Robert Lücking

Towards a unified paradigm for sequence‐based identification of fungi

The nuclear ribosomal internal transcribed spacer (ITS) region is the formal fungal barcode and in most cases the marker of choice for the exploration of fungal diversity in environmental samples. Two problems are particularly acute in the pursuit of satisfactory taxonomic assignment of newly generated ITS sequences: (i) the lack of an inclusive, reliable public reference data set and (ii) the lack of means to refer to fungal species, for which no Latin name is available in a standardized stable way. Here, we report on progress in these regards through further development of the UNITE database (http://unite.ut.ee) for molecular identification of fungi. All fungal species represented by at least two ITS sequences in the international nucleotide sequence databases are now given a unique, stable name of the accession number type (e.g. Hymenoscyphus pseudoalbidus|GU586904|SH133781.05FU), and their taxonomic and ecological annotations were corrected as far as possible through a distributed, third‐party annotation effort. We introduce the term ‘species hypothesis’ (SH) for the taxa discovered in clustering on different similarity thresholds (97–99%). An automatically or manually designated sequence is chosen to represent each such SH. These reference sequences are released (http://unite.ut.ee/repository.php) for use by the scientific community in, for example, local sequence similarity searches and in the QIIME pipeline. The system and the data will be updated automatically as the number of public fungal ITS sequences grows. We invite everybody in the position to improve the annotation or metadata associated with their particular fungal lineages of expertise to do so through the new Web‐based sequence management system in UNITE.

Families of Dothideomycetes

Dothideomycetes comprise a highly diverse range of fungi characterized mainly by asci with two wall layers (bitunicate asci) and often with fissitunicate dehiscence. Many species are saprobes, with many asexual states comprising important plant pathogens. They are also endophytes, epiphytes, fungicolous, lichenized, or lichenicolous fungi. They occur in terrestrial, freshwater and marine habitats in almost every part of the world. We accept 105 families in Dothideomycetes with the new families Anteagloniaceae, Bambusicolaceae, Biatriosporaceae, Lichenoconiaceae, Muyocopronaceae, Paranectriellaceae, Roussoellaceae, Salsugineaceae, Seynesiopeltidaceae and Thyridariaceae introduced in this paper. Each family is provided with a description and notes, including asexual and asexual states, and if more than one genus is included, the type genus is also characterized. Each family is provided with at least one figure-plate, usually illustrating the type genus, a list of accepted genera, including asexual genera, and a key to these genera. A phylogenetic tree based on four gene combined analysis add support for 64 of the families and 22 orders, including the novel orders, Dyfrolomycetales, Lichenoconiales, Lichenotheliales, Monoblastiales, Natipusillales, Phaeotrichales and Strigulales. The paper is expected to provide a working document on Dothideomycetes which can be modified as new data comes to light. It is hoped that by illustrating types we provide stimulation and interest so that more work is carried out in this remarkable group of fungi.

Fungi evolved right on track.

Dating of fungal divergences with molecular clocks thus far has yielded highly inconsistent results. The origin of fungi was estimated at between 660 million and up to 2.15 billion y ago, and the divergence of the two major lineages of higher fungi, Ascomycota and Basidiomycota, at between 390 million y and up to 1.5 billion y ago. Assuming that these inconsistencies stem from various causes, we reassessed the systematic placement of the most important fungal fossil, Paleopyrenomycites, and recalibrated internally unconstrained, published molecular clock trees by applying uniform calibration points. As a result the origin of fungi was re-estimated at between 760 million and 1.06 billion y ago and the origin of the Ascomycota at 500–650 million y ago. These dates are much more consistent than previous estimates, even if based on the same phylogenies and molecular clock trees, and they are also much better in line with the fossil record of fungi and plants and the ecological interdependence between filamentous fungi and land plants. Our results do not provide evidence to suggest the existence of ancient protolichens as an alternative to explain the ecology of early terrestrial fungi in the absence of land plants.

