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1 Departamento de Ingeniería y Ciencia de los Materiales, Escuela
Técnica Superior de Ingenieros Industriales, Universidad
Politécnica de Madrid (UPM), José Gutiérrez Abascal 2,
28006 Madrid, Spain
2 CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht,
Netherlands
3 DECOS, Università degli Studi della Tuscia, Largo
dell'Università, Viterbo, Italy
4 Free University of Berlin and Federal Institute for Materials Research and
Testing (BAM), Department IV "Materials and Environment", Unter
den Eichen 87, 12205 Berlin, Germany
5 Institute für Pflanzenwissenschaften, Karl-Franzens-Universität
Graz, Holteigasse 6, A-8010 Graz, Austria
6 NCBI/NLM/NIH, 45 Center Drive, Bethesda MD 20892, U.S.A.
7 Department of Microbiology, University of Washington, Box 357242, Seattle
WA 98195, U.S.A.
8 Department of Biology, Duke University, Box 90338, Durham NC 27708,
U.S.A.
*
Correspondence: Constantino Ruibal,
tinoruibal{at}yahoo.com
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Abstract |
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 TOP Abstract INTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONReferences |
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Keywords Arthoniomycetes / Capnodiales / Dothideomycetes / evolution / extremotolerance / multigene phylogeny / rock-inhabiting fungi
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INTRODUCTION |
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TOPAbstractINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONReferences |
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Rock-inhabiting fungi (RIF) are peculiar organisms that apparently lack sexual reproductive structures and form compact, melanised colonies on bare rock surfaces (Fig. 1). Although very common, RIF have often been overlooked due to their small size, their slow growth and the lack of diagnostic features. First discovered in hot and cold deserts (Krumbein & Jens 1981, Friedmann 1982, Staley et al. 1982), RIF are now known to be ubiquitous on hard surfaces, in extreme as well as in temperate climates (Urzì et al. 1995, Sterflinger & Prillinger 2001, Gorbushina 2007, Gorbushina & Broughton 2009). RIF are well adapted to nutrient-poor and dry habitats where they are particularly successful colonisers due to restricted competition with other microbes (Gorbushina 2007) and their extremotolerance.
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Sterflinger et al. (1997) provided the first molecular evidence of RIF phylogenetic affiliations, and they are known to belong to two groups of ascomycetes, namely Dothideomycetes and Eurotiomycetes (de Hoog et al. 1999, Sterflinger et al. 1999, Ruibal 2004, Ruibal et al. 2005, 2008, Sert et al. 2007a). In Eurotiomycetes, multigene phylogenetic analyses have shown that RIF cluster in early diverging lineages of Chaetothyriales, whereas two species seem to be more closely related to the lichenised order Verrucariales, the sister group of Chaetothyriales (Gueidan et al. 2008). Gueidan et al. (2008) also demonstrated that the most recent common ancestor of both lichenised Verrucariales and pathogen-rich Chaetothyriales was probably a rock-inhabiting fungus. It was hypothesised that adaptations to life in extreme conditions might have been a prerequisite for the evolution of human pathogenicity (de Hoog 1993, Haase et al. 1999, Gueidan et al. 2008) and lichenisation in this class (Gueidan et al. 2008). In contrast, despite the high diversity of RIF within Dothideomycetes, only very few human pathogens are known from this class of Ascomycota (de Hoog et al. 2000). Alternatively, associations with plants and in particular plant pathogenicity are very common (Schoch et al. 2006, Arzanlou et al. 2007, Crous et al. 2007a, b, c, 2009; this volume). Additionally, lichenised species also appeared to be nested within Dothideomycetes (Lutzoni et al. 2004, James et al. 2006, Del Prado et al. 2006, Muggia et al. 2008, Nelsen et al. 2009). Presently no strong phylogenetic hypothesis is available to assess the placement of RIF within Dothideomycetes. Moreover, no studies have investigated phylogenetic relationships among RIF, lichenforming fungi and plant-associated fungi within Dothideomycetes. Our main goal was to infer phylogenetic relationships of RIF within Dothideomyceta, a lineage including Dothideomycetes and Arthoniomycetes, to explore more specifically their diversity, origins and evolution.
