Publications by authors named "Ana Crespo"

59 Publications

First Report of Cucurbit chlorotic yellows virus infecting Cucumber Plants in Spain.

Plant Dis 2021 Jul 30. Epub 2021 Jul 30.

ValGenetics, Plant Pathology and Microbiology Laboratory, Paterna, Valencia, Spain.

During the winter 2018, symptoms of leaf chlorotic spots (Figure 1) followed by symptoms of leaf interveinal chlorosis (Figure 2) and severe chlorosis in basal leaves were observed in cucumber cv Laredo (Cucumis sativus) plants in three separated greenhouses, sited in distinct locations in southern Spain. In all cases, Bemisia tabaci populations were observed on infected plants. The symptomology observed was similar to that caused by whitefly transmitted Cucurbit yellow stunting disorder virus (CYSDV, genus Crinivirus, family Closteroviridae), which is usually found infecting cucumber plants in this geographical area (1). Samples from four different cucumber plants of distinct greenhouses were collected and tested for the presence of CYSDV. Total RNA was extracted from the samples using the NucleoSpin RNA Plant kit (Macherey-Nagel, Germany). Molecular detection of CYSDV was performed using the multiplex and degenerate primer RT-PCR method (2), specific to the region of the highly conserved RNA-dependent RNA polymerase (RdRp) gene of criniviruses, which also detects other criniviruses such as Lettuce infectious yellows virus (LIYV) and Beet pseudo-yellows virus (BPYV). Results indicated that the viral species CYSDV, LIYV and BPYV were not detected in the four cucurbit plant samples. In 2004, an emergent crinivirus (Cucurbit chlorotic yellows virus, CCYV), inducing symptoms similar to those caused by CYSDV, was described infecting cucurbits in Japan (3). Recently, CCYV was detected in 2011 in Greece (4) and in 2014 in Egypt (5) and Saudi Arabia (6). Therefore, the four RNA samples were tested for the presence of the CCYV by a RT-PCR method previously described (7). Specific primers were designed to amplify 336 nt of the capsid protein (CP) gene and 680 nt of the RdRp gene, located on CCYV genomic RNA 1 and RNA 2, respectively. In all cases, clear cDNA bands of both expected sizes were detected for each cucumber sample that were then purified and sequenced via Sanger technology. BLAST analysis of those sequences showed 99% identity with the nucleotide sequence of the CP and RpRd genes from the CCYV isolates from Greece (LT992911, LT992910), China (KY400633.1, KX118632) and Taiwan (JF502222). To our knowledge, this is the first report of CCYV infecting cucurbits in Spain. Probably CCYV has been spread throughout the Mediterranean basin, remaining undetected due to the yellowing symptom similarities between CYSDV and CCYV. Detection of the emergent virus CCYV in Spain represents a new threat for the horticultural area of southern Europe.
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http://dx.doi.org/10.1094/PDIS-12-20-2553-PDNDOI Listing
July 2021

Thiopurine adherence: high prevalence with low impact in UC outcomes.

Rev Esp Enferm Dig 2021 Mar 18. Epub 2021 Mar 18.

Medicina Digestiva, Hospital Clínico Universitario Valencia, España.

Introduction Thiopurines are used as maintenance therapy in patients with ulcerative colitis (UC). There are contradictory results regarding the relationship between adherence to treatment and risk of relapse. Objectives To quantify and evaluate the trends in thiopurines prescription rates, and to determine the impact and risk factors of non-adherence. Methods Analytical, observational and retrospective study of UC patients, on thiopurines, included in the ENEIDA single-center registry from October 2017 to October 2019. We included adult patients under clinical remission at the beginning of the study on thiopurines maintenance treatment for at least 6 months before recruitment. Adherence was evaluated with an electronic pharmaceutical prescription system. Adherence was considered when 80% or more of the prescribed medication was dispensed at the pharmacy. Kaplan-Meier curves and a regression model were used to examine year-to-year treatment dispensation and identify factors associated to non-adherence. Results A total of 41 patients were included, of whom 71% were males with a mean age of 44 (14) and 26.8% were concomitantly managed with biological therapy. Overall, 22% were non-adherent to thiopurines. No predictive factors of non-adherence were identified. Adherence rate did not correlate with disease activity for two years follow-up (OR 1.6; 95CI =0.3-9.1). Left-sided colitis and concomitant biological treatment were related with disease relapses (p ≤0.01). Conclusion The adherence to thiopurines in UC patients is high (78%). Non-adherence is not related to clinical or pharmacological factors. Adherence rate was not associated with disease activity.
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http://dx.doi.org/10.17235/reed.2021.7630/2020DOI Listing
March 2021

Using target enrichment sequencing to study the higher-level phylogeny of the largest lichen-forming fungi family: Parmeliaceae (Ascomycota).

IMA Fungus 2020 Dec 14;11(1):27. Epub 2020 Dec 14.

Science & Education, The Grainger Bioinformatics Center, Negaunee Integrative Research Center, Gantz Family Collections Center, and Pritzker Laboratory for Molecular Systematics, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL, USA.

Parmeliaceae is the largest family of lichen-forming fungi with a worldwide distribution. We used a target enrichment data set and a qualitative selection method for 250 out of 350 genes to infer the phylogeny of the major clades in this family including 81 taxa, with both subfamilies and all seven major clades previously recognized in the subfamily Parmelioideae. The reduced genome-scale data set was analyzed using concatenated-based Bayesian inference and two different Maximum Likelihood analyses, and a coalescent-based species tree method. The resulting topology was strongly supported with the majority of nodes being fully supported in all three concatenated-based analyses. The two subfamilies and each of the seven major clades in Parmelioideae were strongly supported as monophyletic. In addition, most backbone relationships in the topology were recovered with high nodal support. The genus Parmotrema was found to be polyphyletic and consequently, it is suggested to accept the genus Crespoa to accommodate the species previously placed in Parmotrema subgen. Crespoa. This study demonstrates the power of reduced genome-scale data sets to resolve phylogenetic relationships with high support. Due to lower costs, target enrichment methods provide a promising avenue for phylogenetic studies including larger taxonomic/specimen sampling than whole genome data would allow.
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http://dx.doi.org/10.1186/s43008-020-00051-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7734834PMC
December 2020

Genome-Wide Analysis of Biosynthetic Gene Cluster Reveals Correlated Gene Loss with Absence of Usnic Acid in Lichen-Forming Fungi.