Naming and outline of Dothideomycetes-2014 including proposals for the protection or suppression of generic names

Article 59.1, of the International Code of Nomenclature for Algae, Fungi, and Plants (ICN; Melbourne Code), which addresses the nomenclature of pleomorphic fungi, became effective from 30 July 2011. Since that date, each fungal species can have one nomenclaturally correct name in a particular classification. All other previously used names for this species will be considered as synonyms. The older generic epithet takes priority over the younger name. Any widely used younger names proposed for use, must comply with Art. 57.2 and their usage should be approved by the Nomenclature Committee for Fungi (NCF). In this paper, we list all genera currently accepted by us in Dothideomycetes (belonging to 23 orders and 110 families), including pleomorphic and non-pleomorphic genera. In the case of pleomorphic genera, we follow the rulings of the current ICN and propose single generic names for future usage. The taxonomic placements of 1261 genera are listed as an outline. Protected names and suppressed names for 34 pleomorphic genera are listed separately. Notes and justifications are provided for possible proposed names after the list of genera. Notes are also provided on recent advances in our understanding of asexual and sexual morph linkages in Dothideomycetes. A phylogenetic tree based on four gene analyses supported 23 orders and 75 families, while 35 families still lack molecular data.

A world-wide key to the genus Graphis ( Ostropales : Graphidaceae )

A world-wide key to the genus Graphis is presented, based on extensive type studies and revision of several thousand historical and recent collections. A total of 330 species are accepted and included in the key, and a further 205 epithets are listed as synonyms. The structured key includes taxonomic information on type specimens of epithets considered to be synonyms of the accepted species. In addition, 28 species of other genera ( Carbacanthographis, Diorygma, Dyplolabia, Glyphis ) with carbonized excipulum and hyaline ascospores likely to be confused with Graphis are mentioned under the corresponding key couplets. Although the key is preliminary and some taxonomic and nomenclatural problems remain unresolved at this time, it should allow reliable identification of most specimens especially from tropical regions. The following 14 species are described as new: Graphis brahmanensis Aptroot sp. nov., G. cupei Vain. ex Lucking sp. nov., G. funilina Aptroot sp. nov., G. inspersolongula Aptroot sp. nov., G. leucaenae Aptroot sp. nov., G. lourdesina Aptroot sp. nov., G. myolensis Aptroot sp. nov., G. nadurina Aptroot sp. nov., G. norstictica Archer & Lucking sp. nov., G. sarawakensis Hale ex Lucking sp. nov., G. slendrae Hale ex Lucking sp. nov., G. subintermedians Hale ex Lucking sp. nov., G. subserpens Staiger sp. nov., and G. syzygii Aptroot sp. nov. In addition, 22 new combinations are proposed: Carbacanthographis cleitops (Fee) Lucking comb. nov., C. coccospora (Aptroot) Aptroot & Lucking comb. nov., C. induta (Mull. Arg.) Lucking comb. nov., C. triphoroides (M. Wirth & Hale) Lucking comb. nov., Graphis apoda (Zahlbr.) Lucking comb. et stat. nov., G. cremicolor (H. Magn.) Lucking & Archer comb. nov., G. enteroleuca (Ach.) Lucking comb. nov., G. evirescens (Redinger) Lucking comb. nov., G. galactoderma (Zahlbr.) Lucking comb. nov., G. ingarum (Vain.) Lucking comb. et stat. nov., G. isidiata (Hale) Lucking comb. nov., G. japonica (Mull. Arg.) A. W. Archer & Lucking comb. nov., G. kousyuensis (Horik. & M. Nakan.) Lucking comb. nov., G. negrosina (Vain.) Lucking comb. et stat. nov., G. oxyspora (Zahlbr.) Lucking comb. nov., G. plumbea (Zahlbr.) Lucking comb. nov., G. riopiedrensis (Fink) Lucking comb. nov., G. semirigida (Mull. Arg.) Lucking comb. nov., G. subradiata (Nyl.) Lucking comb. et stat. nov., G. subtecta (Nyl.) Lucking comb. et stat. nov., and G. sulphurella (Zahlbr.) Lucking comb. nov. Replacement names are established for six taxa: Graphis jeanmuelleri Lucking nom. nov. [≡ Graphina elegantula Mull. Arg., non Graphis elegantula Zahlbr.], Graphis neoelongata Lucking nom. nov. [≡ G. elongata Vain., non G. elongata Zenker], Graphis novopalmicola A. W. Archer & Lucking nom. nov. [≡ Graphina palmicola Mull. Arg., non Graphis palmicola Makhija & Adaw.], Graphis paralleloides Caceres & Lucking nom. nov. [≡ G. rimulosa var. parallela Mull. Arg., non G. parallela Mull. Arg.], Graphis subalbostriata Lucking nom. nov. [≡ G. angustata var. albostriata Vain., non G. albostriata Vain.], and Graphis subvernicosa Lucking nom. nov. [≡ Opegrapha vernicosa Fee, non G. vernicosa Nyl.]. Three new synonyms are established for Glyphis substriatula (Nyl.) Staiger: Graphina sulcatula Mull. Arg., G. sulcatula var. conglomerata Mull. Arg., and G. bakeri Zahlbr.