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MATERIAL AND METHODS |
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TOPAbstractINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONReferences |
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DNA isolation and sequencing
Different laboratories contributed data using various protocols, but most
DNA sequence information was produced as follows: genomic DNA was isolated
from cultures grown on MEA. Fungal biomass was transferred to a tube with 500
µL of TES buffer and ground with a micro-pestle for 1–2 min, with or
without silica-mix (2/3 silica-gel, 1/3 Celite® 545). A volume of 140
µL of 5 M NaCl was then added, followed by 65 µL of 10 % (w/v) CTAB
(cetyltrimethylammoniumbromid). After an incubation of 30 min at 65 °C,
700 µL of (24:1) chloroform/isoamylalcohol was added, the tubes were mixed
carefully by hand, stored on icy water for 30 min, and centrifuged for 10 min
at 4 °C (10 000 x g). The supernatant was recovered and the genomic DNA
precipitated using isopropanol. After washing the pellets with 70 % ethanol,
they were dried in a vacuum centrifuge and re-suspended in 60 µL of TE
buffer (protocol modified from Möller
et al. 1992).
Six regions covering five genes were amplified: nucLSU, nucSSU, mtSSU, RPB1 region A–D, RPB2 region 5–7, and RPB2 region 7–11 (see table 2 for primers used). Genomic DNA (1 µL of a 1/10 or 1/100 dilution) was added to a PCR mix comprising 2.5 µL of PCR buffer (buffer IV with 15 mM MgCl2, Abgene, Epsom, U.K.), 2.5 µL of dNTPs (2 mM), 2.5 µL of BSA (10 mg/mL), 2.0 µL of primers (10 µM), 0.15 µL Taq polymerase (5 U/µL, Denville, Metuchen NJ, U.S.A.), and water for a total volume of 25 µL. Amplification cycles for nucLSU, nucSSU and RPB1 (same conditions applied for RPB2) are described in Gueidan et al. (2007), and in Zoller et al. (1999) for mtSSU. The PCR products were purified using Microcon PCR cleaning kits (Millipore, Billerica MA, U.S.A.). Sequencing was carried out using Big Dye Terminator Cycle sequencing Kits (ABI PRISM version 3.1, Perkin-Elmer, Applied Biosystems) on ABI 3730xl DNA Analyzers (Applied Biosystems, Foster City CA, U.S.A.) from the Duke Center for Evolutionary Genomics (Durham NC, U.S.A.) and the Hubrecht Institute (Utrecht, Netherlands).
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Alignments and phylogenetic analyses
Sequences were assembled and edited using Sequencher (Gene Codes
Corporation, Ann Arbor MI, U.S.A.). Manual alignments were performed using
MacClade v. 4.08 (Maddison & Maddison
2003). Ambiguous regions (sensu
Lutzoni et al. 2000)
and introns were delimited manually and excluded from the alignments.
Congruence was tested using a 70 % reciprocal bootstrap criterion
(Mason-Gamer & Kellogg
1996, Reeb et al.
2004). For the three-gene dataset, the test was performed using
Compat (Kauff & Lutzoni
2002) on all possible gene pairs (mtSSU vs. nucSSU, mtSSU vs.
nucLSU, and nucLSU vs. nucSSU) and based on bootstrap consensus trees.
Bootstrap trees were obtained using Neighbor-Joining bootstrap analyses with
Maximum Likelihood distances in PAUP v. 4.0b10
(Swofford 2003). Models of
molecular evolution were estimated using the Akaike Information Criterion
implemented in Modeltest v. 3.7 (Posada
& Crandall 1998). For the five-gene dataset, congruence was
also tested using a 70 % reciprocal bootstrap criterion, but the comparison
was done manually based on trees obtained with 500 bootstrap replicates using
RAxML VI-HPC (Stamatakis et al.