Genome Biol Evol 2020 10;12(10):1858-1868

Department of Science & Education, The Field Museum, Chicago, Illinois.

Lichen-forming fungi are known to produce a large number of secondary metabolites. Some metabolites are deposited in the cortical layer of the lichen thallus where they exert important ecological functions, such as UV filtering. The fact that closely related lineages of lichen-forming fungi can differ in cortical chemistry suggests that natural product biosynthesis in lichens can evolve independent from phylogenetic constraints. Usnic acid is one of the major cortical pigments in lichens. Here we used a comparative genomic approach on 46 lichen-forming fungal species of the Lecanoromycetes to elucidate the biosynthetic gene content and evolution of the gene cluster putatively responsible for the biosynthesis of usnic acid. Whole-genome sequences were gathered from taxa belonging to different orders and families of Lecanoromycetes, where Parmeliaceae is the most well-represented taxon, and analyzed with a variety of genomic tools. The highest number of biosynthetic gene clusters was found in Evernia prunastri, Pannoparmelia angustata, and Parmotrema austrosinense, respectively, and lowest in Canoparmelia nairobiensis, Bulbothrix sensibilis, and Hypotrachyna scytodes. We found that all studied species producing usnic acid contain the putative usnic acid biosynthetic gene cluster, whereas the cluster was absent in all genomes of species lacking usnic acid. The absence of the gene cluster was supported by an additional unsuccessful search for ß-ketoacylsynthase, the most conserved domain of the gene cluster, in the genomes of species lacking usnic acid. The domain architecture of this PKS cluster-homologous to the already known usnic acid PKS cluster (MPAS) and CYT450 (MPAO)-varies within the studied species, whereas the gene arrangement is highly similar in closely related taxa. We hypothesize that the ancestor of these lichen-forming fungi contained the putative usnic acid producing PKS cluster and that the gene cluster was lost repeatedly during the evolution of these groups. Our study provides insight into the genomic adaptations to the evolutionary success of these lichen-forming fungal species and sets a baseline for further exploration of biosynthetic gene content and its evolutionary significance.
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http://dx.doi.org/10.1093/gbe/evaa189DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7643366PMC
October 2020

Draft genome sequences of five species from plantations in China, , and .

IMA Fungus 2019 27;10:22. Epub 2019 Dec 27.

Department of Biochemistry, Genetics and Microbiology (BGM), Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0028 South Africa.

Draft genome sequences of five species [including , , , and ], , and are presented. Species of are the causal agents of Eucalyptus leaf blight disease, threatening the growth and sustainability of plantations in China. is the causal agent of stem canker in native and exotic in South Africa. was first discovered in the infructescences of and in South Africa. is fruticose lichen belongs to the alectorioid clade of the family Parmeliaceae. The availability of these genome sequences will facilitate future studies on the systematics, population genetics, and genomics of these fungi.
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http://dx.doi.org/10.1186/s43008-019-0023-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7325655PMC
December 2019

Chronic Venous Insufficiency as a Predisposing Factor for Basal Cell Carcinoma on Legs.

Ann Vasc Surg 2020 Oct 16;68:185-191. Epub 2020 May 16.

Department of Pathology, Medical School, Unicamp, Campinas, SP, Brazil. Electronic address:

Background: The main risk factor associated with basal cell carcinomas (BCCs) is believed to be exposure to ultraviolet radiation (UVR). In the case of lower limb BCC, the frequency is higher in women, possibly because of greater exposure of the leg to UVR. Chronic venous insufficiency (CVI), also more common in women, may have some association with leg BCCs.

Methods: We retrospectively evaluated the histopathological features of leg BCCs removed between 1993 and 2017 in a tertiary referral center. The patients' clinical data were obtained from medical records, considering, in particular, CVI.

Results: We selected 149 patients with leg BCCs, predominately occurring in elderly Caucasian women. Of those, 71 had a clinical diagnosis of CVI in whom the clinical tumor size and frequency of recurrences were significantly higher than patients without CVI. There was an association between clinical diagnosis of CVI and histological findings of (1) follicular induction in epidermis and (2) distal sweat duct hyperplasia.

Conclusions: CVI, besides the already known UVR exposure, is probably associated with leg BCCs and may determine a worse BCC course.
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http://dx.doi.org/10.1016/j.avsg.2020.04.053DOI Listing
October 2020

Whole-Genome Sequence Data Uncover Widespread Heterothallism in the Largest Group of Lichen-Forming Fungi.

Genome Biol Evol 2019 03;11(3):721-730

Departamento de Farmacología, Farmacognosia y Botánica, Facultad de Farmacia, Universidad Complutense de Madrid, Spain.

Fungal reproduction is regulated by the mating-type (MAT1) locus, which typically comprises two idiomorphic genes. The presence of one or both allelic variants at the locus determines the reproductive strategy in fungi-homothallism versus heterothallism. It has been hypothesized that self-fertility via homothallism is widespread in lichen-forming fungi. To test this hypothesis, we characterized the MAT1 locus of 41 genomes of lichen-forming fungi representing a wide range of growth forms and reproductive strategies in the class Lecanoromycetes, the largest group of lichen-forming fungi. Our results show the complete lack of genetic homothallism suggesting that lichens evolved from a heterothallic ancestor. We argue that this may be related to the symbiotic lifestyle of these fungi, and may be a key innovation that has contributed to the accelerated diversification rates in this fungal group.
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http://dx.doi.org/10.1093/gbe/evz027DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6414310PMC
March 2019

gen. nov. and (Lecanorales, Protoparmelioideae): species description and generic delimitation using DNA barcodes and phenotypical characters.

