Head: Mgr. Zdeněk Kaplan, Ph.D.

People ׀ Projects ׀ Publications

Research topics

Systematics and taxonomy of vascular plants:

• Revision and synthesis of plant diversity
• Taxonomic monographs
• Plant evolution and phylogenetic relationships
• Evolutionary and ecological consequences of genome size variation
• Reproductive systems and microevolution

Systematics, taxonomy and ecology of lichens and fungi (lichenized and non-lichenized fungi):

• Diversity, ecology and evolution of lichens
• Protection of lichens
• Taxonomy and systematics of ascomycetes

Selected recent results

1/ Evolution of the Sabulina verna group (Caryophyllaceae) in Europe

We investigated how different ecological conditions and genome duplication contribute to evolution of the taxonomically intricate Sabulina verna group in Europe. During the postglacial period, members of this group have expanded to the northern tundra, repeatedly colonized mountain ranges and survived at suitable treeless sites in lower altitudes; worth mention is adaptation to various soil types, including toxic substrates containing heavy metals. Applying modern genomic and morphometric methods, we examined 111 populations of this group. We found two distinct groups of diploids, one restricted to the Balkan Peninsula and the other one widespread in Europe. Both groups likely played a role in the origin of tetraploids, which are predominantly found in southern Europe and the Pannonian region. Additionally, we discovered that toxic soils were colonized at least five times, highlighting a complex interaction between geography, toxic substrates, and genome duplication during the evolution of this group.

• Lipánová V., Nunvářová Kabátová K., Zeisek V., Kolář F. & Chrtek J. 2023: Evolution of the Sabulina verna group (Caryophyllaceae) in Europe: A deep split, followed by secondary contacts, multiple allopolyploidization and colonization of challenging substrates. Molecular Phylogenetics and Evolution 189, 1 – 16, doi: 1016/j.ympev.2023.107940

Sabulina verna subsp. hercynica from the former ore pit near Blankenrode in Germany.

 

2/ Alcobiosis – an algal‑fungal association on the threshold of lichenisation

In many corticioid fungi, i.e. fungi that form crust-shaped fruiting bodies on the surface of bark or wood, algae are found inside and underneath the fruiting bodies, often forming a conspicuous layer, and the resulting anatomical structure bears a notable resemblance to lichens. This symbiosis has hitherto escaped the attention of biologists. We described it in detail and introduced the term alobiosis for it. It turns out that a wide range of fungal and algal species enter into this relationship, which together form symbiotic systems at different developmental stages, presumably leading to lichenization. In one case, we even demonstrated carbon transfer from algae to fungi, a process that is characteristic of lichens.

• Vondrák J., Svoboda S., Zíbarová L., Štenclová L., Mareš J., Pouska V., Košnar J. & Kubásek J. 2023: Alcobiosis, an algal‑fungal association on the threshold of lichenisation. Scientific Reports 13, 1–13. doi: 1038/s41598-023-29384-4

Vertical section through alcobiosis in Lyomyces sambuci, observed in UV fluorescence. Algal colonies (red due to chlorophyll autofuorescence) are incorporated in a loose hyphal tissue, below the compact cover of the fungal fruiting body.

 

3/ Consolidation of Chloridium: new classification and re-interpretation of similar morphotypes in the Chaetosphaeriales and Vermiculariopsiellales

Our study presents a novel methodological approach to classification of the genus Chloridium, a poorly explored group of fungi found in soil and decaying wood. Our strategy involves molecular identification, phylogenetic analyses, ancestor reconstruction, morphological hypotheses, and global biogeographic analyses. Our findings challenge the traditional concept of the genus Chloridium. Based on the study of >100 strains, we redefine Chloridium as a monophyletic and polyphyletic genus divided into eight sections. Our analysis of environmental ITS sequences suggests that Chloridium is a common soil fungus, substantially represented in environmental samples. We also demonstrated that Chloridium exhibits species-specific distribution patterns, a rare phenomenon among microscopic soil fungi. Phylogenetic reconstruction of four DNA loci and analysis of an additional 71 strains provided new insights into the relationships between Chloridium and morphologically similar fungi. The latter were classified into two orders within the class Sordariomycetes, representing 11 genera.

