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Sex in the Extremes: Lichen-Forming Fungi

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Sex in the Extremes: Lichen-Forming Fungi Mycologist, Volume 19, Part 2 May 2005. ©Cambridge University Press Printed in the United Kingdom. DOI: 10.1017/S0269915XO5002016 Sex in the extremes: lichen-forming fungi FABIAN A. SEYMOUR, PETER D. CRITTENDEN & PAUL S. DYER* School of Biology, University of Nottingham, University Park, Nottingham, NG7 2RD, UK. Tel. +44 (0) 115 9513203, Fax +44 (0) 115 9513251 E-mail: [email protected]; [email protected] *Corresponding Author Lichens are characteristically found in environments subject to extremes of temperature, desiccation and low nutrient status. Despite this sexual structures are often formed in abundance. The underlying mechanisms of sex in lichen-forming fungi are discussed, together with possible ecological reasons for the persistence of sexuality. Special features of lichen sex are highlighted including sex at the limits of life on earth in Antarctica, re-licheniza- tion following sex and dispersal, and the perennial nature of lichen fruiting bodies. Keywords: lichen, fungi, sex, breeding system, (98%) belonging to the Ascomycotina (Kirk et al., symbiosis, extreme environments, Antarctica 2001). They display a variety of morphologies, from flattened crust (crustose) or leafy (foliose) forms to Lichens - living together in a long-term relation- shrubby or pendulous fruticose types (Honegger, 2001) ship (Figs 3, 4, 7, 8). Lichens are seen as a textbook example of a successful Life in extreme environments mutualistic symbiosis. They consist of at least two A key characteristic of lichens is that they have a organisms: a fungus (the ‘mycobiont’), and an remarkable ability to tolerate extreme environmental intimately associated photosynthetic partner (the conditions and sustain growth despite frequent cycles ‘photobiont’). The photobiont can be either a green of desiccation and rehydration, low nutrient alga or a cyanobacterium, and some lichens contain availability and large daily and annual fluctuations in both. The symbiosis is usually between specific temperature (e.g. Øvstedal & Lewis-Smith, 2001; Nash, mycobiont and photobiont partner species. The 1996). They thrive on soil-less substrata such as the mycobiont typically forms the bulk of the lichen and surfaces of rocks or tree bark, and on poorly developed encloses, or even penetrates, the photobiont cells soils such as those of heathlands, peatlands, sand (Dobson, 2003; Purvis, 2000). The physiological dunes and toxic spoil heaps (e.g. Gilbert, 2000; Dobson, interactions that occur between the partners result in a 2003). Lichens are found globally and it has been new distinct entity termed the lichen ‘thallus’, the estimated that they comprise the dominant morphology of which is determined, in the majority of components of vegetation on 8% of the Earth’s cases, by the mycobiont (Büdel & Scheidegger, 1996). terrestrial surface (Larson, 1987). Therefore, by convention the name given to the lichen The resilience of lichens is emphasized by their ‘species’ is that of the fungal component. The symbiotic success in some of the most extreme environments on relationship is obligatory for the lichen-forming fungus Earth: from the freezing boreal-Arctic, alpine and to complete its life-cycle, whereas the algal and Antarctic regions, to hot arid deserts (e.g. Purvis, cyanobacterial partners are often able to exist 2000). For example, lichens dominate the terrestrial independently (Ingold & Hudson, 1993). Lichens are ‘vegetation’ of ice-free areas of Antarctica, mostly in long-lived and extremely slow-growing with some thalli coastal regions (Figs 1-4) (Øvstedal & Lewis-Smith, sustaining growth for hundreds or even possibly in 2001). Here thalli can be exposed to a diurnal excess of thousands of years (Honegger, 1996). amplitude in temperature in excess of 40ºC, and an Lichen-forming fungi constitute almost one fifth annual difference of perhaps 60-70ºC (Øvstedal & (19%) of all know fungal species with the majority Lewis-Smith, 2001; Purvis, 2000). Lichens have even 51 Mycologist, Volume 19, Part 2 May 2005 been found in the heart of continental Antarctica as far photobiont cells enclosed in a loose network of hyphae; as 86º South on exposed rocky nunataks and in dry these structures can develop diffusely over the surface valleys; precipitation in the latter areas is light, falling of the thallus, or in specialized areas called soralia. exclusively as snow (c. 150 mm y-1 rainfall equivalent) Isidia are small, smooth, cylindrical peg-like structures and much of it is lost by sublimation due to low relative that project outwards from the outer cortex of the humidity so that little free liquid water becomes thallus. Soredia and isidia can be dispersed by wind, available (Longton, 1988; Purvis, 