rao V, Brown AHD, Jackson MT, editors. Managing plant genetic diversity. Oxon: CABI Publishing. 1–22.
[4]  Murtagh GJ, Dyer PS, Crittenden PD (2000) Sex and the single lichen. Nature 404: 564.
[5]  Honegger R, Scherrer S (2008) Sexual reproduction in lichen-forming ascomycetes. In: Nash TH III, editor. Lichen Biology. Cambridge: Cambridge University Press. 94–103.
[6]  Büdel B, Scheidegger C (2008) Thallus morphology and anatomy. In: Nash TH III, editor. Lichen Biology. Cambridge: Cambridge University Press. 40–68.
[7]  Seymour FA, Crittenden PD, Dickinson MJ, Paoletti M, Montiel D, et al. (2005) Breeding systems in the lichen-forming fungal genus Cladonia. Fungal Genet Biol 42: 554–63.
[8]  Charlesworth B (1980) The cost of sex in relation to mating system. J Theor Biol 84: 655–671.
[9]  Charlesworth B (1990) Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet Res 55: 199–221.
[10]  Kück U, P?ggeler S (2009) Cryptic sex in fungi. Fungal Biol Rev 23: 86–90.
[11]  Hawksworth DL (1990) The long-term effects of air pollutants on lichen communities in Europe and North America. In: Woodwell GM, editor. The Earth in transition: patterns and processes of biotic impoverishment. Cambridge: Cambridge University Press. 45–64.
[12]  Brown DH (1992) Impact of agriculture on bryophytes and lichens. In: Bates JW, Farmer AM, editors. Bryophytes and lichens in a changing environment. Oxford: Clarendon Press. 259–83.
[13]  Hawksworth DL, Rose F, Coppins BJ (1973) Changes in the lichen flora of England and Wales attributable to pollution of the air by sulphur dioxide. In: Ferry BW, Baddeley MS, Hawksworth DL, editors. Air pollution and lichens. Toronto: University Toronto Press. 330–367.
[14]  Stofer S, Bergamini A, Aragon G, Carvalho P, Coppins BJ, et al. (2006) Species richness of lichen functional groups in relation to land use intensity. Lichenologist 38: 331–353.
[15]  Coppin E, Debuchy R, Arnaise S, Picard M (1997) Mating types and sexual development in filamentous ascomycetes. Microbiol Mol Biol Rev 61: 411–428.
[16]  Kronstad JW, Staben C (1997) Mating type in filamentous fungi. Annu Rev Genet 31: 245–276.
[17]  Heitman J, Kronstad JW, Taylor JW, Casselton LA (2007) Sex in Fungi: Molecular Determination and Evolutionary Implications. Washington DC: ASM Press. 572 p.
[18]  Turgeon BG, Yoder OC (2000) Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet Biol 31: 1–5.
[19]  Nelson MA (1996) Mating systems in Ascomycetes: a romp in the sac. Trends Genet 12: 69–74.
[20]  Turgeon BG, Bohlmann H, Ciuffetti LM, Christiansen SK, Yang G, et al. (1993) Cloning and analysis of the mating type genes from Cochliobolus heterostrophus. Mol Gen Genet 238: 270–284.
[21]  Martin T, Lu S-W, van Tilbeurgh H, Ripoll DR, Dixelius C, et al. (2010) Tracing the origin of fungal α1 domain places its ancestor in the HMG-box superfamily: Implications for fungal mating-type evolution. PLoS ONE 5: e15199 doi:10.1371/journal.pone.0015199.
[22]  Arie T, Christiansen SK, Yoder OC, Turgeon BG (1997) Efficient cloning of ascomycete mating type genes by PCR amplification of the conserved MAT HMG box. Fungal Genet Biol 21: 118–130.
[23]  Arie T, Kaneko I, Yoshida T, Noguchi M, Nomura Y, et al. (2000) Mating-type genes from asexual phytopathogenic ascomycetes Fusarium oxysporum and Alternaria alternata. Mol Pl Micr Interact 13: 130–1339.
[24]  Honegger R, Zippler U, Gansner H, Scherrer S (2004) Mating systems in the genus Xanthoria (lichen-forming ascomycetes). Mycol Res 108: 480–488.
[25]  Rydholm C, Dyer PS, Lutzoni F (2007) DNA sequence characterization and molecular evolution of MAT1 and MAT2 mating-type loci of the self-compatible ascomycete mold Neosartorya fischeri. Eukaryot Cell 6: 868–874.
[26]  Dyer PS, Paoletti M (2005) Reproduction in Aspergillus fumigatus: sexuality in a supposedly asexual species? Med Mycol 43: S7–S14.
[27]  Consolo V, Cordo C, Salerno G (2005) Mating-type distribution and fertility status in Magnaporthe grisea populations from Argentina. Mycopathologica 160: 285–290.