MycoKeys 2018 14(44):19-50. Epub 2018 Dec 14.

Senckenberg Biodiversity and Climate Research Centre (SBiK-F), Senckenberganlage 25, 60325, Frankfurt am Main, Germany.

Multilocus phylogenetic studies revealed a high level of cryptic diversity within the lichen-forming fungal genus (Protoparmelioideae, Parmeliaceae). Coalescent-based species delimitation suggested that most of the cryptic molecular lineages warranted recognition as separate species. Here we study the morphology and chemistry of these taxa and formally describe eight new species based on phenotypical and molecular characters. Further, we evaluate the use of ITS rDNA as a DNA barcode for identifying species in this genus. For the first time, we obtained an ITS sequence of , the type species of the genus and showed that it is phylogenetically not closely related to species currently placed in or . We assembled a dataset of 66 ITS sequences to assess the interspecies genetic distances amongst the twelve species using ITS as DNA barcode. We found that and form a supported monophyletic group whereas is sister to both. We therefore propose a new genus to accommodate the tropical-subtropical species within Protoparmelioideae, with as the type, , , , , , , and as new species and , , , and as new proposed combinations. We provide a key to and confirm the use of ITS for accurately identifying species in this group.
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http://dx.doi.org/10.3897/mycokeys.44.29904DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6303283PMC
December 2018

Considerations and consequences of allowing DNA sequence data as types of fungal taxa.

IMA Fungus 2018 Jun 24;9(1):167-175. Epub 2018 May 24.

Museum of Evolution, Uppsala University, Norbyvägen 16, 75236 Uppsala, Sweden.

Nomenclatural type definitions are one of the most important concepts in biological nomenclature. Being physical objects that can be re-studied by other researchers, types permanently link taxonomy (an artificial agreement to classify biological diversity) with nomenclature (an artificial agreement to name biological diversity). Two proposals to amend the International Code of Nomenclature for algae, fungi, and plants (ICN), allowing DNA sequences alone (of any region and extent) to serve as types of taxon names for voucherless fungi (mainly putative taxa from environmental DNA sequences), have been submitted to be voted on at the 11 International Mycological Congress (Puerto Rico, July 2018). We consider various genetic processes affecting the distribution of alleles among taxa and find that alleles may not consistently and uniquely represent the species within which they are contained. Should the proposals be accepted, the meaning of nomenclatural types would change in a fundamental way from physical objects as sources of data to the data themselves. Such changes are conducive to irreproducible science, the potential typification on artefactual data, and massive creation of names with low information content, ultimately causing nomenclatural instability and unnecessary work for future researchers that would stall future explorations of fungal diversity. We conclude that the acceptance of DNA sequences alone as types of names of taxa, under the terms used in the current proposals, is unnecessary and would not solve the problem of naming putative taxa known only from DNA sequences in a scientifically defensible way. As an alternative, we highlight the use of formulas for naming putative taxa (candidate taxa) that do not require any modification of the ICN.
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http://dx.doi.org/10.5598/imafungus.2018.09.01.10DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6048565PMC
June 2018

Environment and host identity structure communities of green algal symbionts in lichens.

New Phytol 2018 Jan 11;217(1):277-289. Epub 2017 Sep 11.

Senckenberg Biodiversity and Climate Research Centre (SBiK-F), Senckenberganlage 25, Frankfurt am Main, 60325, Germany.

An understanding of how biotic interactions shape species' distributions is central to predicting host-symbiont responses under climate change. Switches to locally adapted algae have been proposed to be an adaptive strategy of lichen-forming fungi to cope with environmental change. However, it is unclear how lichen photobionts respond to environmental gradients, and whether they play a role in determining the fungal host's upper and lower elevational limits. Deep-coverage Illumina DNA metabarcoding was used to track changes in the community composition of Trebouxia algae associated with two phylogenetically closely related, but ecologically divergent fungal hosts along a steep altitudinal gradient in the Mediterranean region. We detected the presence of multiple Trebouxia species in the majority of thalli. Both altitude and host genetic identity were strong predictors of photobiont community assembly in these two species. The predominantly clonally dispersing fungus showed stronger altitudinal structuring of photobiont communities than the sexually reproducing host. Elevation ranges of the host were not limited by the lack of compatible photobionts. Our study sheds light on the processes guiding the formation and distribution of specific fungal-algal combinations in the lichen symbiosis. The effect of environmental filtering acting on both symbiotic partners appears to shape the distribution of lichens.
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http://dx.doi.org/10.1111/nph.14770DOI Listing
January 2018

A temporal banding approach for consistent taxonomic ranking above the species level.

Sci Rep 2017 05 23;7(1):2297. Epub 2017 May 23.

Science & Education, Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, IL, 60605, USA.

Comparable taxonomic ranks within clades can facilitate more consistent classifications and objective comparisons among taxa. Here we use a temporal approach to identify taxonomic ranks. This is an extension of the temporal banding approach including a Temporal Error Score that finds an objective cut-off for each taxonomic rank using information for the current classification. We illustrate this method using a data set of the lichenized fungal family Parmeliaceae. To assess its performance, we simulated the effect of taxon sampling and compared our method with the other temporal banding method. For our sampled phylogeny, 11 of the 12 included families remained intact and 55 genera were confirmed, whereas 32 genera were lumped and 15 genera were split. Taxon sampling impacted the method at the genus level, whereas yielded only insignificant changes at the family level. The other available temporal approach also gives a similar cutoff point to our method. Our approach to identify taxonomic ranks enables taxonomists to revise and propose classifications on an objective basis, changing ranks of clades only when inconsistent with most taxa in a phylogenetic tree. An R script to find the time point with the minimal temporal error is provided.
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http://dx.doi.org/10.1038/s41598-017-02477-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5442095PMC
May 2017

Protective effects of lichen metabolites evernic and usnic acids against redox impairment-mediated cytotoxicity in central nervous system-like cells.

