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Doctor of Philosophy Botany TAXONOMY, DIVERSITY AND PHYLOGENY OF SOME GASTEROID FUNGI FROM PAKISTAN A dissertation submitted to the University of the Punjab in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY IN BOTANY BY NOUSHEEN YOUSAF DEPARTMENT OF BOTANY UNIVERSITY OF THE PUNJAB LAHORE, PAKISTAN AUGUST, 2014 Dedicated to My loving Mother & Father Without whom none of my success would be possible TABLE OF CONTENTS Chapter Title Page No. no. Summary i Acknowledgements iv List of Plates vi List of Tables Ix List of Figures x 1.0 INTRODUCTION 1 2.0 AIMS AND OBJECTIVES 6 3.0 MATERIALS AND METHODS 7 3.1 Description of sampling sites 7 3.2 Collection of samples 7 3.3 Assigning labels to samples 7 3.4 Drying and preservation of sporocarps 8 3.5 Morpho–anatomical characterization 8 3.5.1 Observations of spores, capillitium and paracapillitium 8 3.5.2 Observations of peridium 8 3.6 Molecular analyses 9 3.6.1 Genomic DNA extraction 9 3.6.2 PCR, Agarose Gel Electrophoresis and Sequencing 9 3.7 Analyses of molecular data 10 3.7.1 Editing of sequences and BLAST analysis 10 3.7.2 Phylogenetic analyses 10 3.8 Analyses of Diversity 10 4.0 RESULTS 13 4.1 Taxonomy 14 4.1.1 Taxa belonging to Agaricaceae 14 4.1.2 Taxa belonging to Nidulariaceae 218 4.1.3 Taxa belonging to Phelloriniaceae 225 4.1.4 Taxa belonging to Diplocystaceae 228 4.1.5 Taxa belonging to Rhizopogonaceae 233 41.6 Taxa belonging to Sclerodermataceae 241 4.1.7 Taxa belonging to Geastraceae 265 4.1.8 Taxa belonging to Phallaceae 299 4.1.9 Taxa belonging to Russulaceae 309 4.2 Taxonomy of Herbarium Gasteroid Taxa 311 4.3 Phylogeny of Gasteroid Fungi 333 4.4 Diversity of Gasteroid Fungi 369 4.4.1 Diversity of gasteroid fungi in different forests 369 4.4.2 Species Richness (SR) of sampling sites 371 4.4.3 Taxonomic diversity of gasteroid fungi 371 4.4.4 Species Frequency (SFl) of gasteroid fung 372 5.0 DISCUSSION 388 6.0 REFERENCES 430 i SUMMARY This investigation deals with taxonomy, phylogeny and diversity of gasteroid fungi from different areas of Pakistan. Sampling was carried out from the regions with varying climates, forests types and altitudes. During this study, 228 specimens were collected and identified using morphological and molecular techniques, comprising 101 different species of gasteroid fungi belonging to 20 genera, 9 families and 5 orders. Among these, fifty taxa (50) seem previously undescribed and twenty four (24) are new records for Pakistan. Total gasteroid fungal taxa of order Agaricales studied in this investigation are seventy (70) represented by three families, i.e. Agaricaceae, Nidulariaceae and Phellorineaceae. Out of these, thirty eight (38) taxa seem new to science (17 of Lycoperdon, 15 of Bovista, 3 of Calvatia, 1 of Arachnion, Cyathus, and Tulostoma each) and sixteen (16) are first time reported from Pakistan. Agaricaceae includes one (1) species of Arachnion (A. olivoflavus), one (1) species of Battarrea (B. phalloides), twenty four (25) of Bovista (B. aestivalis, B. ahmadii nom. prov., B. areolata nom. prov., B. ayubiensis nom. prov., B. brunnescenta nom. prov., B. bovistoides, B. concinna, B. flavescens nom. prov., B. flavum nom. prov., B. fusca, B. himalaica, B. kreiselli nom. prov., B. lahorensis nom. prov., B. levisspora nom. prov., B. longispora, B. minima nom. prov., B. nigrescens var. rectapedicellata nom. prov., B. oblongispora, B. pakistanica nom. prov., B. pesudonigrescens nom. prov., B. plumbea, B. promontori, B. trachyspora and B. viridispora nom. prov., Bovista sp. (BPK92), four (4) of Calvatia (C. cyathiformis var. fragilis nom. prov., C. desosaiensis nom. prov., C. lilacina, C. pseudocyathiformis nom. prov.), 1 of Disciseda (D. hyalothrix), twenty eight (28) of Lycoperdon (L. albiceratum nom. prov., L. altimontanum, L. aurea-bruneum nom. prov., L. curtisii var. ovalisporum nom. prov., L. dermoxanthum var. album nom. prov., L. dermoxanthum var. flavum., L. excipuliforme, L. gilgitii nom. prov., L. japonicum, L. lahorense nom. prov., L. lahorense var. parvasporum nom. prov., L. lignum-bruneum nom. prov., L. lineum nom. prov., L. mammiforme, L. mammiforme var. magnasporum, L. molle, L. nigrescens, L. niveum, L. olivoflavum nom. prov., L. parvasporum nom. prov., L. perlatum, L. pratense var. flavum nom. prov., L. pseudoniveum nom. prov., L. pyriforme, L. sharanense nom. prov., L. sclerocystis nom. prov., L. utriforme, and Lycoperdon sp. (LPK74), one (1) of Montagnea (M. arenarea), 1 of Podaxis (P. pistillaris), five (5) of ii Tulostoma (T. fimbriatum, T. morenoii nom. prov., T. squamosum, Tulostoma sp. 1 (TPK6), Tulostoma sp. 2 (TPK4). Nidulariaceae includes two (2) of Cyathus (C. olla, C. pakistanicus nom. prov.), and Phellorineaceae includes one (1) species of Phellorinia (P. herculeana). Gasteroid fungal taxa of order Boletales are thirteen (13) belonging to three families, i.e. Diplocystaceae, Rhizopogonaceae, and Sclerodermataceae. Among these, three (3) taxa seem new to science (2 of Rhizopogon and 1 of Pisolithus) and five (5) are new records