2005,
2008) on the Cipres Web Portal
(www.phylo.org/sub_sections/portal/).
Taxa or sequences responsible for incongruence were removed from the dataset,
and the markers were combined. Final phylogenetic analyses of the three-gene
and five-gene datasets were performed using RAxML on the Cipres Web Portal.
The ML search followed a GTRMIX model of molecular evolution applied to the
following nine partitions: RPB1 first, second and third codon
positions, RPB2 first, second and third codon positions, nucLSU,
nucSSU and mtSSU. Support values were obtained with bootstrap analyses of 1
000 pseudoreplicates using RAxML.
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RESULTS |
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TOPAbstractINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONReferences |
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Phylogenetic inference
For the three-gene analysis (Figs
2,
3), results show that, within
the two classes Dothideomycetes and Arthoniomycetes,
rock-inhabiting fungi belong to 13 groups, either well-known orders or
families, or lineages that have not previously been characterised. Among the
rock-inhabiting fungi clustering with well-known groups of
Dothideomycetes, two strains are found in the order
Dothideales, four in the order Pleosporales, one in
Myriangiales, 12 forming a monophyletic group sister to the remaining
members of Davidiellaceae, and one in the family
Capnodiaceae. The family Teratosphaeriaceae is not
monophyletic in this analysis (also see
Crous et al. 2009;
this volume). In a first group including the generic type Teratosphaeria
fibrillosa (Teratosphaeriaceae 1,
Fig. 3), many rock-inhabiting
strains are present, including taxa from the three genera
Friedmanniomyces, Elasticomyces and Recurvomyces. The second
group (Teratosphaeriaceae 2, Fig.
3), including the three leaf-colonising species Devriesia
strelitziae, Mycosphaerella eurypotami and Tripospermum myrti,
an unknown species of Capnodiales, the lichen species Cystocoleus
ebeneus as well as 20 undescribed rock inhabiting strains, is supported
as sister to the family Mycosphaerellaceae (91 % bootstrap). The two
rock-inhabiting species Coniosporium uncinatum and C.
apollinis are well supported (100 % bootstrap), but their sister
relationship is not. Neither these two species of Coniosporium nor
the Antarctic genus Cryomyces can be assigned to any known family or
order sampled here. Amongst the unknown lineages, one does not seem to be part
of Dothideomycetes (lineage 1,
Fig. 2), and appears as sister
to Arthoniomycetes (98 % bootstrap). Due to the lack of support for
many deep internodes, it is not possible to determine if lineages 2 and 3 can
be accommodated by the expansion of known groups of Dothideomycetes,
or if the recognition of new taxonomical entities are needed. Finally, the
rock isolates A6, AN13, TRN 437 and CCFEE 5413 do not significantly cluster
with any other taxa.
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DISCUSSION |
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TOPAbstractINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONReferences |
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Classification of rock fungi related to Dothideomycetes
Although very diverse within Dothideomycetes, RIF have not been
included in recent phylogenetic studies of this class
(Lumbsch et al. 2001,
Schoch et al. 2006).
Only very few of these rock-inhabiting species have been taxonomically
described (Sterflinger et al.
1997, Bills et al.
2005, Sert et al.
2007b), and the molecular marker available for most of these
species (ITS) does not allow their inclusion in large-scale phylogenetic
analyses. The few attempts to produce phylogenies involving RIF have shown
that they belong to two diverse classes of Ascomycota, namely
Eurotiomycetes (particularly the order Chaetothyriales) and
Dothideomycetes (preponderantly the orders Capnodiales,
Dothideales and Pleosporales)
(Sterflinger et al.
1999, Ruibal 2004,
Ruibal et al. 2005,
2008).
