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1342 LICH 44.3 11 1100084 Vondrak 401..418 The Lichenologist 44(3): 401–418 (2012) 6 British Lichen Society, 2012 doi:10.1017/S0024282911000843 Absence of anthraquinone pigments is paraphyletic and a phylogenetically unreliable character in the Teloschistaceae Jan VONDRA´ K, Jaroslav Sˇ OUN, Olga VONDRA´ KOVA´ , Alan M. FRYDAY, Alexander KHODOSOVTSEV and Evgeny A. DAVYDOV Abstract: It has been suggested that the absence of anthraquinones is not a synapomorphic character, but appears independently in unrelated lineages of Teloschistaceae. We analyzed ITS nrDNA regions in species of the genus Caloplaca and present evidence for five such examples: the Caloplaca cerina group, C. obscurella,theC. servitiana group, the C. xerica group and the C. variabilis group (Pyrenodesmia). In some cases, loss of anthraquinones is observed only in individuals within ordinarily pigmented popula- tions, but sometimes the loss covers whole lineages containing one or more species. Both situations are observed in the C. servitiana group. Loss of anthraquinones is always followed by the synthesis of ‘alternative’ pigments (often Sedifolia-grey). In the specimens with anthraquinone-containing apothecia studied, these pigments are not visible in apothecial sections after dissolving anthraquinones in K. Fully unpigmented apothecia have not been observed. The Caloplaca xerica group is a newly established, infraspecific grouping of species related to, and similar to, C. xerica. The Caloplaca servitiana group is also newly established and represents an isolated lineage covering two rather different, but related species. Caloplaca neotaurica is described here as a new species with apothecia of two colour variants; orange-red (with anthraquinones) and grey (with Sedifolia-grey). The genus Huea represents another taxon lacking anthraquinones within Teloschistaceae. The genera Apatoplaca and Cephalophysis, which lack anthraquinones, are tentatively placed in Teloschistaceae, but their phylogenetic identity has not been recognized. Hueidea is reported to have no anthraquinones, but its secondary metabolites should be studied further and its possible placement in Teloschistaceae assessed. We suggest that Caloplaca abbreviata var. lecideoides and C. celata represent variants of C. stillicidiorum lacking anthraquinones. Key words: Apatoplaca, Caloplaca neotaurica, Cephalophysis, Huea, Hueidea, lichens, phylogeny, taxonomy, UV-radiation Accepted for publication 11 October 2011 Introduction J. Vondra´k: Institute of Botany, Academy of Sciences, Za´mek 1, Pru˚honice, CZ-25243, Czech Republic, and In one of the largest lichen families, Teloschis- Faculty of Science, University of South Bohemia, Brani- taceae, the majority of lichens produce yellow- sˇovska´ 31, CZ-370 05, Cˇ eske Budejovice, Czech Re- orange-red anthraquinone pigments in the public. Email: [email protected] J. Sˇ oun: Department of Botany, Faculty of Science, superficial tissues of their fruiting bodies University of South Bohemia, Branisˇovska´ 31, Cˇ eske´ and/or thallus (e.g., Søchting 1997). They Budeˇjovice, CZ-370 05, Czech Republic. are produced in various Teloschistaceae in 1) O. Vondra´kova´: Institute of Steppe (Urals Branch of both thallus and apothecia, 2) in apothecial Russian Academy of Sciences), Pionerskaya st. 11, disc and margin only, 3) in apothecial disc Orenburg, RF-460000, Russia. A. M. Fryday: Herbarium, Department of Plant Biology, only or 4) are entirely absent. Anthraqui- Michigan State University, East Lansing, MI 48824- nones are known to protect lichens from 1312, USA. absorption of UV radiation (Solhaug et al. A. Khodosovtsev: Kherson State University, 40 Rokiv 2003); their content in Xanthoria parietina Zhovtnya str. 27, 73000 Kherson, Ukraine. E. A. Davydov: Altai State University, Lenin Ave. 61, (L.) Beltr. (Teloschistaceae) significantly in- Barnaul, RF-656049, Russia; Tigirek State Reserve, creases with exposition to solar radiation Nikitina, 111, Barnaul, RF-656043, Barnaul, Russia. (Gauslaa & McEvoy 2005). 402 THE LICHENOLOGIST Vol. 44 Some Teloschistaceae also have the ability 2006; Muggia et al. 2008; Vondra´k et al. to synthesize green or grey pigments of 2008; Xahidin et al. 2010). unknown structure, for example, ‘Lecidea- Although the absence of anthraquinones green’ (Wetmore 1996; Arup et al. 2007) or in Teloschistaceae has often been treated as ‘Sedifolia-grey’ (e.g., Wetmore 1996; Meyer an important grouping character, no studies & Printzen 2000), which may have the same to date have tested whether or not this function, that is, protection against UV radia- is a reliable character for classification, or tion (e.g., Hauck et al. 2007). These pigments whether species with such characters repre- usually occur in parts of the thalli or apo- sent a monophyletic group. The purpose