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SYSTEMATIC STUDY of TRUFFLES in the GENUS Ruhlandiella with the DESCRIPTION of TWO NEW SPECIES from PATAGONIA

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SYSTEMATIC STUDY of TRUFFLES in the GENUS Ruhlandiella with the DESCRIPTION of TWO NEW SPECIES from PATAGONIA SYSTEMATIC STUDY OF TRUFFLES IN THE GENUS Ruhlandiella WITH THE DESCRIPTION OF TWO NEW SPECIES FROM PATAGONIA By NATTAPOL KRAISITUDOMSOOK A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2018 © 2018 Nattapol Kraisitudomsook To Jutharut and Chatchawan Kraisitudomsook (Mom and Dad) ACKNOWLEDGMENTS I wish to thank Dr. Matthew E. Smith for his guidance and for being an incredible advisor, Dr. Rosaria A. Healy for her help with microscopy and for being a wonderful mentor, Dr. Alija B. Mujic for his help with molecular analysis, Dr. Donald H. Pfister for his expert advice in Pezizales systematics, Dr. Eduardo R. Nouhra for his help with the collection permits in South America. I also wish to thank all the herbarium curators and Mr. Ángel Suárez for loaning the fungal specimens, the National Science Foundation for funding this study (grant DEB 1354802), and the Thai Ministry of Science and Technology for the scholarship. Lastly, I thank my parents, family, and friends for their love and emotional support. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS ...............................................................................................................4 LIST OF TABLES ...........................................................................................................................6 LIST OF FIGURES .........................................................................................................................7 LIST OF ABBREVIATIONS ..........................................................................................................8 ABSTRACT .....................................................................................................................................9 CHAPTER 1 INTRODUCTION ..................................................................................................................10 2 MATERIALS AND METHODS ...........................................................................................13 3 RESULTS ...............................................................................................................................17 Phylogenetic Analyses ............................................................................................................17 Taxonomy ...............................................................................................................................18 Ruhlandiella patagonica Kraisit., Pfister, Healy & M. E. Sm., sp. nov. .........................18 Ruhlandiella lophozoniae Kraisit., Pfister, Healy & M. E. Sm., sp. nov. .......................21 Ruhlandiella verrucosa (Warcup & Talbot) Kraisit., Pfister, Healy & M. E. Sm., comb. nov. ....................................................................................................................23 Key to Described Species of Ruhlandiella .............................................................................23 4 DISCUSSION .........................................................................................................................30 LIST OF REFERENCES ...............................................................................................................37 BIOGRAPHICAL SKETCH .........................................................................................................40 5 LIST OF TABLES Table page 3-1 Comparative morphological characteristics of described Ruhlandiella species ................25 6 LIST OF FIGURES Figure page 3-1 Phylogram of Ruhlandiella and related taxa (Pezizales) obtained from Maximum Likelihood analysis of four concatenated genes (28S rDNA, RPB1, RPB2, ß-tub).. ........26 3-2 Phylogram of Ruhlandiella species obtained from the ITS rDNA alignment based on Maximum Likelihood (ML) analysis.. ...............................................................................27 3-3 Morphology of Ruhlandiella patagonica...........................................................................28 3-4 Morphology of Ruhlandiella lophozoniae. ........................................................................29 4-1 Morphological comparison of Sphaerosoma fuscescens and Ruhlandiella berolinensis. .......................................................................................................................36 7 LIST OF ABBREVIATIONS C Celsius DNA Deoxyribonucleic acid MYA Million years ago r Ribosomal RNA Ribonucleic acid 8 Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science SYSTEMATIC STUDY OF TRUFFLES IN THE GENUS Ruhlandiella WITH THE DESCRIPTION