A new classification for the family Graphidaceae (Ascomycota: Lecanoromycetes: Ostropales)

A revised classification for the emended family Graphidaceae is proposed, based on recent phylogenetic studies, including the finding that three previously separated families (Asterothyriaceae, Gomphillaceae, Thelotremataceae) are nested within Graphidaceae and in part polyphyletic. The family comprises three major clades which are here delimited as subfamilies Fissurinoideae, Gomphilloideae, and Graphidoideae. The latter is composed of three major clades which are formally delimited as tribes Graphideae, Ocellularieae, and Thelotremateae. In addition, three new genera are described to accommodate the Ocellularia clandestina (Clandestinotrema) group, the Ocellularia cruentata group (Cruentotrema) and Myriotrema pycnoporellum (Pycnotrema). Keys are provided for the species placed in the new genera.

Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota)

The Verrucariaceae (Ascomycota) is a family of mostly lichenized fungi with a unique diversity of algal symbionts, including some algae that are rarely or never associated with other lichens. The phylogenetic position of most of these algae has not yet been studied and, because morphology-based identifications can often be misleading, molecular data is necessary to revisit their identity and to explore patterns of association between fungal and algal partners. For this reason, the diversity of photobionts in this lichen family was investigated using molecular markers (rbcL and nuSSU) amplified from DNA extracts of lichen thalli and cultured isolates. Although a single algal genus, Diplosphaera (Trebouxiophyceae), was associated with 12 out of the 17 sampled genera of Verrucariaceae, representatives of eight other genera in five orders of the Chlorophyta and one genus in the Xanthophyceae also form lichen associations with members of the family. Fungal genera with simple crustose thalli (e.g. Hydropunctaria, Wahlenbergiella, Bagliettoa) use a high diversity and unusual selection of photobionts. In contrast, fungal genera with more complex thalli (e.g. Placidium, Dermatocarpon) tend to have lower photobiont diversity. Habitat requirements and phylogenetic histories are both partly reflected in the observed patterns of associations between lichenized fungi from the family Verrucariaceae and their photobionts.

A single macrolichen constitutes hundreds of unrecognized species

Significance Macrolichens are considered to be well known, including the tropical montane basidiolichen fungus Dictyonema glabratum, also known as Cora pavonia, an important component of threatened paramo ecosystems, where it acts as a biological fertilizer due to its ability to fix atmospheric nitrogen. This lichen was long believed to represent a single species, but after revising this number to 16 in two genera (Cora and Corella), here we show that at least 126 phylogenetically and morphologically distinct species are contained within this group, with statistical analysis predicting more than 400. Our findings underline the importance of accurately documenting species richness for conservation purposes and support the notion of neotropical paramos as hotspots of recent diversification in plants, animals, and fungi. The number of Fungi is estimated at between 1.5 and 3 million. Lichenized species are thought to make up a comparatively small portion of this figure, with unrecognized species richness hidden among little-studied, tropical microlichens. Recent findings, however, suggest that some macrolichens contain a large number of unrecognized taxa, increasing known species richness by an order of magnitude or more. Here we report the existence of at least 126 species in what until recently was believed to be a single taxon: the basidiolichen fungus Dictyonema glabratum, also known as Cora pavonia. Notably, these species are not cryptic but morphologically distinct. A predictive model suggests an even larger number, with more than 400 species. These results call into question species concepts in presumably well-known macrolichens and demonstrate the need for accurately documenting such species richness, given the importance of these lichens in endangered ecosystems such as paramos and the alarming potential for species losses throughout the tropics.