Food Chem Toxicol 2017 Jul 24;105:262-277. Epub 2017 Apr 24.

Department of Pharmacology, Faculty of Pharmacy, University Complutense of Madrid, Plaza Ramón y Cajal s/n, 28040, Madrid, Spain. Electronic address:

Lichens species produce unique secondary metabolites that attract increasing pharmacological interest, including their redox modulatory activities. Current work evaluated for the first time the in vitro cytoprotective properties, based on the antioxidant activities, of the Parmeliaceae lichens Evernia prunastri and Usnea ghattensis and the mechanism of action of their major phenolic constituents: the evernic and usnic acids, respectively. In two models of central nervous system-like cells (U373-MG and SH-SY5Y cell lines), exogenous HO induced oxidative stress-mediated cytotoxicity. We first assessed their radical scavenging capacities (ORAC and DPPH tests) and the phenolic content of the extracts. At the optimal concentrations, pretreatments with evernic acid displayed significant protection against HO-induced cytotoxic damage in both models. It reversed the alterations in oxidative stress markers (including ROS generation, glutathione system and lipid peroxidation levels) and cellular apoptosis (caspase-3 activity). Such effects were in part mediated by a notable enhancement of the expression of intracellular phase-II antioxidant enzymes; a plausible involvement of the Nrf2 cytoprotective pathway is suggested. Usnic acid exerted similar effects, to some extent more moderate. Results suggest that lichen polyketides evernic and usnic acids merit further research as promising antioxidant candidates in the therapy of oxidative stress-related diseases, including the neurodegenerative disorders.
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http://dx.doi.org/10.1016/j.fct.2017.04.030DOI Listing
July 2017

[Thyroid Metastasis as the Initial Presentation of an Asymptomatic Clear Cell Renal Carcinoma].

Acta Med Port 2016 Nov 30;29(11):755-758. Epub 2016 Nov 30.

Serviço de Cirurgia Geral. Hospital de Curry Cabral. Centro Hospitalar de Lisboa Central. Lisboa. Portugal.

Introduction: Clear cell renal carcinoma metastases to the thyroid gland are rare and only diagnosable after an immunohistochemistry analysis of the histological sample. The purpose of this article is to report a case of thyroid metastasis as the initial presentation of a clear cell renal carcinoma.

Case Report: Male patient with a solid nodule in the left lobe of the thyroid, 5.3 cm in diameter, suspicious of malignancy, for which a total thyroidectomy with central compartment lymphadenectomy was performed. Histology revealed two clear cell renal carcinoma metastases. After evaluation of the kidney, the patient underwent radical nephrectomy four months later.

Discussion: What makes this case interesting is that thyroid metastases as the initial presentation of renal cell carcinoma are rare, but if treated early, a 'double surgical resection' is possible, leading to a 5 year survival rate of 80%.
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http://dx.doi.org/10.20344/amp.7277DOI Listing
November 2016

Panmixia and dispersal from the Mediterranean Basin to Macaronesian Islands of a macrolichen species.

Sci Rep 2017 01 19;7:40879. Epub 2017 Jan 19.

Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain.

The Mediterranean region, comprising the Mediterranean Basin and the Macaronesian Islands, represents a center of diversification for many organisms. The genetic structure and connectivity of mainland and island microbial populations has been poorly explored, in particular in the case of symbiotic fungi. Here we investigated genetic diversity and spatial structure of the obligate outcrossing lichen-forming fungus Parmelina carporrhizans in the Mediterranean region. Using eight microsatellite and mating-type markers we showed that fungal populations are highly diverse but lack spatial structure. This is likely due to high connectivity and long distance dispersal of fungal spores. Consistent with low levels of linkage disequilibrium and lack of clonality, we detected both mating-type idiomorphs in all populations. Furthermore we showed that the Macaronesian Islands are the result of colonization from the Mediterranean Basin. The unidirectional gene flow, though, seemed not to be sufficient to counterbalance the effects of drift, resulting in comparatively allelic poor peripheral populations. Our study is the first to shed light on the high connectivity and lack of population structure in natural populations of a strictly sexual lichen fungus. Our data further support the view of the Macaronesian Islands as the end of the colonization road for this symbiotic ascomycete.
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http://dx.doi.org/10.1038/srep40879DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5244402PMC
January 2017

In vitro neuroprotective potential of lichen metabolite fumarprotocetraric acid via intracellular redox modulation.

Toxicol Appl Pharmacol 2017 02 29;316:83-94. Epub 2016 Dec 29.

Department of Pharmacology, Faculty of Pharmacy, University Complutense of Madrid, Plaza Ramón y Cajal s/n, 28040 Madrid, Spain. Electronic address:

The lichen-forming fungi Cetraria islandica has been largely used in folk medicines, and it has recently showed promising in vitro antioxidant effects in glial-like cells. Current work aimed at investigating the neuroprotective potential of its major isolated secondary metabolite: the depsidone fumarprotocetraric acid (FUM). HO was used herein to induce oxidative stress (OS)-mediated cytotoxicity in two models of neurons and astrocytes cells (SH-SY5Y and U373-MG cell lines). We found that a pre-treatment with FUM significantly enhanced cell viability compared to HO-treated cells, and we selected the optimal concentrations in each model (1 and 25μg/ml, respectively) for assessing its cytoprotective mechanisms. FUM, which exerted effective peroxyl radical scavenging effect in the chemical oxygen radical antioxidant capacity (ORAC) assay, alleviated the alterations in OS markers provoked by HO. It attenuated intracellular ROS formation, lipid peroxidation and GSH depletion. At mitochondrial level, FUM prevented from the dissipation of mitochondrial membrane potential and the increase in mitochondrial calcium, implying a protective role against oxidative damage in mitochondrial membrane. Similarly, FUM pre-treatment diminished HO-induced apoptosis, as evidenced by the reduction in caspase-3 activity and expression; inmunoblot analysis also revealed a decrease in Bax and an increase in Bcl-2 proteins levels. Furthermore, FUM up-regulated the expression of the antioxidant enzymes catalase, superoxide dismutase-1, and hemeoxigenase-1. These findings and the activation of Nrf2 binding activity in nuclear extracts suggest a plausible involvement of Nrf2 signaling pathway in the cytoprotection by FUM. In conclusion, FUM emerges as a potential drug candidate in the therapy of OS-related diseases, such as the neurodegenerative disorders.
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http://dx.doi.org/10.1016/j.taap.2016.12.020DOI Listing
February 2017