OF TWO NEW SPECIES FROM PATAGONIA By Nattapol Kraisitudomsook May 2018 Chair: Matthew E. Smith Major: Plant Pathology Ruhlandiella is a genus of exothecial fungi in the order Pezizales. Ascomata of exothecial fungi typically lack a peridium and are covered with a hymenial layer instead. Ruhlandiella have non-operculate asci and highly ornamented ascospores. The genus was first described by Hennings in 1903 based on Ruhlandiella berolinensis from the Australian greenhouse in a German botanical garden. R. berolinensis was later identified as an ectomycorrhizal fungus associated with Eucalyptus trees. Since then, mycologists have uncovered Ruhlandiella species from elsewhere, including Australia, Spain, Italy, and the U.S.A. Currently, there are four recognized species in this genus: R. berolinensis, R. peregrina, R. reticulata and R. truncata. All were found near Eucalyptus or Melaleuca trees of Australasian origin. Recently, we discovered two new species of Ruhlandiella in Nothofagaceae forests in South America. They regularly form mitospore mats directly on soil across Patagonia. Here, we formally describe these new species and construct the phylogeny of Ruhlandiella and its related taxa using a multi-locus phylogenetic analysis. Furthermore, we provide the identification key to accepted species of Ruhlandiella and also revise our current understanding of Ruhlandiella taxonomy. 9 CHAPTER 1 INTRODUCTION Ruhlandiella (Pezizaceae) is a genus of exothecial fungi in the order Pezizales. Exothecial fungi are essentially ‘inside-out’ truffles, i.e. their ascomata lack a peridium and are instead covered with a hymenial layer (Weber et al. 1997). Like many truffles, species of Ruhlandiella have highly ornamented ascospores and their asci lack opercula (Dissing and Korf 1980). The genus was first described by Hennings (1903) who described the type species Ruhlandiella berolinensis, from a Berlin Botanical Garden in Germany (Dissing and Korf 1980). This species was later identified as an ectomycorrhizal symbiont of Eucalyptus trees; it fruited abundantly after wildfires and formed ectomycorrhizae on seedlings in greenhouse studies (Warcup 1990). Dissing and Korf (1980) indicated that the holotype of R. berolinensis was lost, and thus designated a collection from a eucalypt plantation in the Canary Islands as a neotype (CUP-MM- 1230). Since then, Ruhlandiella specimens have been collected in Australia, Spain, Italy, and the U.S.A (Dissing and Korf 1980, Galan and Moreno 1998, Rubio et al. 2010, Lantieri et al. 2012). All of the collections were found near Eucalyptus, Melaleuca or other ectomycorrhizal Myrtaceae trees of Australasian origin. It has been suggested that the genus Muciturbo is a synonym of Ruhlandiella, but this claim has not been addressed using molecular phylogenetic data (Hansen et al. 2005). Muciturbo was described by Warcup and Talbot (1989) based on the type species M. reticulatus, which was discovered under Eucalyptus trees in South Australia. Three species of Muciturbo were described: M. reticulatus, M. truncatus, and M. verrucosus. Rubio et al. (2010) concluded that Muciturbo is a synonym of Ruhlandiella based on the morphological similarities between the two genera (e.g. the exothecial ascomata, amyloid reaction of the asci, spore ornamentation, 10 paraphyses with gelatinous sheathes, and paraphyses that exceed the asci significantly in length). An Australian specimen identified as a Muciturbo sp. was also determined to be closely related to R. berolinensis in a phylogeny by Healy et al. (2013). Several other taxa have been placed in the genus Ruhlandiella. For instance, Dissing and Korf (1980) considered Ruhlandiella hesperia to be synonyms of R. berolinensis. Hirsch (1983) transferred Boudiera parvispora, an apothecial fungus described from India, to the genus Ruhlandiella. Rouppert (1909) considered Sphaerosoma fuscescens to be identical to R. berolinensis. None of these opinions have been confirmed with molecular analyses. In 1905-1906, during his expedition in Nothofagaceae-dominated forests in South America, Dr. Roland Thaxter found Ruhlandiella-like ascomata that he referred to as the “pearly livid white fungus hypogeous” (Halling 1981). Healy et al. (2013) reported finding mitotic spore mats of Ruhlandiella from Nothofagaceae-dominated forests across Patagonia. These mitotic spore mats were morphologically similar to the Muciturbo anamorphs drawn by Warcup and Talbot (1989). More recently, we discovered several new collections of gelatinous exothecial fungi in Nothofagaceae forests in South America. These fungi also match the general morphology of Ruhlandiella, as well as Thaxter’s description of them as a pearly, livid, white hypogeous fungus, but are distinct from all known species. Here, we critically review the taxonomy
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