A world-wide key to the thelotremoid Graphidaceae , excluding the Ocellularia - Myriotrema - Stegobolus clade

In the course of an ongoing systematic and taxonomic revision of the lichen family Graphidaceae (including Thelotremataceae ), we present world-wide keys to the currently accepted thelotremoid genera and species, excluding the columellate taxa and their relatives of the Ocellularia - Myriotrema - Stegobolus clade ( Melanotrema , Myriotrema , Ocellularia , Ocellularia clandestina group, Redingeria , Stegobolus ), which will be treated in a forthcoming paper. The keys include all genera and species with chroodiscoid, lepadinoid, and topeliopsidoid apothecia and other taxa featuring periphysoids or fibrils, and their relatives. Taxa keyed out to genus and species level are Acanthotrema , Chapsa , Chroodiscus , Diploschistes , Fibrillithecis , Gyrotrema , Leptotrema , Leucodecton , Melanotopelia , the ‘ Ocellularia ’ cruentata group, Pseudoramonia , Reimnitzia , Schizotrema , Thelotrema , Topeliopsis and Wirthiotrema . Over 260 species are treated, including a few yet unnamed taxa. The following taxonomic and nomenclatural novelties are introduced: Acanthotrema frischii Lucking sp. nov., Chapsa aggregata (Hale) Sipman & Lucking comb. nov., C. albida (Nyl.) Lucking & Sipman comb. nov.; C. albomaculata (Sipman) Sipman & Lucking comb. nov., C. boninensis (Tat. Matsumoto) Rivas Plata & Mangold comb. nov., C. elabens (Mull. Arg.) Rivas Plata & Mangold comb. nov., C. imperfecta (Hale) Rivas Plata & Lucking comb. nov., C. laceratula (Mull. Arg.) Rivas Plata & Lucking comb. nov., C. magnifica (Berk. & Broome) Rivas Plata & Lucking comb. nov., C. meghalayensis (Patw. & Nagarkar) Lumbsch & Divakar comb. nov., C. meridensis (Kalb & Frisch) Lucking, Lumbsch & Rivas Plata comb. nov., C. mirabilis (Zahlbr.) Lucking comb. nov., C. neei (Hale) Mangold & Lucking comb. nov., C. paralbida (Riddle) Rivas Plata & Lucking comb. nov., C. pseudoexanthismocarpa (Patw. & C. R. Kulk.) Rivas Plata & Lucking comb. nov., C. pulvereodisca (Hale) Rivas Plata & Mangold comb. nov., C. scabiomarginata (Hale) Rivas Plata & Lucking comb. nov., C. waasii (Hale) Sipman & Lucking comb. nov., Fibrillithecis argentea (Mull. Arg.) Rivas Plata & Lucking comb. nov., F. carneodisca (Hale) Rivas Plata & Lucking comb. nov., F. confusa Lucking, Kalb & Rivas Plata spec. nov., F. diminita (Hale) Rivas Plata & Lucking comb. nov., F. eximia (R. C. Harris) Rivas Plata & Lucking comb. nov., F. fissurata (Nagarkar & Hale) Rivas Plata & Lucking comb. nov., F. gibbosa (H. Magn.) Rivas Plata & Lucking comb. nov., Leucodecton desquamescens (Vain.) Lucking comb. nov., L. oxysporum (Redinger) Lucking comb. nov., Schizotrema cryptotrema (Nyl.) Rivas Plata & Mangold comb. nov., Thelotrema patwardhanii (Hale) Rivas Plata & Mangold comb. nov., Topeliopsis guaiquinimae (Sipman) Rivas Plata & Mangold comb. nov., and T. tuberculifera (Vain.) Rivas Plata & Mangold comb. nov. Using the examples of Fibrillithecis halei s. lat., Leucodecton compunctellum s. lat., and Thelotrema monosporum s. lat., we show how difficult species complexes can be flexibly treated in a key, allowing for either a broad concept or the distinction of several individual taxa.

A First Assessment of the Ticolichen Biodiversity Inventory in Costa Rica: The Genus Graphis, with Notes on the Genus Hemithecium (Ascomycota: Ostropales: Graphidaceae)

