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Convergent Evolution of Sequestrate Forms in Amanita Under Mediterranean Climate Conditions

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Convergent Evolution of Sequestrate Forms in Amanita Under Mediterranean Climate Conditions University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications in Food Science and Technology Food Science and Technology Department 2010 Convergent evolution of sequestrate forms in Amanita under Mediterranean climate conditions Alfredo Justo Clark University, [email protected] Ingo Morgenstern Clark University Heather E. Hallen-Adams University of Nebraska at Lincoln, [email protected] David S. Hibbett Clark University Follow this and additional works at: https://digitalcommons.unl.edu/foodsciefacpub Part of the Food Science Commons Justo, Alfredo; Morgenstern, Ingo; Hallen-Adams, Heather E.; and Hibbett, David S., "Convergent evolution of sequestrate forms in Amanita under Mediterranean climate conditions" (2010). Faculty Publications in Food Science and Technology. 72. https://digitalcommons.unl.edu/foodsciefacpub/72 This Article is brought to you for free and open access by the Food Science and Technology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in Food Science and Technology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Mycologia, 102(3), 2010, pp. 675–688. DOI: 10.3852/09-191 # 2010 by The Mycological Society of America, Lawrence, KS 66044-8897 Convergent evolution of sequestrate forms in Amanita under Mediterranean climate conditions Alfredo Justo1 cally intermediate between gasteroid and their agar- Ingo Morgenstern icoid/boletoid ancestors. The advantage of these Biology Department, Clark University, 950 Main Street, forms against loss of moisture under unfavorable Worcester, Massachusetts 01610 conditions (extreme drought or cold) has been Heather E. Hallen-Adams proposed as a main factor favoring their evolution Department of Plant Biology, Michigan State (Thiers 1984). It also has been postulated that natural University, 166 Plant Biology Laboratories, East selection would act against intermediate (secotioid) Lansing, Michigan 48824-1312 forms because they lack the dispersal advantages of the agaricoid and gasteroid forms (via air and animals David S. Hibbett respectively) and are only partially adapted to Biology Department, Clark University, 950 Main Street, Worcester, Massachusetts 01610 seasonal xeric conditions (Bruns et al. 1989). Peint- ner et al. (2001) showed that it also is possible that successfully adapted, stable, sequestrate (secotioid Abstract: The systematic position of secotioid (Tor- and gasteroid) forms tend to radiate but they can rendia) and gasteroid (Amarrendia) forms within the radiate only into species with the same basidiome type agaricoid Amanita lineage (Agaricales, Basidiomyco- or a further reduced type. This study concerns the ta) was studied with molecular (nLSU, ITS) data. evolution of secotioid (Torrendia)andgasteroid Secotioid and gasteroid forms occur in four indepen- (Amarrendia) forms within the Amanitaceae (Agar- dent clades nested within agaricoid forms. One clade icales). corresponds to the secotioid T. pulchella from The secotioid genus Torrendia was created by southern Europe and northern Africa. The others Bresadola (1902) to accommodate a small, whitish, correspond to Torrendia and Amarrendia species from volvate and stipitate gasteromycete collected in Australia. Mediterranean climatic conditions are Portugal by C. Torrend. After a careful study of the postulated as a force driving the convergent evolution morphology and development of Torrendia pulchella of these secotioid and at least one of the gasteroid Bres. a close relationship with the agaricoid genus forms in geographically distant areas. Species former- Amanita Pers. was postulated (Malenc¸on 1955, Bas ly placed in Torrendia and Amarrendia are transferred 1975). Miller and Horak (1992) described a second to Amanita. A new species of Torrendia from Australia species of Torrendia from Western Australia, T. was discovered during the revision of the collections arenaria O.K. Mill. & E. Horak, very similar in its originally identified as T. arenaria and is described external morphology to T. pulchella but differing in here as Amanita pseudoinculta. spore shape and size, presence of sclerobasidia, Key words: Amarrendia, ITS, nLSU, phylogeny, absence of clamp connections and different mycor- sequestrate forms, Torrendia rhizal partners. A variant with yellowing flesh was given the name T. arenaria f. lutescens O.K. Mill & E. Horak. Bougher (1999) described two new species INTRODUCTION also from Western Australia, T. grandis Bougher, Secotioid and gasteroid forms have evolved indepen- mainly characterized by the relatively big basidiomes, dently several times from agaricoid/boletoid ances- and