Fungal-algal association patterns in lichen symbiosis linked to macroclimate.

New Phytol 2017 Apr 5;214(1):317-329. Epub 2016 Dec 5.

Department of Biological Sciences, Institute of Ecology, Evolution and Diversity, Goethe Universität, Frankfurt am Main, Germany.

Both macroclimate and evolutionary events may influence symbiont association and diversity patterns. Here we assess how climatic factors and evolutionary events shape fungal-algal association patterns in the widely distributed lichen-forming fungal genus Protoparmelia. Multilocus phylogenies of fungal and algal partners were generated using 174 specimens. Coalescent-based species delimitation analysis suggested that 23 fungal hosts are associating with 20 algal species. Principal component analysis (PCA) was performed to infer how fungal-algal association patterns varied with climate. Fungi associated with one to three algal partners whereas algae accepted one to five fungal partners. Both fungi and algae were more specific, associating with fewer partners, in the warmer climates. Interaction with more than one partner was more frequent in cooler climates for both the partners. Cophylogenetic analyses suggest congruent fungal-algal phylogenies. Host switch was a more common event in warm climates, whereas failure of the photobiont to diverge with its fungal host was more frequent in cooler climates. We conclude that both environmental factors and evolutionary events drive fungal and algal evolution in Protoparmelia. The processes leading to phylogenetic congruence of fungi and algae are different in different macrohabitats in our study system. Hence, closely related species inhabiting diverse habitats may follow different evolutionary pathways.
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http://dx.doi.org/10.1111/nph.14366DOI Listing
April 2017

Hidden diversity before our eyes: Delimiting and describing cryptic lichen-forming fungal species in camouflage lichens (Parmeliaceae, Ascomycota).

Fungal Biol 2016 11;120(11):1374-1391

Science & Education, The Field Museum, 1400 South Lake Shore Drive, Chicago, IL, 60605, USA.

Molecular data provide unprecedented insight into diversity of lichenized fungi, although morphologically cryptic species-level lineages circumscribed from sequence data often remain undescribed even in well-studies groups. Using diagnostic characters from DNA sequence data and support from the multispecies coalescent model, we formally describe a total of eleven new species and resurrect two others in the hyperdiverse lichen-forming fungal family Parmeliaceae. These include: four in the genus Melanelixia - M. ahtii sp. nov., M. epilosa comb. nov., M. hawksworthii sp. nov., and M. robertsoniorum sp. nov.; six in Melanohalea - M. austroamericana sp. nov., M. beringiana sp. nov., M. clari sp. nov., M. columbiana sp. nov., M. davidii sp. nov., and M. tahltan sp. nov.; and three species in Montanelia - M. occultipanniformis sp. nov., M. saximontana comb. nov., and M. secwepemc sp. nov. Morphological, ecological and geographical features were revised to corroborate species descriptions. These species can consistently be distinguished by differences in nucleotide position characters in the fungal barcoding marker (ITS) and high speciation probabilities. This study helps close the "taxonomic gap" between molecular species delimitation studies and formal taxonomy by incorporating statistical evaluation of lineage independence, diagnostic differences in DNA data, and additional consideration of differences in morphology and species distributions.
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http://dx.doi.org/10.1016/j.funbio.2016.06.001DOI Listing
November 2016

A Festschrift for David L. Hawksworth.

Fungal Biol 2016 11 20;120(11):1269-1271. Epub 2016 Aug 20.

Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA. Electronic address:

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http://dx.doi.org/10.1016/j.funbio.2016.08.003DOI Listing
November 2016

Hidden Genetic Diversity in an Asexually Reproducing Lichen Forming Fungal Group.

PLoS One 2016 11;11(8):e0161031. Epub 2016 Aug 11.

Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense, Madrid, Spain.

Asexual species with vegetative propagation of both symbiont partners (soredia) in lichens may harbor lower species diversity because they may indeed represent evolutionary dead ends or clones. In this study we aim to critically examine species boundaries in the sorediate lichen forming fungi Parmotrema reticulatum-Parmotrema pseudoreticulatum complex applying coalescent-based approaches and other recently developed DNA-based methods. To this end, we gathered 180 samples from Africa, Asia, Australasia, Europe, North and South America and generated sequences of internal transcribed spacer of nuclear ribosomal DNA (ITS) and DNA replication licensing factor MCM7 (MCM7). The dataset was analysed using different approaches such as traditional phylogeny-maximum likelihood and Bayesian-genetic distances, automatic barcode gap discovery and coalescent-based methods-PTP, GMYC, spedeSTEM and *Beast-in order to test congruence among results. Additionally, the divergence times were also estimated to elucidate diversification events. Delimitations inferred from the different analyses are comparable with only minor differences, and following a conservative approach we propose that the sampled specimens of the P. reticulatum-P. pseudoreticulatum complex belong to at least eight distinct species-level lineages. Seven are currently classified under P. reticulatum and one as P. pseudoreticulatum. In this work we discuss one of only few examples of cryptic species that have so far been found in sorediate reproducing lichen forming fungi. Additionally our estimates suggest a recent origin of the species complex-during the Miocene. Consequently, the wide distribution of several of the cryptic species has to be explained by intercontinental long-distance dispersal events.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0161031PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4981466PMC
August 2017

An Integrative Approach for Understanding Diversity in the Punctelia rudecta Species Complex (Parmeliaceae, Ascomycota).

