Under favourable climatic conditions the mycobiont of Coniocybe furfuracea bears masses of conidia in chains on macronematous conidiophores. The same type of conidia were also formed by axenically grown mycobionts which had been isolated from single ascospores. Germinating conidia were found on the thalli. Coniocybe furfuracea is one of the very few lichen mycobionts so far known with a teleomorph and hyphomycetous anamorp

Honegger, Rosmarie

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Lichenologist 17(3): 273-279 (1985)THE HYPHOMYCETOUS ANAMORPH OFCONIOCYBE FURFURACEARosmarie HONEGGER*Abstract: Under favourable climatic conditions the mycobiont of Coniocybefurfuracea bears masses of conidia in chains on macronematous conidiophores. Thesame type of conidia were also formed by axenically grown mycobionts which hadbeen isolated from single ascospores. Germinating conidia were found on the thalli.Coniocybe furfuracea is one of the very few lichen mycobionts so far known with ateleomorph and hyphomycetous anamorph.IntroductionAbout 8000 species of lichenized fungi form conidia in pycnidial conidiomata(Vobis & Hawksworth 1981), some of which represent the coelomycetousanamorph, others spermatial stages or, with high probability, functionlessrelics of spermatial stages (Vobis 1977, Vobis & Hawksworth 1981, Honegger1984a, b). Various lichenized Hyphomycetes have been described (reviewedby Vobis & Hawksworth 1981), but hyphomycetous anamorphs seem to beextremely rare among lichen-forming fungi with known teleomorphs. Themycobiont of Vezdaea aestivalis forms macronematous conidiophores in thesymbiotic state and very soon after germination in pure cultures of ascospores(Tschermak-Woess & Poelt 1976). Conidial formation was also observed incultured, but not in free-living symbiotic states of the mycobiont of Pertusariapertusa (Lallemant 1977a, b). Other reports on hyphomycetous structures incultured lichen mycobionts (Hale 1957, Ahmadjian 1963) were either notsubstantiated in subsequent studies (Ahmadjian 1965) or require furtherexamination. Hyphomycete-like structures embedded in the gelatinousthallus which bear spermatia were observed in some Collema species(Bachmann 1912, Degelius 1954), and very peculiar synnematous structurestermed hyphophores have been detected in the foliicolous Asterothyriaceae(reviewed by Vobis & Hawsksworth 1981).In the course of a study on the mycobiont-phycobiont relationship inConiocybe furfuracea, many macronematous conidiophores were noted. Therelationship of these structures to the teleomorph of Coniocybe furfuracea(Fig. 1) was investigated by means of culture techniques and scanningelectron microscopy.Materials and MethodsFresh material was collected in the cold season (November to April 1982/83 and 1983/84) in dif-ferent locations of central Switzerland. Only very well developed, fertile thalli were used. (1)•Cytology, Institute of Plant Biology, University of Zurich, CH-8008 Zurich, Switzerland.0024-2829/85/030273 + 07 $03.00/0 © 1985 British Lichen Societyuse, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282985000354Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:05:22, subject to the Cambridge Core terms of274 THELICHENOLOGIST Vol.17Merliwald W Giswil, NW, 1300 m, November 1982. (2) Ratenpass E Aegeri, SZ, 1000 m,November 1982, March 1983, November 1983. (3) Murgtal S Walensee, SG, 750 m, April 1984,E. Urmi.Herbarium specimens (Herbarium Institute of Systematic Botany, University of Zurich,Zurich) examined: Switzerland: (1) Hongg bei Felsenegg, ZH, 1900, Hegetschweiler. (2) Salevebei Genf, GE, Schweiz, Bernet [Krypt. exsicc. no. 814]. (3) Hiitten bei Zurich, ZH, 1975, K.Urmi. (4) Silenen, UR, 1974, K. Urmi. Germany: (1) Wombrunn, im Griinewalder Park beiMunchen, 1892, Arnold [Lich. Monacenses exs. no. 225]. (2) Kreuzberger Alpe bei Schliersee,bayr. Alpen, 1882, Arnold.Isolation of the mycobiont and culture techniques. Mature ascomata were broken off the thalluswith the aid of fine, sterile forceps. The surface of a sterile non-nutrient agar (Bold's basalmedium, BBM, according to Deason & Bold 1960) was touched repeatedly with the mazaedium.At each contact of the mazaedium with the agar surface a group of ascospores remained on theagar. The first five groups of each ascoma were discarded in order to eliminate possible con-taminants. Dispersion of the ascospores was obtained by spreading the groups of ascospores overthe agar surface with the aid of a sterile needle and using a dissecting microscope. The Petri disheswere incubated at 17°C at a 14:10h light:dark interval. Germination of ascospores occurredwithin 1 week and was studied with a Reichert Biovert conversion microscope.Single spore isolates were transferred either to a nutrient medium containing BBM with 3-5°0malt