• Réblová M., Hernández-Restrepo M., Sklenář F., Nekvindová J., Réblová K. & Kolařík M. 2022: Consolidation of Chloridium: new classification into eight sections with 37 species and reinstatement of the genera Gongromeriza and Psilobotrys. Studies in Mycology 103, 87–212, doi: 3114/sim.2022.103.04

Diversity of colonies in the genus Chloridium.

 

4/ Global biosystematic study of evolution, diversity and hybridization in Stuckenia

Aquatic plants are often widespread, even across continents. They pose a challenge to species delimitation and taxonomy due to their reduced morphology and high phenotypic plasticity. We conducted a multidisciplinary study on the evolution, diversity, genetic variation, fertility and hybridization in Stuckenia, based on worldwide sampling. By applying multiple molecular markers, we were able to clarify species delimitations, describe intraspecific variation and its geographic structuring, and identify a large amount of intra- and interspecific hybrids. We showed that genetic distance is not always correlated with the biological differentiation of the species, the hybridization has been underestimated as a source of diversity, and that misidentifications and erroneous entries in sequence databases are frequent. Phenotypic variation inferred from cultivation experiments as well as assessments of fertility were integrated into an overall interpretation of the speciation patterns. Our study emphasizes that reliable taxonomic conclusions should take a complementary approach that combines data from morphology, distribution, cytology, reproductive biology and genetics.

• Fehrer J., Nagy Nejedlá M., Hellquist C. B., Bobrov A. A. & Kaplan Z. Evolutionary history and patterns of geographical variation, fertility, and hybridization in Stuckenia (Potamogetonaceae). Front. Pl. Sci. 2022, 13: 1042517, doi: 10.3389/fpls.2022.1042517

Phylogenetic analysis showing evolutionary relationships between Stuckenia species and the geographic structuring of intraspecific variation.

 

5/ New classification, taxonomic stability and biogeography of selected microscopic fungi

Our polyphasic study represents a new, comprehensive view on the molecular systematics and biogeography of the polyphyletic genus Codinaea and its relatives. We introduced a new generic concept and defined Codinaea as a monophyletic, polythetic genus that includes four morphotypes that contribute to its morphological complexity. Ancestral inference showed that evolution of some traits is correlated and that these traits previously used to delimit genera occur in species that were newly shown to be congeneric. We recognized five lineages of Codinaea-like fungi and introduced them as new genera. Dual DNA barcoding was successfully used to facilitate species-level identification. Codinaea and its segregates thrive on decaying plants, rarely occurring as endophytes or plant pathogens. In-depth analysis of environmental ITS sequences indicated that they are common in bulk soil and that most species are distributed in either the Holarctic realm or tropical geographic regions. The ancestral climatic zone was temperate, followed by transitions to the tropics.

• Réblová M., Kolařík M., Nekvindová J., Réblová K., Sklenář F., Miller A. N., Hernández-Restrepo M. Phylogenetic Reassessment, Taxonomy, and Biogeography of Codinaea and Similar Fungi. Journal of Fungi 2021, 7: 1097. doi:10.3390/jof7121097

Morphotypes of Codinaea and similar genera with setulate conidia. Conidia and pigments formed in vitro are shown in the central (white) part of the circle. The arrangement of conidiophores with setae, if present, of each genus, along with the morphology of the conidiogenous cells and colony characters are shown in the outer (grey) part of the circle. Pigments diffusing in MLA and OA are shown by their respective colours and colony images; if no pigment is formed, the place at the centre is blank; n/a indicates that this information is not available.

 

6/ Genomic basis and phenotypic manifestation of (non-)parallel serpentine adaptation in Arabidopsis arenosa

Parallel evolution is common in nature and provides one of the most compelling examples of rapid adaptation. There are many studies addressing genomic basis of parallel evolution, but studies linking genomic and phenotypic parallelism are scarce. Toxic serpentine soils, characterized by naturally elevated levels of heavy metals and magnesium, provide an ideal system for rapid parallel adaptation. In our study, we showed independent adaptation in three serpentine populations of Arabidopsis arenosa using a cultivation experiment with serpentine and non-serpentine soils. We found pervasive phenotypic parallelism, for example in heavy metal ion uptake. Genomic parallelism at the gene level was significant, although relatively minor. In contrast, the parallelism at the level of biological functions was relatively high, this may indicate the selection of genes in similar functional pathways, which however lead to the same phenotype.