PLoS One 2016 10;11(2):e0146537. Epub 2016 Feb 10.

Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, Madrid, Spain.

High levels of cryptic diversity have been documented in lichenized fungi, especially in Parmeliaceae, and integrating various lines of evidence, including coalescent-based species delimitation approaches, help establish more robust species circumscriptions. In this study, we used an integrative taxonomic approach to delimit species in the lichen-forming fungal genus Punctelia (Parmeliaceae), with a particular focus on the cosmopolitan species P. rudecta. Nuclear, mitochondrial ribosomal DNA and protein-coding DNA sequences were analyzed in phylogenetic and coalescence-based frameworks. Additionally, morphological, ecological and geographical features of the sampled specimens were evaluated. Five major strongly supported monophyletic clades were recognized in the genus Punctelia, and each clade could be characterized by distinct patterns in medullary chemistry. Punctelia rudecta as currently circumscribed was shown to be polyphyletic. A variety of empirical species delimitation methods provide evidence for a minimum of four geographically isolated species within the nominal taxon Punctelia rudecta, including a newly described saxicolous species, P. guanchica, and three corticolous species. In order to facilitate reliable sample identification for biodiversity, conservation, and air quality bio-monitoring research, these three species have been epitypified, in addition to the description of a new species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0146537PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4749632PMC
July 2016

Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi.

New Phytol 2015 Dec 24;208(4):1217-26. Epub 2015 Aug 24.

Biodiversity and Climate Research Centre BiK-F, Senckenberganlage 25, 60325, Frankfurt am Main, Germany.

We studied the evolutionary history of the Parmeliaceae (Lecanoromycetes, Ascomycota), one of the largest families of lichen-forming fungi with complex and variable morphologies, also including several lichenicolous fungi. We assembled a six-locus data set including nuclear, mitochondrial and low-copy protein-coding genes from 293 operational taxonomic units (OTUs). The lichenicolous lifestyle originated independently three times in lichenized ancestors within Parmeliaceae, and a new generic name is introduced for one of these fungi. In all cases, the independent origins occurred c. 24 million yr ago. Further, we show that the Paleocene, Eocene and Oligocene were key periods when diversification of major lineages within Parmeliaceae occurred, with subsequent radiations occurring primarily during the Oligocene and Miocene. Our phylogenetic hypothesis supports the independent origin of lichenicolous fungi associated with climatic shifts at the Oligocene-Miocene boundary. Moreover, diversification bursts at different times may be crucial factors driving the diversification of Parmeliaceae. Additionally, our study provides novel insight into evolutionary relationships in this large and diverse family of lichen-forming ascomycetes.
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http://dx.doi.org/10.1111/nph.13553DOI Listing
December 2015

Neuroprotective activity and cytotoxic potential of two Parmeliaceae lichens: Identification of active compounds.

Phytomedicine 2015 Aug 27;22(9):847-55. Epub 2015 Jun 27.

Department of Pharmacology, Faculty of Pharmacy, University Complutense of Madrid, Plaza Ramón y Cajal s/n, 28040 Madrid, Spain. Electronic address:

Background: Lichens are symbiotic organisms capable of producing unique secondary metabolites, whose pharmacological activities are attracting much interest.

Purpose: The present study aimed to investigate the in vitro neuroprotective effects and anticancer potential of methanol extracts of two Parmeliaceae lichens: Cetraria islandica and Vulpicida canadensis. The chemical composition of the two lichens was also determined.

Methods: Neuroprotective activity was studied with respect to the antioxidant properties of the extracts; radical scavenging tests (ORAC and DPPH assays) were performed and oxidative stress markers (intracellular ROS production, caspase-3 activity, MDA and glutathione levels) were assessed in a hydrogen peroxide-induced oxidative stress model in astrocytes. Cytotoxic activity was tested against human HepG2 (hepatocellular carcinoma) and MCF-7 (breast adenocarcinoma) cell lines.

Results: Cell viability studies identified a single concentration for each extract that was subsequently used to measure oxidative stress markers. Lichen extracts were able to reverse the oxidative damage caused by hydrogen peroxide, thus promoting astrocyte survival. Both lichen extracts also had anticancer activity in the cell lines, with IC50 values of 19.51-181.05 µg/ml. The extracts had a high total phenolic content, and the main constituents identified by HPLC were fumarprotocetraric acid in Cetraria islandica, and usnic, pinastric and vulpinic acids in Vulpicida canadensis. The biological activities of the lichen extracts can be attributed to these secondary metabolites.

Conclusion: The lichen species studied are promising sources of natural compounds with neuroprotective activity and cytotoxic potential, and warrant further research.
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http://dx.doi.org/10.1016/j.phymed.2015.06.005DOI Listing
August 2015

Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota).

Mol Ecol 2015 07 14;24(14):3779-97. Epub 2015 Jul 14.

Science & Education, The Field Museum, Chicago, IL, USA.