2000; Øvstedal & rain or small animals (Büdel & Scheidegger, 1996; Lewis-Smith, 2001). At the other extreme, lichen Dobson 2003; Purvis, 2000). In the short term, dominated communities are found in some of the vegetative propagules have the advantage that both the world’s hottest desert environments where daytime mycobiont and the photobiont are dispersed temperatures soar to 55ºC and night temperatures may simultaneously and so can rapidly establish a new fall below freezing (Nash, 1996) e.g. rich lichen ‘fields’ thallus (Ott, 1987a, b). However, the most commonly occur in the coastal Namib Desert in south west Africa, produced lichen propagules are sexually derived the most spectacular of which are dominated by the ascospores that are exclusively fungal in origin. For yellow fruticose Teloschistes capensis (Fig 5). Even in example, an analysis of the 1350 lichen species listed temperate habitats, lichens may experience by Purvis et al., (1992) in The Lichen Flora of Great temperatures in excess of 70ºC, considerably above the Britain and Ireland reveals that 90% produce ascomata ambient air temperature. containing sexually derived ascospores, whereas only What is more remarkable is that even in these 29% form symbiotic vegetative propagules. Whilst hostile environments many lichens produce sexual ascospores might be effective in long distance dispersal structures, often in abundance (Figs 3, 4, 8). This is of the fungus, as lichen propagules they have the perhaps surprising, as there are metabolic costs to sex inherent problem that they are not normally packaged and many of these environments are subject to low with a photobiont and so chance encounter with a biotic pressure, which might be predicted to favour suitable photobiont is necessary in order to reestablish vegetative/asexual reproduction. Examples of sexual the symbiosis (see later). Only a very few lichens, such reproduction include communities of Acarospora, as Staurothele species, carry algal cells in their fruiting Buellia and Lecidia species in the Antarctic dry valleys bodies and eject these together with fungal spores which grow within rocks (termed cryptoendolithic (Purvis, 2000). Thus, vegetative and sexual lichens), the only visible structures being apothecia reproductive strategies appear to serve two produced on the rock surface (Purvis, 2000), and most complementary functions: a means of rapid spread of species in hot desert lichen communities, including locally-adapted genotypes in a given local environment Teloschistes capensis. Thus lichen-forming fungi provide via asexual propagules, and long-distance dispersal of fascinating examples of ‘extreme sex’! Of course it must potentially novel genotypes via sexually derived be remembered that lichen thalli are invariably ascospores. desiccated and physiologically inactive when exposed to Anatomical details of fruit body development high temperatures and that growth and physiological (mainly apothecia and perithecia) have been studied in activity, including reproduction, occur in hydrated lichens (Jahns et al., 1995) but have offered little thalli at usually moderate to low temperatures. information about underlying genetic mechanisms. Nonetheless, the preponderance of sexual reproduction The nature of sex in lichen-forming fungi therefore in lichens raises questions such as how do they have remains poorly understood. For example, do lichens sex, what are the reasons for sexuality in harsh have any special adaptations for ‘extreme sex’? environments, and does ‘lichen sex’ have any special characteristics? Breeding systems in lichen-forming fungi Reproduction in Lichens As in ascomycete fungi in general, sex in lichen fungi can occur via one of two principal breeding systems. Being dual organisms, reproduction and dispersal of These are heterothallism in which individuals are lichens present challenges since both partners have to self-sterile and there is a requirement for a compatible be present for the successful development of a new partner of different mating type for sexual reproduction lichen thallus (Dobson, 2003). Evolution has provided to occur, and homothallism in which individuals are one solution in the form of vegetative propagules such self-fertile, although they may retain the ability to mate as ‘isidia’ and ‘soredia’, which contain both the fungal with similar genetic strains (Dyer et al., 1992). Inherent and photosynthetic partner. Soredia typically consist of experimental difficulties, such as very slow growth 52 Mycologist, Volume 19, Part 2 May 2005 Fig 1 Rock outcrops of the Haupt Nunataks, Wilkes Land, Antarctica, on which sexually reproducing lichens occur. Fig 2 Rocky fell-field near Casey Station (Wilkes Land), Antarctica, with dense cover of the black fruticose lichen Usnea sphacelata. Fig 3 Fruticose thalli of Usnea
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