Abstract The genus Graphis sensu Staiger is treated as a further contribution to the TICOLICHEN biodiversity inventory in Costa Rica. Graphis s.str. is the largest tropical lichen genus, with more than 300 accepted species worldwide, and also the largest in Costa Rica, with a total of 115 species recognized in this work. The following 25 species are described as new: Graphis altamirensis Sipman & Lücking sp. nov., G. argentata Lücking & Umaña sp. nov., G. bettinae Lücking, Umaña, Chaves & Sipman sp. nov., G. duplicatoinspersa Lücking sp. nov., G. firferi Lücking sp. nov., G. flavoaltamirensis Sipman & Lücking sp. nov., G. flavominiata Moncada & Lücking sp. nov., G. fournierii Lizano & Lücking sp. nov., G. gomezii Lücking, Will-Wolf & Umaña, G. gregmuelleri Sipman & Lücking, sp. nov., G. hypocrellina Lücking & Chaves sp. nov., G. inspersostictica Sipman & Lücking sp. nov., G. litoralis Lücking, Sipman & Chaves sp. nov., G. mirabilis Lücking, Sipman, Umaña & Chaves sp. nov., G. nudaeformis Lücking sp. nov., G. oryzaecarpa Lücking sp. nov., G. paradisserpens Sipman & Lücking sp. nov., G. paraserpens Lizano & Lücking sp. nov., G. pittieri Lücking, Umaña, Sipman & Chaves sp. nov., G. pseudocinerea Lücking & Umaña sp. nov., G. pseudoserpens Chaves & Lücking sp. nov., G. subflexibilis Lücking & Chaves sp. nov., G. subruiziana Sipman, Chaves & Lücking sp. nov., G. subturgidula Lücking & Sipman sp. nov., and G. tenoriensis Chaves & Lücking sp. nov. Graphis immersoides Lücking, nom. nov. [Bas. Graphina immersa Müll. Arg.; non Graphis immersa Fink], Graphis subchrysocarpa Lücking, nom. nov. [Bas.: Phaeographina ochracea C. W. Dodge; non Graphis ochracea Hepp], and Graphis submarginata Lücking, nom. nov. [Bas. Graphis marginata G. Mey. & Flot.; non Graphis marginata Raddi] are introduced as replacement names. Furthermore, 17 new combinations are proposed: G. bipartita (Müll. Arg.) Lücking, comb. nov., G. chondroplaca (Redinger) Lücking comb. et stat. nov., G. consanguinea (Müll. Arg.) Lücking, comb. nov., G. dichotoma (Müll. Arg.) Lücking, comb. nov., G. granulosa (Müll. Arg.) Lücking comb. nov., G. insulana (Fée) Lücking & Sipman, comb. nov., G. lutea (Chevall.) Aptroot, comb. nov., G. multisulcata (Müll. Arg.) Lücking & Chaves comb. nov., G. myrtacea (Müll. Arg.) Lücking, comb. nov., G. nuda (H. Magn.) Staiger & Lücking, comb. nov., G. plurispora (Redinger) Lücking & Chaves, comb. nov., G. puiggarii (Müll. Arg.) Lücking, comb. nov., G. rhizocola (Fée) Lücking & Chaves, comb. nov. [syn. G. anguilliformis Taylor; G. serpens Fée], G. subcontorta (Müll. Arg.) Lücking & Chaves, comb. nov., G. subhiascens (Müll. Arg.) Lücking comb. nov., G. xylophaga (R. C. Harris) Lücking, comb. nov., and Hemithecium plicosum (Meissn.) Lücking & Aptroot, comb. nov. [syn. Graphina malmei Redinger]. The new name Pallidogramme Staiger, Kalb & Lücking, nom. nov. is introduced for Leucogramma A. Massal. [nom. illeg.;  =  Hemithecium subgen. Leucogramma Staiger], comprising a group of three species formerly included in Hemithecium: Pallidogramme chapadana (Redinger) Staiger, Kalb & Lücking, comb. nov., P. chlorocarpoides (Nyl.) Staiger, Kalb & Lücking, comb. nov., and P. chrysenteron (Mont.) Staiger, Kalb & Lücking, comb. nov. More than 600 types of Graphidaceae suspected to represent species of Graphis s.str. were examined for this study, and notes on type material are given when appropriate. Also, the names previously reported for Costa Rica by the Swiss lichenologist Müller Argoviensis in 1891 and 1893 were checked when possible, and 175 unpublished collections from Costa Rica housed at the Farlow Herbarium (fh) of Harvard University and collected and identified by Carroll William Dodge and colleagues and students were revised. A key is presented to all species, including an image-based identification guide, and diagnostic characters in the genus Graphis are briefly discussed and illustrated. Diagnoses and remarks are given for all species treated here, as are more detailed descriptions for the taxa new to science. Data from 803 collections were analyzed using the ordination technique of principal component analysis to display habitat and microhabitat preferences for species groups.