from Pakistan. Diplocystaceae includes one (1) species of Astraeus (A. hygrometricus). Rhizopogonaceae includes three (3) species of Rhizopogon (R. flavescens nom. prov., R. himalayensis nom. prov., R. roseolus). Sclerodermataceae includes six (6) species of Scleroderma (S. areolatum, S. bovista, S. chevelerii, S. dictyosporum, S. fuscum, Scleroderma sp. SPK21), 3 species of Pisolithus (P. flavescens, P. tinctorious, Pisolithus sp. PPK16). Among twelve (12) gasteroid taxa of geastrales belong to one family, geastraceae which includes ten (10) species of Geastrum (G. fimbriatum, G. himlayensis nom. prov., G. lycogalopsus nom. prov., G. pakistanicus nom. prov., G. parvulus nom. prov., G. patulus nom. prov., G. pseudolimbatum, G. pseudosaccatum nom. prov., P. saccatum, G. triplex), one (1) of Myriostoma (M. coliforme), one (1) of Radiigera (R. ayubiensis nom. prov.). In this family, seven (7) species are presented here as new and one (1) taxon is first time being reported from Pakistan. Phallales is represented by phallaceae in this study. It includes five (5) species of Phallus (P. ahmadii nom. prov., P. galericulatus, P. hadriani, P. roseus, and P. rubicundus). Among these, one (1) is proposed as a new species, and two (2) are new records for Pakistan. One sequestrate fungus Russula i.e. R. pakistanica nom. prov., belonging to Russulaceae of Russulales is also included in this study and seems previously undescribed. Some gasteroid specimens were taken as a loan from LAH herbarium, Pakistan, morphological descriptions of which are given at the end. iii Taxonomy is correlated with phylogenetic analysis of each genus based on ITS-nr- DNA region. Diversity of gasteroid species studied in different forests is also given. During this investigation, maximum diversity of gasteroid species was found in Himalayan moist temperate forests. Published work during this investigation has been appended as Annexure. iv ACKNOWLEDGEMENTS I would like to pay my heartiest gratitude to my respected teacher and PhD supervisor, Dr. Abdul Nasir Khalid for his continuous guidance, support, kindness and advices throughout the duration of my research work. I am thankful to Prof. Dr. Muhammad Saleem, Chairman, Department of Botany, and Prof. Dr. Khan Rass Masood, Ex-Chairman, for providing me conducive environment and facilities for carrying out this research project. Thanks are also due to Prof. Donald H. Pfister (Harvard University, Cambridge, MA, USA) for providing me excellent opportunity to work in his lab under his supervision, allowing me to use library and herbarium facilities for six months. I am indebted to Higher Education Commission of Pakistan for funding this research project and awarding me the scholarships under indigenous 5000 fellowships (Batch IV) and IRSIP (International Research Support Initiative Program). I am thankful to my foreign collaborators, Prof. Hanns Kreisel (Germany), Prof. F. D. Calonge (Spain), Prof. G. Moreno (University of Alcalá, Madrid, Spain), Dr. Scott. T. Bates (USA), Ms. Larissa Trierveiler-Pereira (Brazil), Dr. Takamichi Orihara (Curator, Kanagawa Prefectural Museum of Natural History, Japan) for their help, valuable comments and suggestions for improvement of my work and publications. I must thank Genevieve E. Tocci (Curatorial Assistant, Harvard University Herbaria) for helping me getting access to gasteroid collections. Thanks are also due to Dr. Abdul Rehman Niazi (Deptt. of Botany, PU, Lahore) and Dr. Najam-ul-Sehar Afshan (Center for Undergraduate Studies, PU, Lahore) for their moral support and assistance in field tours. I extend my thanks to Dr. Katherine Lobuglio for her guidance and supervision in molecular work at Pfister lab, Harvard University, USA. I sincerely thank Prof. Meredith Blackwell (Radcliffe Institute for Advanced Study, Harvard University, USA), Dr. Rosane Healy (Postdoctoral Fellow, Pfister Lab. USA), Dr. Teresa Iturriaga (Venezuela), Mr. Danny Haelewaters, and Mr. Jason for their affection and simulating discussions during my work at Harvard University. v I highly acknowledge my friends especially Ms. Syeda Bint-e-Zahira, Ms. Aamna Ishaq, and Ms. Sana Jabeen for always being there for me. I also acknowledge all my lab fellows especially Dr. Muhammad Fiaz, Dr. Abdul Razaq, Dr. Sobia Ilyas, Dr. Samina Sarwar, Dr. M. Hanif, Ms. Malka Saba, and Ms. Tasleem Javaid for their cheerful company. This project would have impossible without the prayers and support of my parents. I am thankful to my sisters, brothers, brother in law, and all my family for their endless support and unconditional love. Nousheen Yousaf vi LIST OF PLATES Plate no. Title Page no. 1–3 Morphology of Arachnion olivoflavus 15–17 4–5 Morphology of Battarrea phalloides 19–20 6–7 Morphology of Bovista areolata 22–23 8–10 Morphology of B. bovistoides 25–27 11–13 Morphology of B. fusca 29–31 14–16 Morphology of B. kreiselli 33–35 17–18 Morphology of B. nigrescens var. rectapedicellata 37–38 19–20 Morphology of B. plumbea 41–42 21–22 Morphology of B.
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