• Konečná V., Šustr M., Požárová D., Čertner M., Krejčová A., Tylová E. & Kolář F. Genomic basis and phenotypic manifestation of (non-) parallel serpentine adaptation in Arabidopsis arenosa. Evolution 2022, 76: 2315–2331, doi:1111/evo.14593

Illustrative photos of parallel growth response to serpentine soils after 4 months of cultivation (dot colors denote the plant origin; population pairs are in columns; photos taken by V. Konečná).

 

7/ Genetic insight into the adaptation of plants to toxic soils

We showed that genome doubling is an important source of genetic variants. We found that Arabidopsis arenosa repeatedly colonized and adapted to serpentines, toxic edaphic soils, which contain high levels of heavy metals and magnesium. We identified 61 genes under selection. Most of adaptive variants of these genes had a shared origin. However, we also identified potentially functional de novo mutations in polyploids suggesting their broad evolutionary flexibility.

• Konečná V., Bray S., Vlček J., Bohutínská M., Požárová D., Choudhury R. R., Bollmann-Giolai A., Flis P., Salt D. E., Parisod C., Yant L. & Kolář F. 2021: Parallel adaptation in autopolyploid Arabidopsis arenosa is dominated by repeated recruitment of shared alleles. Nature Communications 12, 1 – 13. doi:10.1038/s41467-021-25256-5

Model species Arabidopsis arenosa at a serpentine locality in Austria. Credit D. Požárová

 

8/ Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives

Can we predict evolution? This question is interesting to evolutionary biologists and also to researchers fighting antibiotics or pesticide resistance. We studied the degree of predictability on a model system of convergent adaptation, in which unrelated lineages independently adapt t similar environmental challenges. Thanks to the population genomics analysis of hundreds of plants we showed that the species adapt more similarly (via more comparable gene sets) if they are more related. The reason for this relationship is the ability of related lineages to share beneficial alleles, which they can repeatedly use in their adaptation.

• Bohutínská M., Vlček J., Yair S., Laenen B., Konečná V., Fracassetti M., Slotte T. & Kolář F. 2021: Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives. Proceedings of The National Academy of Sciences of The United States of America 118, 1 – 10. doi:10.1073/pnas.2022713118

Independently evolved alpine forms of Arabidopsis arenosa (upper row) and their foothill ancestors (bottom row).

 

9/ Disparity between morphology and genetics in Urtica dioica (Urticaceae)

The Urtica dioica agg. is a striking example of a polyploid complex, in which diploid taxa are often found in remote and partly relictual geographical ranges, in contrast to widely distributed weed tetraploids, which have an unknown evolutionary history and occur in a variety of synanthropic habitats. Our morphological studies have revealed that diploids form more-or-less separate clusters corresponding to widely accepted subspecies, while molecular evaluation did not reveal any clear structure. Moreover, tetraploids coalesced with diploids in both morphological and molecular analyses, except for plants from south-western Asia. The low genetic differentiation and disparity between morphological and molecular data might be driven by local adaptation of the diploid cytotype that is mirrored in specific phenotypes, only recent genetic diversification of the group and/or homoploid and heteroploid hybridization events.

• Rejlová L., Böhmová A., Chumová Z., Hořčicová Š., Josefiová J., Schmidt P.-A., Trávníček P., Urfus T., Vít P. & Chrtek J. 2021: Disparity between morphology and genetics in Urtica dioica (Urticaceae). Botanical Journal of the Linnean Society 195, 606 – 621. doi:10.1093/botlinnean/boaa076

Diploid Urtica dioica subsp. kurdistanica: (A) upper part of the plant, (B) natural habitat in southern Anatolia, Turkey, (C) middle part of the stem (photo by T. Urfus).

