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Diversification and Species Delimitation of Lichenized Fungi in Selected Groups of the Family Parmeliaceae (Ascomycota)

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Diversification and Species Delimitation of Lichenized Fungi in Selected Groups of the Family Parmeliaceae (Ascomycota) Diversification and species delimitation of lichenized fungi in selected groups of the family Parmeliaceae (Ascomycota) Kristiina Mark Tartu 7.10.2016 Publications I Mark, K., Saag, L., Saag, A., Thell, A., & Randlane, T. (2012) Testing morphology-based delimitation of Vulpicida juniperinus and V. tubulosus (Parmeliaceae) using three molecular markers. The Lichenologist 44 (6): 752−772. II Saag, L., Mark, K., Saag, A., & Randlane, T. (2014) Species delimitation in the lichenized fungal genus Vulpicida (Parmeliaceae, Ascomycota) using gene concatenation and coalescent-based species tree approaches. American Journal of Botany 101 (12): 2169−2182. III Mark, K., Saag, L., Leavitt, S. D., Will-Wolf, S., Nelsen, M. P., Tõrra, T., Saag, A., Randlane, T., & Lumbsch, H. T. (2016) Evaluation of traditionally circumscribed species in the lichen-forming genus Usnea (Parmeliaceae, Ascomycota) using six-locus dataset. Organisms Diversity & Evolution 16 (3): 497–524. IV Mark, K., Randlane, T., Hur, J.-S., Thor, G., Obermayer, W. & Saag, A. Lichen chemistry is concordant with multilocus gene genealogy and reflects the species diversification in the genus Cetrelia (Parmeliaceae, Ascomycota). Manuscript submitted to The Lichenologist. V Mark, K., Cornejo, C., Keller, C., Flück, D., & Scheidegger, C. (2016) Barcoding lichen- forming fungi using 454 pyrosequencing is challenged by artifactual and biological sequence variation. Genome 59 (9): 685–704. Systematics • Provides units for biodiversity measurements and investigates evolutionary relationships • Inadequate and unstable taxonomy affects a variety of fields and can have financial ramifications Lichen taxonomy • Lichens classified based on the fungal partner of the symbiotic organism • Identification traditionally based on thallus morphology • Incongruence between morphological circumscriptions of species and DNA sequence data of mycobiont The main objectives of the thesis (1) Estimate phylogenetic relationships and delimit species in selected groups of the family Parmeliaceae (2) Evaluate the utility of traditionally used characters in these lichens (3) Assess the accuracy of DNA-based species identification in lichenized fungi using next-generation sequencing (NGS) Study groups I Taxonomic study of genus Vulpicida with emphasis on European taxa II Taxonomic study of genus Vulpicida in northern hemisphere III Taxonomic study of genus Usnea sect. Usnea in Europe and North America IV Taxonomic study of genus Cetrelia in Asia V NGS barcoding of 100 species from the order Lecanorales in Switzerland Study material I n=78 II n=70 III n=144 IV n=64 V n=100 Parmotrema (350) Crespoa (4) Study groups Flavoparmelia (32) 9 Austroparmelina (13) 18 Punctelia (45) Nesolechia (1) Canoparmelia sp Flavopunctelia (5) Canoparmelia s.str. (35) Xanthoparmelia (820) 8 Cetrelia (18) Parmelioid 5 Melanohalea (22) Melanelixia (15) 18 species Emodomelanelia masonii Montanelia (5) Remototrachyna 6 (19) Bulbothrix (20) 4 Bulbothrix (40) Parmelinella (7) Parmelina (10) Myelochroa (30) Hypotrachyna (260) Parmeliopsis (3) Nipponoparmelia (4) Parmelia (45) Notoparmelia (16) Relicinopsis (5) Relicina (54) Platismatia (11) Imshaugia aleurites Oropogon (40) 12 Sulcaria (5) Psiloparmelia (13) 14 Everniopsis trulla Psiloparmelioid Hypogymnia (90) Hypogymnioid Pseudevernia (4) 16 Brodoa (3) Arctoparmelia (5) Letharia+Lethariella (17) Tuckermanella (6) Kaernefeltia (2) Ahtiana (3) Arctocetraria (9) Melanelia culbersonii Tuckermannopsis (9) Flavocetraria nivalis Nephromopsis (21) Cetreliopsis (7) Flavocetraria cucullata Masonhalea (2) Cetrarioid Vulpicida (6) Allocetraria (9) 3 Cetraria (15) Usnocetraria oakesiana Cetraria obtusata 15 Cetrariella (4) Dactylina (2) 6 species Melanelia (6) Esslingeriana idahoensis Evernia (10) Omphalodium pisacomense Parmeliaceae Bryoria (51) 11 Alectoria (9) Alectorioid Nodobryoria (3) Pseudephebe (2) Bryocaulon (4) 2 Allantoparmelia (3) 17 Protousnea (8) Phacopsis (10) Anzioid Anzia (34) 10 Pannoparmelia (5) 1 7 Usnea (350) Usneoid Cornicularia normoerica 13 Menegazzia (70) Coelopogon (2) Protoparmelia s.str. (10) Gypsoplacaceae ca 350 species Protoparmelia Miriquidica Lecanora 0.06 substitutions per site Photos © University of Tartu Cladia Cladonia, Metus Cladoniaceae 6-locus phylogeny by Divakar et al. 2015 Study groups: Vulpicida • 6 species worldwide, 3 species with overlapping distributions and habitat, and morphological intermediates © University of Tartu Are morphospecies genetically distinct? V. juniperinus? V. tubulosus? V. lesii? Study groups: Usnea sect. Usnea • Young species complex • Transitional forms and complexity of diagnostic