Our results confirm the placement of RIF in the same orders of Dothideomycetes, although some lineages are shown to belong to additional groups. Based on our results, many RIF should be classified within Dothideales, Pleosporales and Capnodiales, the latter order holding the largest number in rock-colonising species. The genera Elasticomyces and Recurvomyces, as well as the Antarctic genus Friedmanniomyces, were previously attributed to Capnodiales based on nucSSU data (Selbmann et al. 2008). Our multigene analyses confirm this placement, and show that these three genera belong to Teratosphaeriaceae s. str., the family currently showing the highest diversity in RIF (Fig. 3). We also showed that one RIF (TRN 235) previously thought to be related to the Dothideales (Ruibal et al. 2008) actually belongs to Myriangiales, along with Sarcinomyces crustaceus, a species similarly melanised and meristematic, but isolated from plant material (Sigler et al. 1981).
Several well-supported groups of RIF could not be attributed to any known families and orders according to our data. As a consequence, Cryomyces should still be considered as Dothideomycetes incertae sedis, as no close relationship was recovered for this enigmatic Antarctic genus (Selbmann et al. 2005). The positions of RIF-rich genera Coniosporium and Sarcinomyces are also problematic. Previous studies placed them either in Dothideales or Chaetothyriales based on ITS or nucSSU data (de Leo et al. 1999, Sterflinger et al. 1999, Sert et al. 2007a). Yet, the limited taxon and gene sampling on which these analyses were based was probably insufficient to demonstrate clear phylogenetic relationships. Our results show that Coniosporium apollinis (including the type strain CBS 352.97), C. uncinatum (including the type strain CBS 100219) and Sarcinomyces crustaceus belong to Dothideomyceta (Fig. 4). However, a previous multigene analysis showed that two other species, Coniosporium perforans and Sarcinomyces petricola, belong to Chaetothyriales (Gueidan et al. 2008). These anamorphic genera are therefore not monophyletic, and additional research is required to clarify their status.
Among lineages lacking known reference taxa, two groups seem to belong to Dothideomycetes (unknown group 2, a lineage comprising RIF from the Alps, and unknown group 3, a lineage including strains isolated in Arizona; Fig. 2). Another unknown group (lineage 1) clusters outside Dothideomycetes, sister to the Arthoniales (Figs 2, 4). A previous study had noted the problematic placement of this latter group (Ruibal et al. 2008). Many lineages including RIF still need to be named. In the past, several melanised meristematic species and genera have been described such as Lichenothelia (Hawksworth 1981; see also Henssen 1987), which could potentially correspond to some of these RIF lineages. However, little is known about these formerly named taxa, and no molecular data or cultures are available for many of them. Naming RIF will therefore require an extensive study of both rock-inhabiting species and formerly described melanised meristematic species, whether they grow on rock or not.
Rock surfaces: "terroirs" for ancient lineages or reservoirs for plant-associated fungi?
Despite the prevailing extreme conditions, rock surfaces host a large
variety of specialised fungi. Fungal colonisation of subaerial rocks can be
explained by two non-exclusive hypotheses. Firstly, atmosphere-exposed rock
substrates could constitute "terroirs" for ancient fungal
lineages. Rock surfaces were among the first terrestrial substrates available
for living organisms on earth (Gorbushina
& Broughton 2009). It is therefore likely that, early on, some
species became adapted to colonise rock surfaces. RIF are persistent to
different types of physical stress, but are poor competitors and surrender to
more combative organisms (Gorbushina
et al. 2008). Increasing competition with other
rock-inhabiting organisms living under more permissive conditions may have
restricted some of these ancient, morphologically reduced, slow-growing,
fungal relicts to extreme habitats. The presence of lineages comprising
exclusively RIF that diverged early in the evolution of Dothideomyceta
(e.g., Cryomyces and lineage 1,
Fig. 2) supports this
hypothesis of rock surfaces as substrates for ancient fungal lineages.