of thecia where anthraquinones are absent, al- the present study is to test this hypothesis though both pigments may co-occur in the using a broad sampling of species lacking superficial tissues of the apothecia of some anthraquinones, which would traditionally species. These species, for example, Calo- be treated as closely related (e.g., Muggia placa conversa (Kremp.) Jatta, C. exsecuta et al. 2008). Specifically, we will test whether (Nyl.) Dalla Torre & Sarnth., C. oleicola (J. or not these species can be recovered as a Steiner) van den Boom & Breuss and C. well-supported monophyletic group. pollinii (A. Massal.) Jatta, may resemble those with an entire absence of anthraqui- nones, because their old apothecia turn Materials and Methods black as they contain large amounts of mela- nin pigments. In these cases, the anthraqui- Lichen samples were collected by the authors from vari- ous localities in the Northern Hemisphere. Detailed nones may be identified by the reactions of herbarium data for specimens used in our phylogenetic the apothecial sections (K+ strongly purple- studies are given in Table 1. Data for paratypes of C. violet, K ! HCl+ yellow, N+ orange, N ! neotaurica are abbreviated; full information for samples K+ purple-violet-blue, N ! K ! HCl+ yel- from CBFS is available at http://botanika.bf.jcu.cz/ low; Vondra´k et al. 2010a). lichenology/data.php. The absence of anthraquinones is known at various levels; their absence in the thallus Morphological examinations has arisen in many lineages throughout Telo- A detailed morphological description is given only for schistaceae, for example, the C. cerina group the new species. Measurements are accurate to 0Á25 mm (Sˇ oun et al. 2011). Occasional loss of anthra- for cells (e.g., conidia and ascospores), 1 mm for width quinones in the thallus is also documented of asci, or 10 mm for larger structures (e.g., hymenium, width of exciple). All measurements of cells (ascospores, in individuals or populations of species that conidia, asci, paraphyses) include their walls. Paraphyses usually have a pigmented thallus (Søchting tips were observed after treatment with c. 10% KOH. 1973; Vondra´k et al. 2010b). Aberrant popu- Only those ascospores with well-developed septa were lations lacking anthraquinones completely measured; in these ascospores, loculi were connected are suggested in C. tiroliensis Zahlbr. (Hansen with a thin cytoplasmatic channel, never disconnected. Measurements with more than ten repeats (n b 10) are et al. 1987; Søchting 1989) or C. xerica Poelt given as (min.-- ) x#eSD (-- max.), where x#¼ mean value &Veˇzda (Poelt 1975). and SD ¼ standard deviation. Morphological terminol- Species (or individuals) of Teloschistaceae ogy follows Smith et al. (2009). with a complete loss of yellow-orange-red pig- ments, sometimes grouped under Pyrenodes- Chemistry mia (Caloplaca variabilis group), have been The acetone extracts from apothecia were subjected studied since the 19th century but attempts to high-performance liquid chromatography (HPLC) to treat them systematically began with Mag- analysis. Reverse phase column (C18, 5 mm, Lichrocart nusson (1950), followed by Wunder (1974) 250-4) was eluted with MeOH / 30%MeOH+ in the Old World and Wetmore (1994) in 1%H3PO4 for 77 min and the absorbances at 270 nm North America. More recently, several works were recorded (for details see Søchting 1997). The compounds were determined on the basis of their reten- have dealt with this group using single locus tion times and absorption spectra. In the newly described (ITS) molecular data (Arup & Grube 1999; species, five specimens were examined (CBFS JV2048, Tretiach et al. 2003; Tretiach & Muggia 5925, 6023, 7094, 7105). 2012 Teloschistaceae without anthraquinones—Vondra´k et al. 403 Table 1. Sample data, engaging to groups and GenBank accession numbers of the ITS sequences newly generated for phylogenetic analyses. GenBank Species Specimen Group accession number Caloplaca Greece: Crete: Sternes, on calcareous stone, C. xerica group JN641762 albolutescens 2005, J. Vondra´k (CBFS JV4098) C. aractina Sweden: Bohusla¨n: Askum par., Barlindarna, C. haematites group JN641763 2006, U. Søchting 10579 (C) C. atroflava Czech Republic: North Moravia:Sˇ umperk, C. xerica group JN641764 Rasˇkov, on serpentinite, 2007, Palice 11741 (PRA) C. cerina, grey Greece: Astakos, on bark of Olea, 2010, C. cerina group JN641765 J. Vondra´k (CBFS JV8329) C. cerina, orange Greece: Astakos, on bark of Olea, 2010, C. cerina group JN641766 J. Vondra´k (CBFS JV8329) C. erythrocarpa Bulgaria: Strandzha Mts: Malko Tarnovo, on C. xerica group JN641767 limestone, 2005, J. Vondra´k (CBFS JV3208) C. fuscoatroides Bulgaria: Black Sea coast: Burgas, Sozopol, C. xerica group JN641768 2007, J. Vondra´k (CBFS JV6468) C. haematites
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