characters Types of soralia Photos © University of Tartu Complicated taxonomy and problematic species delimitation Study groups: Cetrelia • Morphologically uniform but with a characteristic set of lichen metabolites in each species ‘7 Olivetoric acid Imbricaric acid ‘5 OH OH O O O HO HO O O O O © University of Tartu CH3 HO OH ‘3 HO O ‘5 Cetrelia olivetorum Cetrelia monachorum A continuing debate over chemical species concept in Cetrelia Sample preparaon Molecular methods Thin-layer DNA chromatography (TLC) extracFon Polymerase chain reacFon (PCR) Agarose gel preparaon PCR product purificaon Sequencing reacFons Sequencing on ABI 3730xl DNA Analyzer Sample preparaon Thin-layer DNA chromatography (TLC) extracFon Polymerase chain reacFon (PCR) Agarose gel preparaon PCR product purificaon Sequencing reacFons Sequencing on ABI 3730xl DNA Analyzer Lichen sequencing • saprophytic, endophytic, and parasitic fungi live intimately admixed with the lichen mycobiont EPIPHYTES: free living algae, fungi, bacteria Algal cells of lichen photobiont Fungal hyphae of lichen mycobiont ENDOPHYTES: lichen-associated fungi, disnct bacterial communies Cross-secFon photograph by Bill Malcolm 1031bpNGS applicability to lichen barcoding 500bp • Different gene copies in a PCR mixture can produce low quality 10Sanger ng/µL sequences 4 ng/µL • NGS metabarcoding allows identification of a lichen sample even when contaminants dominate in the PCR mixture 1 ng/µL How effectively can pyrosequencing be applied to lichen barcoding? Sample preparaon Thin-layer DNA chromatography (TLC) extracFon Polymerase chain reacFon (PCR) Agarose gel preparaon PCR product purificaon Second PCR Sequencing With fusion primers reacFons Purificaon, Cloning in vector Sequencing on quanFficaon, and plang on ABI 3730xl DNA pooling into agar plates equimolar pools Analyzer Sequencing on GS Roche Sequencer Colony-PCR Sequencing on ABI 3730xl DNA Analyzer Molecular markers I II III IV V nuRNA ITS ITS ITS ITS ITS cistron IGS IGS IGS Bt protein- MCM7 MCM7 MCM7 MCM7 coding RPB1 RPB1 RPB1 RPB2 mitochondrial mtSSU mtSSU Molecular phylogenetic analyses Mul@species coalescent model analyses Single-locus DNA sequence Sequence Recombinaon evoluFonary and Species Species Species detecFon alignment models concatenated delimitaon tree validaon gene trees Barcoding data analyses Consensus sequence approach Cluster Consensus Tree-based idenFficaon Target Quality Clustering sequence = idenFficaon Chimera using NCBI taxon and filtering detecFon at 95% nucleode barcode alignment confirmaon database assignment Key results 1 R1. Incongruences between morphological circumscription of species and DNA based results were found in each study group Ex1.1. Vulpicida Ex1.2. Usnea Ex1.1: Morphospecies Vulpicida juniperinus, V. tilesii and V. tubulosus do not represent genetically distinct species typical V. juniperinus typical V. tubulosus Syn. V. juniperinus V. pinastri (= V. tubulosus) (= V. tilesii) Photos © University of Tartu Vulpicida 3-locus concatenated tree Usnea cavernosa Ex1.2: Only 4 of 17 sect. Usnea morphologically circumscribed species from Usnea sect. Usnea were Usnea silesiaca recovered monophyletic in genetic analyses Usnea wasmuthii Usnea praetervisa Photos © University of Tartu 0.0030 Usnea 6-locus concatenated tree Ex1.2: Only 4 of 17 sect. Usnea morphologically circumscribed species from Usnea sect. Usnea were recovered monophyletic in genetic analyses 4 clusters of two or more species: • Usnea fulvoreagens – U. glabrescens – U. pacificana • Usnea florida – U. subfloridana • Usnea barbata – U. chaetophora – U. dasopoga – U. diplotypus • Usnea barbata – U. intermedia – U. lapponica – U. substerilis 0.0030 Usnea 6-locus concatenated tree Key results 1 R1. Incongruences between morphological circumscription of species and DNA based results were found in each study group Ex1.1. Vulpicida Ex1.2. Usnea ! The level of incongruence is individual for each group Ex1.3. Cetrelia Ex1.3: Chemical species concept in Cetrelia is justified – chemotypes form monophyletic clades with sub-clades usually correlating to morphotypes Densitree of 20,000 B/MCMC gene trees Photos © University of Tartu sanguinea Outgroup monachorum alaskana pseudolivetorum olivetorum cetrarioides japo chic braunsian +delavayana +or nica itae ien tali a s m IMBRICARIC OLIVETORIC R=H: ANZIAIC MICROPHYLLINIC R=H: α-ALECTORONIC R=CH3: PERLATOLIC R=CH3: α-COLLATOLIC Cetrelia 4-locus concatenated densitree Key results 2 R2. Lichen reproductive mode and thallus gross morphology, traditionally with high diagnostic importance, often do not correlate with genetics Ex2.1. Vulpicida Ex2.2. Usnea Ex2.3. Cetrelia Ex2.1: Morphospecies distinguished mainly by the shape of lobes and development of apothecia in the Vulpicida juniperinus complex are not separated genetically Vulpicida juniperinus with broad, dorsiventral lobes Vulpicida tubulosus with terete lobes Photos © University of
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