Secondly, rock surfaces could form reservoirs for plant-associated or saprobic fungi. Through spore or propagule dispersal, some species of various unrelated groups of plant pathogens, epiphytes or saprobes can reach rock substrates. Their ability to survive in these environments will depend on some key features, namely oligotrophy, melanisation and pleiomorphism (or diversity of growth forms, amongst which meristematic growth). Under extreme conditions prevailing on rock surfaces, fungi possessing these key features can survive due to their slow, meristematic, clumpy growth and thick-walled, heavily melanised cells. These key features seem to have evolved several times in Dothideomycetes, allowing different lineages to colonise rock substrates. In Dothideales, phyllosphere fungi such as Aureobasidium pullulans and relatives, which have a filamentous or yeast-like growth under moist conditions, but convert to a meristematic form when colonising inert substrates, have also been isolated from rock surfaces (Ruibal et al. 2008). The family Teratosphaeriaceae s. l. is another example of a group in which some leaf-colonising species can also grow meristematically and form dark, thick-walled cells. According to our results, this family (as traditionally delimited; i.e., including Teratosphaeriaceae 1 and 2) is also extremely diverse in RIF (Fig. 3). Rocks supporting growth of subaerial biofilms (Gorbushina & Broughton, 2009) may be viewed as a reservoir for all types of melanised meristematic fungi, from where other habitats can be re-colonised. Survival of new comers is probably additionally facilitated by the existing microbial community on rocks (Gorbushina & Broughton 2009) in a fashion known for immigrant bacteria on leaf surfaces (Monier & Lindow 2005).
Alternatively, rock-colonising lichens may supply buffered environments and refugia for RIF or organisms otherwise occupying other niches (Selbmann et al. 2010). Recent studies have shown that lichens harbour an amazing diversity of ascomycetous endophyte-like (endolichenic) fungi (Arnold et al. 2009), and phylogenetic relatedness was found between some endolichenic fungi isolated from saxicolous lichens and RIF (Harutyunyan et al. 2008). If in most cases, species from rock surfaces can still go back to their primary habitats, in some cases, these fungi keep specialising and get trapped in these extreme habitats. This may be the case for groups with no close relationships with plant-associated fungi, such as the genus Friedmanniomyces (Fig. 3).
Geographical distribution of rock-inhabiting fungi
The large majority of rock-inhabiting strains isolated thus far originated
from rocks in the Mediterranean region or Antarctica
(Sterflinger et al.
1999, Ruibal 2004,
Ruibal et al. 2005,
2008 Selbmann et al.
2005,
2008). In Antarctica, RIF tend
to grow within rocks, together with the cryptoendolithic lichen communities,
finding shelter from extreme conditions prevailing on rock surfaces. In the
Mediterranean area, RIF tend to grow on the rock surface or in cracks, causing
damages to the substrate (e.g., biopitting of marble). Despite
differences in temperature, they share similar morphological and physiological
adaptations, such as melanisation, meristematic growth and oligotrophism.
Similarly to previous studies (Selbmann et al. 2005, Ruibal et al. 2008), our results show that Antarctic RIF often share an evolutionary history with RIF from semi-arid areas. In our study, RIF sampled in geographically disjoint localities (Antarctica versus Mediterranean region) cluster together in Davidiellaceae, the two groups of Teratosphaeriaceae, and unknown lineage 1 (Figs 2, 3). In some cases, Antarctic and Mediterranean strains are even phylogenetically very closely related, showing a recent common evolutionary history (e.g., in Teratosphaeriaceae 2, the Mediterranean rock isolates TRN 124 and A73 with the Antarctic strain CCFEE 5489). Likewise, some strains of Recurvomyces mirabilis and Elasticomyces elasticus have been recorded in the Antarctic as well as in high peaks of the Alps and Andes (Selbmann et al. 2008). Therefore, it seems that an efficient mechanism of dispersal, most probably wind-mediated (Gorbushina et al. 2007, Gorbushina & Broughton 2009), have led to a colonisation spanning different continents.
Rock-dwelling habit and evolution of lichenisation
Most of the diversity in lichen-forming fungi is found in
Lecanoromycetes, a large and diverse class of ascomycetes including
approximately 14 000 species (Miadlikowska
et al. 2006, Kirk
et al. 2008). Yet, the classes Lichinomycetes
(with the single order Lichinales), Eurotiomycetes (with the
orders Pyrenulales and Verrucariales),
Arthoniomycetes (with the single order Arthoniales), and
Dothideomycetes also include lichens. Although Lichinales,
Pyrenulales, Verrucariales and Arthoniales are monophyletic
lineages containing mostly lichenised species, lichens in
Dothideomycetes seem to encompass a broader phylogenetic spectrum:
the Trypetheliaceae, a family of mostly tropical bark-colonising
lichens, forms a monophyletic group within Dothideomycetes
(Del Prado et al.