[28]  Saleh D, Xu P, Shen Y, Li C, Adreit H, et al. (2012) Sex at the origin: an Asian population of the rice blast fungus Magnaporthe oryzae reproduces sexually. Mol Ecol 21: 1330–44.
[29]  Olarte RA, Horn BW, Dorner JW, Monacell JT, Singh R, et al. (2012) Effect of sexual recombination on population diversity in aflatoxin production by Aspergillus flavus and evidence for cryptic heterokaryosis. Mol Ecol 21: 1453–76.
[30]  Grube M, Spribille T (2012) Exploring symbiont management in lichens. Mol Ecol 21: 3098–3099.
[31]  Hilmo O, Lundemo S, Holien H, Stengrundet K, Stenoien HK (2012) Genetic structure in a fragmented Northern Hemisphere rainforest: large effective sizes and high connectivity among populations of the epiphytic lichen Lobaria pulmonaria.. Mol Ecol 21: 3250–3265.
[32]  Schei FH, Blom HH, Gjerde I, Grytnes JG, Heegaard E (2012) Fine-scale distribution and abundance of epiphytic lichens: environmental filtering or local dispersal dynamics? J Veg Sci 23: 459–470.
[33]  Werth S, Wagner HH, Gugerli F, Holderegger R, Csencsics D, et al. (2006) Quantifying dispersal and establishment limitation in a population of an epiphytic lichen. Ecology 87: 2037–2046.
[34]  Scheidegger C, Werth S (2009) Conservation strategies for lichens: insights from population biology. Fung Biol Rev 23: 55–66.
[35]  Dal Grande F, Widmer I, Wagner HH, Scheidegger C (2012) Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Mol Ecol 21: 3159–72.
[36]  Wirth VHS, Sch?ller H, Scholz P, Ernst G, Feuerer T, et al. (1996) Rote Liste der Flechten (Lichenes) der Bundesrepublik Deutschland. In: Bonn-Bad Godesberg: Bundesamt für Naturschutz, Schriftenreihe für Vegetationskunde Schmitt JA, Benkert D, D?rfelt H, editors. Rote Liste Gef?hrdeter Pflanzen Deutschlands. 28: 307–368.
[37]  Scheidegger C, Goward T (2002) Monitoring lichens for conservation: red lists and conservation action plans. In: Nimis PL, Scheidegger C, Wolseley P, editors. Lichen Monitoring - Monitoring Lichens. Dordrecht: Kluwer Academic Publishers. 163–181.
[38]  Zoller S, Lutzoni F, Scheidegger C (1999) Genetic variation within and among populations of the threatened lichen Lobaria pulmonaria in Switzerland and implications for its conservation. Mol Ecol 8: 2049–2059.
[39]  Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters 9: 615–629.
[40]  Widmer I, Dal Grande F, Excoffier L, Holderegger R, Keller C, et al.. (2012) European phylogeography of the epiphytic lichen fungus Lobaria pulmonaria and its green algal symbiont. Mol Ecol DOI: 10.1111/mec.12051.
[41]  Denison WC (2003) Apothecia and ascospores of Lobaria oregana and Lobaria pulmonaria investigated. Mycologia 95: 513–518.
[42]  Widmer I, Dal Grande F, Cornejo C, Scheidegger C (2010) Highly variable microsatellite markers for the fungal and algal symbionts of the lichen Lobaria pulmonaria and challenges in developing biont-specific molecular markers for fungal associations. Fungal Biol 114: 538–544.
[43]  Ochman H, Gerber AS, Hartl DL (1988) Genetic applications of an inverse polymerase chain reaction. Genetics 120: 621–623.
[44]  Liu YG, Whittier RF (1995) Thermal Asymmetric Interlaced PCR - automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25: 674–681.
[45]  Singer T, Burke E (2003) High-throughput TAIL-PCR as a tool to identify DNA flanking insertions. Methods Mol Biol 236: 241–271.
[46]  Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, et al. (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35: W71–74.
[47]  Mikryukov VS (2011) Population ecology of epiphytic lichen Lobaria pulmonaria (L.) Hoffm. in Urals and Siberia. Ph.D. Thesis. Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences: Ekaterinburg, Russia.
[48]  Walser JC, Sperisen C, Soliva M, Scheidegger C (2003) Fungus-specific microsatellite primers of lichens: application for the assessment of genetic variation on different spatial scales in Lobaria pulmonaria. Fungal Genet Biol 40: 72–82.
[49]  Dal Grande F, Widmer I, Beck A, Scheidegger C (2010) Microsatellite markers for Dictyochloropsis reticulata (Trebouxiophyceae), the symbiotic alga of the lichen Lobaria pulmonaria (L.). Conserv Genet 11: 1147–1149.
[50]  Haubold B, Hudson RR (2000) LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics 16: 847–848.
[51]  Raymond M, Rousset F (1995) genepop (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86: 248–249.
[52]  Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47–50.
[53]  Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24: 2498–2504.