Microbial symbionts are instrumental to the ecological and long-term evolutionary success of their hosts, and the central role of symbiotic interactions is increasingly recognized across the vast majority of life. Lichens provide an iconic group for investigating patterns in species interactions; however, relationships among lichen symbionts are often masked by uncertain species boundaries or an inability to reliably identify symbionts. The species-rich lichen-forming fungal family Parmeliaceae provides a diverse group for assessing patterns of interactions of algal symbionts, and our study addresses patterns of lichen symbiont interactions at the largest geographic and taxonomic scales attempted to date. We analysed a total of 2356 algal internal transcribed spacer (ITS) region sequences collected from lichens representing ten mycobiont genera in Parmeliaceae, two genera in Lecanoraceae and 26 cultured Trebouxia strains. Algal ITS sequences were grouped into operational taxonomic units (OTUs); we attempted to validate the evolutionary independence of a subset of the inferred OTUs using chloroplast and mitochondrial loci. We explored the patterns of symbiont interactions in these lichens based on ecogeographic distributions and mycobiont taxonomy. We found high levels of undescribed diversity in Trebouxia, broad distributions across distinct ecoregions for many photobiont OTUs and varying levels of mycobiont selectivity and specificity towards the photobiont. Based on these results, we conclude that fungal specificity and selectivity for algal partners play a major role in determining lichen partnerships, potentially superseding ecology, at least at the ecogeographic scale investigated here. To facilitate effective communication and consistency across future studies, we propose a provisional naming system for Trebouxia photobionts and provide representative sequences for each OTU circumscribed in this study.
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http://dx.doi.org/10.1111/mec.13271DOI Listing
July 2015

Biogeography and Genetic Structure in Populations of a Widespread Lichen (Parmelina tiliacea, Parmeliaceae, Ascomycota).

PLoS One 2015 11;10(5):e0126981. Epub 2015 May 11.

Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Madrid, Spain.

The genetic diversity and population structure of the foliose lichenized fungus Parmelina tiliacea has been analyzed through its geographical range, including samples from Macaronesia (Canary Islands), the Mediterranean, and Eurosiberia. DNA sequences from the nuclear ribosomal internal transcribed spacer, the mitochondrial large subunit ribosomal RNA gene, and the translation elongation factor 1-α were used as molecular markers. The haplotypes of the three markers and the molecular variance analyses of multilocus haplotypes showed the highest diversity in the Canary Islands, while restricted haplotypes occurred at high frequencies in Mediterranean coastal samples. The multilocus haplotypes formed three unevenly distributed clusters (clusters 1-3). In the Canary Islands all the haplotypes were present in a similar proportion, while the coastal Mediterranean sites had almost exclusively haplotypes of cluster 3; cluster 2 predominated in inland Mediterranean sites; and cluster 1 was more abundant in central and northern Europe (Eurosiberian area). The distribution of clusters is partially explained by climatic factors, and its interaction with local spatial structure, but much of the variation remains unexplained. The high frequency of individuals in the Canary Islands with haplotypes shared with other areas suggests that could be a refugium of genetic diversity, and the high frequency of individuals of the Mediterranean coastal sites with restricted haplotypes indicates that gene flow to contiguous areas may be restricted. This is significant for the selection of areas for conservation purposes, as those with most genetic variation may reflect historical factors and biological properties of the species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0126981PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4427293PMC
February 2016

A Tale of Two Hyper-diversities: Diversification dynamics of the two largest families of lichenized fungi.

Sci Rep 2015 May 6;5:10028. Epub 2015 May 6.

Science and Education, The Field Museum, 1400 S Lake Shore Drive, Chicago, IL 60605 USA.

Renewed interests in macroevolutionary dynamics have led to the proliferation of studies on diversification processes in large taxonomic groups, such as angiosperms, mammals, and birds. However, such a study has yet to be conducted in lichenized fungi--an extremely successful and diverse group of fungi. Analysing the most comprehensive time-calibrated phylogenies with a new analytical method, we illustrated drastically different diversification dynamics between two hyper-diverse families of lichenized fungi, Graphidaceae and Parmeliaceae, which represent more than a fourth of the total species diversity of lichenized fungi. Despite adopting a similar nutrition mode and having a similar number of species, Graphidaceae exhibited a lower speciation rate, while Parmeliaceae showed a sharp increase in speciation rate that corresponded with the aridification during the Oligocene-Miocene transition, suggesting their adaptive radiation into a novel arid habitat.
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http://dx.doi.org/10.1038/srep10028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4421861PMC
May 2015

Coalescent-based species delimitation approach uncovers high cryptic diversity in the cosmopolitan lichen-forming fungal genus Protoparmelia (Lecanorales, Ascomycota).

PLoS One 2015 1;10(5):e0124625. Epub 2015 May 1.

Department of Biological Sciences, Institute of Ecology, Evolution and Diversity, Goethe Universität, Grüneburgplatz 1, 60323, Frankfurt am Main, Germany; Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, 60325, Frankfurt am Main, Germany.

Species recognition in lichen-forming fungi has been a challenge because of unsettled species concepts, few taxonomically relevant traits, and limitations of traditionally used morphological and chemical characters for identifying closely related species. Here we analyze species diversity in the cosmopolitan genus Protoparmelia s.l. The ~25 described species in this group occur across diverse habitats from the boreal-arctic/alpine to the tropics, but their relationship to each other remains unexplored. In this study, we inferred the phylogeny of 18 species currently assigned to this genus based on 160 specimens and six markers: mtSSU, nuLSU, ITS, RPB1, MCM7, and TSR1. We assessed the circumscription of species-level lineages in Protoparmelia s. str. using two coalescent-based species delimitation methods--BP&P and spedeSTEM. Our results suggest the presence of a tropical and an extra-tropical lineage, and eleven previously unrecognized distinct species-level lineages in Protoparmelia s. str. Several cryptic lineages were discovered as compared to phenotype-based species delimitation. Many of the putative species are supported by geographic evidence.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0124625PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4416777PMC
January 2016

Antioxidant potential of lichen species and their secondary metabolites. A systematic review.

Pharm Biol 2016 17;54(1):1-17. Epub 2015 Apr 17.

b Department of Plant Biology II, Faculty of Pharmacy , Universidad Complutense Madrid , Madrid , Spain.