2006, Nelsen et al.
2009, Schoch et al.
2009a). Arthopyrenia salicis, a corticolous, temperate
lichen species nests within the order Pleosporales
(Del Prado et al.
2006, Nelsen et al.
2009). Two melanised micro-filamentous lichens, Cystocoleus
ebeneus and Racodium rupestre, were assigned to the order
Capnodiales (Muggia et
al. 2008, Nelsen et
al. 2009). Finally, the two lichen families
Strigulaceae (mostly leaf-colonising tropical species) and
Monoblastiaceae (temperate and tropical species) are now shown to
belong to Dothideomycetes (Nelsen
et al. 2009; this volume).
Whether these lichen lineages, that are unrelated to Lecanoromycetes, originated from independent gains of lichenisation is not clear (Lutzoni et al. 2001, James et al. 2006, Gueidan et al. 2008, Arnold et al. 2009, Schoch et al. 2009a, b). Within Eurotiomycetes, phylogenetic data suggest that the lineage including Pyrenulales and Verrucariales possibly results from an independent gain of lichenisation (Gueidan et al. 2008, Schoch et al. 2009a). Phylogenetic data suggest that lichens in Verrucariales may have evolved from rock-inhabiting fungi (Gueidan et al. 2008), a result in agreement with experimental data demonstrating that some RIF and one melanised lichen-colonising fungus could form associations with lichen-associated algae (Gorbushina et al. 2005, Brunauer et al. 2007). This rock-inhabiting ancestor may have evolved associations with epilithic microalgae in order to get a more constant supply in nutrients. If the evolution of fungal-algal associations occurred in Eurotiomycetes, it most likely also occurred in different fungal groups. It is therefore interesting to see if in Dothideomycetes, where rock fungi are so diverse, similar transitions in lifestyles can be suggested.
Although many lichenised species in Dothideomycetes are either corticolous or only secondarily or occasionally saxicolous, Cystocoleus ebeneus and Racodium rupestre are true rock inhabitants. Amongst lichens in Dothideomycetes, these two species are the most likely to have evolved from a rock-inhabiting ancestor. They share substrate preference and some morphological features, such as their melanised hyphae, with RIF. Strikingly, in our result, Cystocoleus ebeneus is nested within a lineage comprising almost exclusively RIF (Teratosphaeriaceae 2, Fig. 3). Racodium rupestre is also related to a RIF, but this relationship is not supported (Fig. 3). This result agrees with a rock-inhabiting ancestor for these two lichenised species, but further data will however be necessary to test this hypothesis. Also of interest is the close phylogenetic relationship between the lichen order Arthoniales and the lineage 1 of RIF (Figs 2, 4). Although mostly corticolous or foliicolous, Arthoniales also comprises saxicolous species (Ertz et al. 2009). Further data is needed to explore the relationships between saxicolous species of Arthoniales and RIF. In conclusion, these preliminary results suggest that there might be a link between rock-dwelling habit and lichenisation. However, additional taxon and gene sampling are needed to confirm the phylogenetic placements of some of the lichenised taxa and to clarify their relationships to RIF. Only then the hypothesis of RIF as ancestors of lichenised lineages can be adequately tested.
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Acknowledgments |
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TOPAbstractINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONReferences |
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50 % are shown below or above branches. RIF are highlighted in red
and lichens in green. Geographical origins are also labeled for RIF (Alp =
Alps, And = Andes, Ant = Antarctica, Ari = Arizona desert, Cri = Crimea, Fra =
France, Med = Mediterranean region, including Greece, Israel, Italy, Slovenia,
Spain and Turkey). Phylogenetic relationships within Capnodiales are
detailed in 