 

10/ Exploring generic boundaries in the Chaetosphaeriaceae

Based on a polyphasic approach we present a new, comprehensive view on the systematics and taxonomy of several genera of microscopic fungi, namely Catenularia, Dictyochaeta, Menisporopsis and Zanclospora. They are associated with significant variability of asexual morphological traits, which led to their broad delimitation. On the other hand, their sexual characters are uniform, leading to speculations whether the extensive morphological plasticity of asexual morphs could be correlated with their ecology. By integrating molecular, RNA structural, morphological and biogeographic data, it was possible to resolve and clarify the concepts of several genera that have been identified as polyphyletic. The dual DNA barcoding using ITS and tef1-α genes, together with tub2, facilitated accurate identification of members of these genera. The geographic distribution inferred from metabarcoding data using GlobalFungi database was consistent with known data and significantly increased our knowledge. Our studies are part of a long-term project leading to a rational classification of chaetosphaeriaceous genera based on phylogeny, and will help find answers regarding the value of morphological characters traditionally used to delimit microscopic fungi.

• Réblová M., Nekvindová J., Kolařík M. & Hernández-Restrepo M. 2021: Delimitation and phylogeny of Dictyochaeta, and introduction of Achrochaeta and Tubulicolla, genera nova. Mycologia 113, 390 – 433. doi:10.1080/00275514.2020.1822095
• Réblová M., Kolařík M., Nekvindová J., Miller A. N. & Hernández-Restrepo, M. 2021: Phylogeny, global biogeography and pleomorphism of Zanclospora. Microorganisms 9, 1 – 61. doi:10.3390/microorganisms9040706
• Réblová M., Nekvindová J. & Miller A. N. 2021: Phylogeny and taxonomy of Catenularia and similar fungi with catenate conidia. MycoKeys 81, 1 – 44. doi:10.3897/mycokeys.81.67785
• Réblová M., Nekvindová J. & Hernández-Restrepo M. 2021: Reflections on Menisporopsis, Multiguttulispora and Tainosphaeria using molecular and morphological data. Journal of Fungi 7, 1 – 36. doi:10.3390/jof7060438

Variability of colonies of the Dictyochaeta fuegiana complex on four nutrient media and sterile stems of Urtica dioica.

 

11/ Atlas of Czech lichens: Dalib.cz

At the beginning of 2021, a new on-line atlas of lichens in the Czech Republic was launched. This is the first Czech lichen atlas, produced with the aim to make the data collected more transparent and better accessible. The portal Dalib.cz includes general characteristics of the Czech lichen biota, current taxonomic treatment and specific information on ecology, distribution and abundance of more than 1700 taxa. Almost 2000 pictures are available in the photo gallery and in individual species cards. For specialists, we developed a database of lichen secondary metabolites, which plays an important role in lichen identifications. General biodiversity (hot-spot) maps and individual species maps are generated from almost 141 000 current records in the DaLiBor database (Database of Lichens and Bryophytes in the Czech Republic). For every single record, a user can display details, including locality, date of collection, substrate and original source. The atlas should serve the public as well as specialists. We believe it will become a useful tool in practical nature conservation. Information on the website is available in Czech and English.

Lichen biodiversity in the Czech Republic – number of taxa recorded in 11×12 km squares (source: Dalib.cz).

 

12/ A strikingly high species diversity on the Roof of the World: the genus Taraxacum in Ladakh

A detailed exploration of Ladakh, a mountain region situated in a rain shadow of the Great Himalaya Range, revealed a twice higher plant species diversity than previously known. The monograph of the model genus Taraxacum encompasses 120 species, of which 50 were discovered as new. This study revealed that the West Himalaya represents one of the world centres of the Taraxacum diversity, with a number of endemic and morphologically and evolutionarily isolated species.

• Kirschner J., Štěpánek J., Klimeš L., Dvorský M., Brůna J., Macek M. & Kopecký M. 2020. The Taraxacum flora of Ladakh, with notes on the adjacent regions of the West Himalaya. Phytotaxa 457: 1-409. doi: 10.11646/phytotaxa.457.1.1

  
Taraxacum dilutissimum Kirschner & Štěpánek, one of the most widespread species in Ladakh, which was, however, scientifically unknown until recently.