Context: Pharmacological interest of lichens lies in their capacity to produce bioactive secondary metabolites, being most of them phenolic compounds with reactive hydroxyl groups that confer antioxidant potential through various mechanisms. Increasing incidence and impact of oxidative stress-related diseases (i.e., neurodegenerative disorders) has encouraged the search of new pharmacological strategies to face them. Lichens appear to be a promising source of phenolic compounds in the discovery of natural products exerting antioxidant activity.

Objective: The present review thoroughly discusses the available knowledge on antioxidant properties of lichens, including both in vitro and in vivo studies and the parameters assessed so far on lichen constituents.

Methods: Literature survey was performed by using as main databases PubMed, Google Scholar, Scopus, Science Direct, and Recent Literature on Lichens. We reviewed 98 highlighted research articles without date restriction.

Results: Current report collects data related to antioxidant activities of more than 75 lichen species (from 18 botanical families) and 65 isolated metabolites. Much information comes from in vitro investigations, such as chemical assays evaluating radical scavenging properties, lipid peroxidation inhibition, and reducing power of lichen species and compounds; similarly, research on cellular substrates and animal models generally measures antioxidant enzymes levels and other antioxidant markers, such as glutathione levels or tissue peroxidation.

Conclusion: Since consistent evidence demonstrated the contribution of oxidative stress on the development and progression of several human diseases, reviewed data suggest that some lichen compounds are worthy of further investigation and better understanding of their antioxidant and neuroprotective potentials.
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http://dx.doi.org/10.3109/13880209.2014.1003354DOI Listing
September 2016

A reliable and valid questionnaire was developed to measure computer vision syndrome at the workplace.

J Clin Epidemiol 2015 Jun 28;68(6):662-73. Epub 2015 Jan 28.

Community Nursing Preventive Medicine Public Health and History of Science Department, Public Health Research Group, Occupational Health Research Centre (CISAL), CIBER Epidemiology and Public Health (CIBERESP), University of Alicante, Carretera de San Vicente del Raspeig s/n. 03690, San Vicente del Raspeig, Alicante, Spain.

Objectives: To design and validate a questionnaire to measure visual symptoms related to exposure to computers in the workplace.

Study Design And Setting: Our computer vision syndrome questionnaire (CVS-Q) was based on a literature review and validated through discussion with experts and performance of a pretest, pilot test, and retest. Content validity was evaluated by occupational health, optometry, and ophthalmology experts. Rasch analysis was used in the psychometric evaluation of the questionnaire. Criterion validity was determined by calculating the sensitivity and specificity, receiver operator characteristic curve, and cutoff point. Test-retest repeatability was tested using the intraclass correlation coefficient (ICC) and concordance by Cohen's kappa (κ).

Results: The CVS-Q was developed with wide consensus among experts and was well accepted by the target group. It assesses the frequency and intensity of 16 symptoms using a single rating scale (symptom severity) that fits the Rasch rating scale model well. The questionnaire has sensitivity and specificity over 70% and achieved good test-retest repeatability both for the scores obtained [ICC = 0.802; 95% confidence interval (CI): 0.673, 0.884] and CVS classification (κ = 0.612; 95% CI: 0.384, 0.839).

Conclusion: The CVS-Q has acceptable psychometric properties, making it a valid and reliable tool to control the visual health of computer workers, and can potentially be used in clinical trials and outcome research.
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http://dx.doi.org/10.1016/j.jclinepi.2015.01.015DOI Listing
June 2015

Characterization of fungus-specific microsatellite markers in the lichen-forming fungus Parmelina carporrhizans (Parmeliaceae).

Appl Plant Sci 2014 Dec 20;2(12). Epub 2014 Nov 20.

Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, Madrid 28040, Spain.

Unlabelled:

Premise Of The Study: Microsatellite loci were developed to study the lichen-forming fungus Parmelina (Parmeliaceae) in different habitats of western Europe and the Mediterranean for baseline studies to understand the effects of climate change on its distribution. •

Methods And Results: We cultured P. carporrhizans from ascospores for genomic sequencing with Illumina HiSeq. We successfully developed 11 polymorphic microsatellite markers and associated primer sets and assessed them with 30 individuals from two of the Canary Islands. The average number of alleles per locus was 8.8. Nei's unbiased gene diversity of these loci ranged from 0.53 to 0.91 in the tested populations. Amplification in two closely related species (P. tiliacea, P. cryptotiliacea) yielded only limited success. •

Conclusions: The new microsatellite markers will allow the study of genetic diversity and population structure in P. carporrhizans. We propose eight markers to combine in two multiplex reactions for further studies on a larger set of populations.
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http://dx.doi.org/10.3732/apps.1400081DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4259457PMC
December 2014

Characterization of microsatellite loci in lichen-forming fungi of Bryoria section Implexae (Parmeliaceae).

Appl Plant Sci 2014 Jul 10;2(7). Epub 2014 Jul 10.

Swiss Federal Research Institute WSL, Zürcherstrasse 111, CH-8903 Birmensdorf, Switzerland.

Unlabelled:

Premise Of The Study: The locally rare, haploid, lichen-forming fungi Bryoria capillaris, B. fuscescens, and B. implexa are associated with boreal forests and belong to Bryoria sect. Implexae. Recent phylogenetic studies consider them to be conspecific. Microsatellite loci were developed to study population structure in Bryoria sect. Implexae and its response to ecosystem disturbances. •

Methods And Results: We developed 18 polymorphic microsatellite markers using 454 pyrosequencing data assessed in 82 individuals. The number of alleles per locus ranged from two to 13 with an average of 4.6. Nei's unbiased gene diversity, averaged over loci, ranged from 0.38 to 0.52. The markers amplified with all three species, except for markers Bi05, Bi15, and Bi18. •

Conclusions: The new markers will allow the study of population subdivision, levels of gene introgression, and levels of clonal spread of Bryoria sect. Implexae. They will also facilitate an understanding of the effects of forest disturbance on genetic diversity of these lichen species.
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http://dx.doi.org/10.3732/apps.1400037DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4103479PMC
July 2014
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