T. inculta Bougher with a gleba that fragments tors in different groups of fungi (Hibbett 2007), such during stipe elongation. Both species have clamp as Boletales (Binder and Hibbett 2006), Russulales connections and lack sclerobasidia, which separates (Eberhardt and Verbeken 2007), Agaricales (Peintner them from T. arenaria, and possess ellipsoid to et al. 2001) and Phallomycetidae (Hosaka et al. 2006). oblong spores, which separates them from T. Gasteroid fungi such as false truffles, puffballs and pulchella. stinkhorns are highly modified for nonballistosporic Torrendia has a puzzling distribution pattern; one dispersal, whereas secotioid forms are morphologi- species (T. pulchella) occurs in the Mediterranean Basin, including the Iberian Peninsula (Spain, Portu- gal), northern Africa (Morocco, Algeria), southern Submitted 29 Jun 2009; accepted for publication 17 Oct 2009. France, Sardinia (Italy) and Turkey, with putative 1 Corresponding author. E-mail: [email protected] mycorrhizal partners such as Pinus, Quercus and 675 676 MYCOLOGIA Cistus (Neville and Poumarat 2004), and the other MATERIALS AND METHODS three taxa (T. arenaria, T. grandis, T. inculta) occur in Western Australia with putative mycorrhizal part- Sequences.—Thirty-six new sequences (nuclear ribosomal RNA large subunit [nLSU] and the internal transcribed ners such as Eucalyptus, Allocasuarina and Leptosper- spacers [ITS]) were generated from herbarium material of mum (Miller and Horak 1992, Bougher 1999). With T. pulchella, T. arenaria, T. inculta, T. grandis and this disjunct distribution in both hemispheres a Amarrendia oleosa. Sequences generated from an unidenti- monophyletic Torrendia would imply that the group fied herbarium collection (H909), possibly belonging to is ancient or that there has been long distance Amarrendia, also were included in the study. The nLSU data dispersal, either by natural or anthropogenic means. for Amarrendia grandispora came from Hallen et al. (2004). The gasteroid genus Amarrendia Bougher & T. A total of 167 sequences of Amanita, two of Limacella and Lebel was created to include species with these one of Torrendia pulchella, the majority coming from the characteristics: white to cream peridium and gleba, works of Weiß et al. (1998), Drehmel et al. (1999) and basidiome flesh fragile and minutely granular; gleba Zhang et al. (2004), were retrieved from GenBank (TABLES I, II). loculate; spores smooth, thin-walled, hyaline, non- Approximately 0.05 g each herbarium collection were amyloid and nondextrinoid, with a large oil droplet, ground in liquid nitrogen, and DNA was extracted with 3% broadly ellipsoid and with a broad apiculus; context SDS extraction buffer; DNA then was isolated by the trama composed of inflated and hyphal elements sequential addition of phenol chloroform and chloro- intermixed. Bougher and Lebel (2002) described form-isoamyl alcohol; finally, isopropyl alcohol and 3M three new species of Amarrendia (viz. Amarrendia sodium acetate were added to precipitate the DNA, which oleosa Bougher & T. Lebel, Amarrendia nemoribus was washed with 70% EtOH and resuspended in sterile Bougher & T. Lebel and Amarrendia peridiocrystalia water. A portion of the nLSU and the complete ITS1 + 5.8 + Bougher & T. Lebel) and recombined two species ITS2 (ITS) regions were amplified by PCR with fungal formerly placed in Alpova (Amarrendia grandispora primers LR0R and LR5 and ITS1F and ITS4 respectively [G.W. Beaton, Pegler & T.W.K. Young] Bougher & T. (Gardes and Bruns 1993, http://www.biology.duke.edu/ fungi/mycolab/primers.htm). Amplification products were Lebel and Amarrendia lignicolor [G.W. Beaton, Pegler sequenced with ABI PRISM Big Dye Terminator Cycle & T.W.K. Young] Bougher & T. Lebel ). The genus is Sequencing Ready Reaction reagents with primers LR0R distributed in Western Australia, Victoria and Tasma- and LR5 (with additional LR3R and LR3 for some samples) nia with putative mycorrhizal partners such as and ITS1F and ITS4. Sequencing was carried out on an ABI Eucalyptus, Allocasuarina, Acacia and Gastrolobium. 3130 Genetic Analyzer. Raw data were processed with Amarrendia was proposed to occupy a systematic Sequencher 4.7 (GeneCodes, Ann Arbor, Michigan). The position within a complex of related taxa that also ITS region of all the Australian taxa of Torrendia and incorporates Torrendia and Amanita mainly based in Amarrendia showed a high level of intragenomic variability, the presence of inflated elements in the trama and so the PCR products were cloned with the TOPO TA the characteristics of the spores (Bougher and Lebel Cloning Kit (Invitrogen, Carlsbad, California) following the 2002) manufacturer’s instructions. Previous molecular work has shown that T. pul- Alignment.—Sequences were aligned with MAFFT (http:// chella is a secotioid derivative of Amanita
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