[54]  AnalystSoft Inc. StatPlus:mac - statistical analysis program for Mac OS. Version 2009. www.analystsoft.com/en/(accessed 17 October 2012).
[55]  Foster SJ, Fitt BDL (2004) Isolation and characterization of the mating-type (MAT) locus from Rhynchosporium secalis. Curr Genet 44: 277–286.
[56]  Walser JC, Gugerli F, Holderegger R, Kuonen D, Scheidegger C (2004) Recombination and clonal propagation in different populations of the lichen Lobaria pulmonaria. Heredity 93: 322–329.
[57]  Walser JC (2004) Molecular evidence for limited dispersal of vegetative propagules in the epiphytic lichen Lobaria pulmonaria. Am J Bot 91: 1273–1276.
[58]  Werth S, Gugerli F, Holderegger R, Wagner HH, Csencsics D, et al. (2007) Landscape-level gene flow in Lobaria pulmonaria, an epiphytic lichen. Mol Ecol 16: 2807–2815.
[59]  Pentecost A, Richardson CB (2011) Niche separation and overlap in the foliose lichens Lobaria pulmonaria (L.) Hoffm. and L. virens (With.) Laundon in the Killarney oakwoods, Ireland. Royal Irish Academy 111: 1–7.
[60]  Gauslaa Y, Palmqvist K, Solhaug KA, Hilmo O, Holien H, et al. (2009) Size-dependent growth of two old-growth associated macrolichen species. New Phytol 181: 683–692.
[61]  Pringle A, Chen D, Taylor JW (2003) Sexual fecundity is correlated to size in the lichenized Xanthoparmelia cumberlandia. Bryologist 106: 221–225.
[62]  Koella JC (1988) The Tangled Bank: The maintenance of sexual reproduction through competitive interactions. J Evol Biol 2: 95–116.
[63]  Stat M, Loh WKW, Hoegh-Guldberg O, Carter DA (2008) Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs 27: 763–772.
[64]  Genkai-Kato M, Yamamura N (1999) Evolution of mutualistic symbiosis without vertical transmission. Theor Popul Biol 55: 309–323.
[65]  Dal Grande F (2011) Phylogeny and co-phylogeography of a photobiont-mediated guild in the lichen family Lobariaceae. PhD Thesis. Bern, Switzerland: University of Bern.
[66]  Hoistad F, Gjerde I (2011) Lobaria pulmonaria can produce mature ascospores at an age of less than 15 years. Lichenologist 43: 495–497.
[67]  Tomiuk J, Guldbrandtsen B, Loeschcke V (1998) Population differentiation through mutation and drift – a comparison of genetic identity markers. Genetica 102/103: 545–558.
[68]  Arnaud-Haond S, Duarte CM, Alberto F, Serr?o EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16: 5115–5139.
[69]  Honegger R (2008) Mycobionts. In: Nash TH III, editor. Lichen Biology, 2nd edn. Cambridge: Cambridge University Press. 27–39.
[70]  Alby K, Schaefer D, Bennett RJ (2009) Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 460: 890–893.
[71]  Lin X, Hull CM, Heitman J (2005) Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434: 1017–1021.
[72]  Wang L, Lin X (2011) Mechanisms of unisexual mating in Cryptococcus neoformans. Fungal Genet Biol 48: 651–660.
[73]  Scherrer S, Zippler U, Honegger R (2005) Characterization of the mating-type locus in the genus Xanthoria (lichen-forming ascomycetes, Lecanoromycetes). Fungal Genet Biol 42: 976–988.
[74]  Paoletti M, Seymour FA, Alcocer MJC, Kaur N, Calvo AM, et al. (2007) Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans.. Curr Biol 17: 1384–1389.
[75]  Scheidegger C (1995) Early development of transplanted isidioid soredia of Lobaria pulmonaria in an endangered population. Lichenologist 27: 361–374.
[76]  Scheidegger C, Frey B, Zoller S (1995) Transplantation of symbiotic propagules and thallus fragments: methods for the conservation of threatened epiphytic lichen populations. Mitteilungen der Eidgen?ssisches Forschungsanstalt für Wald, Schnee und Landschaft 70: 41–62.
[77]  Barton NH, Charlesworth B (1998) Why sex and recombination? Science 281: 1986–1990.
[78]  Otto SP, Lenormand T (2002) Resolving the paradox of sex and recombination. Nat Rev Genet 3: 252–261.
[79]  Scheidegger C, Bilovitz PO, Werth S, Widmer I, Mayrhofer H (2012) Hitchhiking with forests: population genetics of the epiphytic lichen Lobaria pulmonaria in primeval and managed forests in southeastern Europe. Ecology and Evolution 2: 2223–2240.
[80]  Honegger R, Zippler U (2007) Mating systems in representatives of Parmeliaceae, Ramalinaceae and Physciaceae (Lecanoromycetes, lichen-forming ascomycetes). Mycol Res 111: 424–32.

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