extract, 0-5°0 glucose, 005°o peptone, 0025°o casamino acids, and 0025°o yeast extract(agar: T5°(l), or to fresh non-nutrient agar (BBM) and covered with the Stichococcus bacillarisphycobiont which had been cultured axenically on the same non-nutrient medium. All strains arekept in our laboratory.Transmission electron microscopy. See Honegger (1984b).Scanning electron microscopy (SEM). Lichen thalli or agar blocks with cultured symbiontswere exposed to the vapour of a 4% solution of osmium tetroxide at room temperature overnight,dehydrated in a graded series of acetone, critical point dryed and mounted on specimen stubs withconductive silver print paint (GC Electronics). Mounted specimens were sputter-coated with analloy of gold and palladium (80°o/20°o) and examined in a Cambridge Stereoscan S-4.ResultsIn the fluffy thalli of freshly collected and herbarium samples of Coniocybefurfuracea the mycobiont either tightly adheres to or overgrows the chain-likecolonies of the ulotrichalean Stichococcus phycobiont, or forms erect hyphae(Fig. 2A-C). In most of the samples examined no special structures could beseen at the tip of the erect hyphae (Fig. 2B). In material collected in late winter(March-April), when the temperature was not too cold and the humidity highdue to melting snow around the tree trunks, these erect hyphae produced amass of conidia, often in chains (Fig. 2D-E) and so represent conidiophores.As the loose thalli of Coniocybe furfuracea are not clearly delimited and yeastsand other conidial fungi can occasionally be seen developing within the tufts,it was not clear whether the abundantly formed conidiophores of the funguscontacting the phycobiont cells were produced by the mycobiont or byanother fungus living in the same habitat. Culture experiments becamenecessary.Single ascospore isolates of Coniocybe furfuracea were easily obtained (seeabove). In material collected in the winter months the germination rate wasabove 90%, and the contamination rate was surprisingly low. When trans-ferred to nutrient agar the mycobiont formed cartilaginous, thallus-likestructures with filamentous hyphal growth at the periphery (Fig. 3A), butalmost pseudoparenchymatous structures in the older parts. This is a commonfeature among lichen mycobionts (reviewed by Lallemant 1977b), and theuse, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282985000354Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:05:22, subject to the Cambridge Core terms of1985 Hyphomycetous anamorph of C. furfur acea—Honegger 275FIG. 1. The teleomorph of Coniocybe furfuracea. A, SEM preparation of a young, not fullydeveloped ascoma, x 300. B, SEM preparation of two fully differentiated ascospores with charac-teristically structured exospore, x 5000. C, TEM preparation of a cross-section of part of themazaedium with different developmental stages of asci (a) and ascospores (as), cr, croziers,x 3800. Scale = 1 ftm unless otherwise stated.use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282985000354Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:05:22, subject to the Cambridge Core terms of276 THE LICHENOLOGIST Vol. 17FIG. 2. SEM of thallus morphology and conidiophore structure in the symbiotic (freeliving) stateof Coniocyte furfuracea. A, Thalline tuft with chain-like colonies of the ulotrichalean Stichococcusbacillaris phycobiont (phy) which are held together by the closely contacting mycobiont, andnumerous erect hyphae of the mycobiont (cp), x 460. B, Phycobiont cells overgrown by themycobiont, and erect hyphae which represent dormant conidiophores (cp), x 1300. C, Agerminating (arrow) conidium (c) and a chain of conidia (c) on the thallus surface, x 4700. D, Tipof a conidiophore (cp) producing a chain of conidia (c), x 6700. E, Conidiophore producing aconidium (c). Phy, phycobiont cell, x 4700. Scale = 1 jim unless otherwise stated.use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282985000354Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:05:22, subject to the Cambridge Core terms ofFIG. 3. SEM of growth pattern and conidium formation in axenically cultured Coniocybefurfur-acea. A, The growing edge of a thallus-like structure of the mycobiont on nutrient agar withnumerous swollen cells (arrows), x 2000. B, Filamentous growth of the mycobiont on non-nutrient agar with chain-like colonies of Stichococcus bacillaris, the cultured phycobiont, x 1900.C, Conidiophores and conidia developing on non-nutrient agar without phycobiont cells, x 4700.D, Conidium (c) producing conidiophore (cp) developing in between phycobiont cells (phy) onnon-nutrient agar, x 8500. Scale = 1 fan.use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282985000354Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:05:22, subject to the Cambridge Core terms of278 THE LICHENOLOGIST Vol.17same is true for the many swollen cells rich in lipid droplets (Fig. 3A) whichare produced on nutrient media. On non-nutrient media, filamentous hyphalgrowth was observed (Fig. 3B-C). No conidiophores were formed on thenutrient medium, but a few developed on the non-nutrient medium (Fig. 3D).A limited number of conidiophores appeared on the non-nutrient mediumafter addition of the Stichococcus phycobiont (Fig. 3D), although themycobiont-phycobiont relationship was nowhere as close as in the free-livingsymbiotic state (Fig. 2B—C). Development from ascospore germination toconidium production took 7.