 

13/ Parallel alpine differentiation in Arabidopsis arenosa

Parallel evolution provides powerful natural experiments for studying repeatability of evolution and genomic basis of adaptation. Well-documented examples from plants are, however, still rare. Arabidopsis arenosa, a predominantly foothill species with scattered morphologically distinct alpine occurrences is a promising candidate. We sampled foothill and alpine populations in all regions known to harbor the alpine ecotype and used SNP genotyping to test for repeated alpine colonization. We combined field surveys and a common garden experiment to quantify phenotypic parallelism. Genetic clustering by region and coalescent simulations demonstrated parallel origin of alpine ecotype in four mountain regions. Alpine populations exhibited parallelism in height and floral traits. In contrast, leaf traits were distinctive only in certain region(s), reflecting a mixture of plasticity and genetically determined non-parallelism. We demonstrate varying degrees and causes of parallelism and non-parallelism across populations and traits within a plant species. Parallel divergence along a sharp elevation gradient makes A. arenosa a promising candidate for studying the genomic basis of adaptation.

• Knotek A., Konečná V., Wos G., Požárová D., Šrámková G., Bohutínská M., Zeisek V., Marhold K. & Kolář F. Parallel alpine differentiation in Arabidopsis arenosa. Frontiers in Plant Science 2020, 11:561526. doi: 10.3389/fpls.2020.561526

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Alpine morphotype of Arabidospsi arenosa from four mountain ranges: (A) Niedere Tauern, (B) Vysoké Tatry, (C) Rodna, (D) Făgăraș.

 

14/ Evolutionary relationships within the aquatic plant genus Callitriche

Despite a number of unique environmental adaptations, aquatic plants are considerably underrepresented in contemporary biosystematic studies. Moreover, the determination and taxonomic evaluation of aquatic plants is intricate due to the strong morphological reduction and a high degree of phenotypic plasticity. We reconstructed the phylogenetic relationships within the notoriously challenging aquatic genus Callitriche. We demonstrated that most of the recognized Callitriche species are genetically well defined, despite their similar morphologies. In at least three species we discovered and proved the occurrence of cryptic, previously unknown genetic lineages. Two species are probably allopolyploids, i.e. they arose through hybridization and subsequent genome duplication. We also detected four interspecific hybrids, two of which we described as new to science.

• Prančl J.,  Fehrer J., Caklová P., Bambasová V., Lučanová M. & Kaplan Z. Intricate evolutionary history of Callitriche (Plantaginaceae) taxa elucidated by a combination of DNA sequencing and genome size. Taxon 2020, 69: 1016–1041. doi: 10.1002/tax.12315

Floating leaf rosettes of blunt-fruited water starwort (Callitriche obtusangula).

 

15/ New insights into the systematics of Chaetosphaeriales and Savoryellales

Microscopic fungi of Chaetosphaeriales and Savoryellales are important components of ecosystems inhabiting decaying wood and leaves. We focused on traditionally broadly conceived Bactrodesmium and Chaetosphaeria. Research based on phylogenetic analyses, culture and morphological studies enabled to evaluate important taxonomic traits and placement of both genera. After 155 years since the description, we successfully collected B. abruptum, type species of the genus, which prompted a revision of the genus. We discovered that conidia secede rhexolytically, exhibiting multiple secession patterns. We stabilized the generic concept of Bactrodesmium in Savoryellales, while unrelated species were transferred to new genera Aphanodesmium, Gamsomyces and Kaseifertia. Although the morphology of sexual states of most Chaetosphaeria is relatively uniform, their asexual states show variability and evolutionary change. An exception to this morphological monotony is the group of species defined by the unique wall of the fruit body and the morphology of the needle-like spores. We resurrected the genus Paragaeumannomyces in Chaetosphaeriaceae, where these former Chaetosphaeria species were transferred.

• Réblová M., Nekvindová J., Fournier J. & Miller A. N. Delimitation, new species and teleomorph-anamorph relationships in Codinaea, Dendrophoma, Paragaeumannomyces and Striatosphaeria (Chaetosphaeriaceae). MycoKeys 2020, 74: 17–74. doi: 10.3897/mycokeys.74.57824

Coloured fruit bodies of representatives of Paragaeumannomyces and a vertical section of the wall exhibiting a unique three-layered structure.