\ months. The culture experiments were carriedout in triplicate, with lichens collected at three different sites.Conidial germination was also observed on the surface of free-living thalli(Fig. 2B). The conidia can be easily distinguished from ascospores (Figs1B-C) by their different size, shape, and surface structure.DiscussionThe present data demonstrate the teleomorph-anamorph relationship inConiocybe furfuracea, a situation also observed in other calicialean myco-bionts. Vobis (1977) reported conidium germination under axenic conditionsin Calicium adspersum but there the conidia are formed in pycnidialconidiomata. This is also the case in all other calicialean conidia so farreported (e.g. Gallee 1972, Henssen & Jahns 1973, Poelt 1974, Tibell 1978),with the exception of the non-lichenized Mycocalicium schefflerae which hasa Phialophora-\ike macronematous anamorph (Samuels & Buchanan 1983).However, in many calicialean species no data on conidia are available, sinceascomatal ontogeny and ascus and ascospore structures are the main charac-ters used in the delimitation of species and genera (e.g. Schmidt 1970a, b,Tibell 1971, 1978). The occurrence of coelomycetous and hyphomycetousanamorphs within the same family may at first seem anomalous, but in somenon-lichenized ascomycetes both types of conidium-bearing structures arereported within closely related species or even in different developmentalstages of a single species (reviewed by Miiller 1981). Sporodochial, acervular,and pycnidial conidiomata were detected in the lichen genus Micarea(Coppins 1983). On the basis of studies on ascomatal and ascal ontogeny,Schmidt (1970b) concluded first, that the Caliciaceae (and even more so theCaliciales) are a very heterogeneous group, and secondly that some speciesof Coniocybe (including C. furfuracea) and Chaenotheca differ considerablyfrom other Caliciaceae in that ascus formation occurs in chains. Whether thetype of conidial formation might provide a further taxonomic criterion in theCaliciaceae requires further investigation.The mechanism of conidial formation in Coniocybe furfuracea requiresfurther study as it is not possible to interpret the type of conidiogenesis fromthe SEM pictures available. The conidiophores might represent either true orfalse chain phialides in the sense of Minter et al. (1982, 1983a, b) or evenother types of conidial-bearing structures. Due to the very small size of theconidiogenous cells, only transmission electron microscopic studies willenable a more detailed interpretation to be made. Without these data it isnot possible to make comparisons between the conidiophores of Coniocybeuse, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282985000354Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:05:22, subject to the Cambridge Core terms of1985 Hyphomycetous anamorph of C. furfuracea—Honegger 279furfuracea and non-lichenized fungi, although a certain morphologicalsimilarity to saprophytes of the genera Humicola and Botryotrichum may benoted.My sincere thanks are due to Professor E. Miiller for stimulating discussions; to Drs Katharinaand E. Urmi for the loan of herbarium specimens and collecting fresh material; and to ProfessorD. L. Hawksworth for valuable comments and for improving the style of this manuscript.REFERENCESAhmadjian, V. (1963) The fungi of lichens. Sci. Am. 208: 122-132.Ahmadjian, V. (1965) Lichens. A. Rev. Microbiol. 19: 1-20.Bachmann, F. M. 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Lichenologist 9: 131-136.Vobis, G. & Hawksworth, D. L. (1981) Conidial lichen-forming fungi. In Biology of ConidialFungi (G. T. Cole & B. Kendrick, eds) 1: 245-273. New York: Academic Press.Accepted for publication 2 September 1984use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282985000354Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:05:22, subject to the Cambridge Core terms ofuse, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282985000354Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:05:22, subject to the Cambridge Core terms of

The Hyphomycetous Anamorph of Coniocybe Furfuracea

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