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Multi-Gene Phylogenies Indicate Ascomal Wall Morphology Is a Better

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Multi-Gene Phylogenies Indicate Ascomal Wall Morphology Is a Better Molecular Phylogenetics and Evolution 35 (2005) 60–75 www.elsevier.com/locate/ympev Multi-gene phylogenies indicate ascomal wall morphology is a better predictor of phylogenetic relationships than ascospore morphology in the Sordariales (Ascomycota, Fungi) Andrew N. Miller a,¤, Sabine M. Huhndorf b a Illinois Natural History Survey, Center for Biodiversity, 607 E. Peabody Dr., Champaign, IL 61820, USA b The Field Museum of Natural History, Botany Department, 1400 S. Lake Shore Dr., Chicago, IL 60605-2496, USA Received 3 December 2003; revised 20 October 2004 Abstract Ascospore characters have commonly been used for distinguishing ascomycete taxa, while ascomal wall characters have received little attention. Although taxa in the Sordariales possess a wide range of variation in their ascomal walls and ascospores, genera have traditionally been delimited based on diVerences in their ascospore morphology. Phylogenetic relationships of multiple representa- tives from each of several genera representing the range in ascomal wall and ascospore morphologies in the Sordariales were esti- mated using partial nuclear DNA sequences from the 28S ribosomal large subunit (LSU), -tubulin, and ribosomal polymerase II subunit 2 (RPB2) genes. These genes also were compared for their utility in predicting phylogenetic relationships in this group of fungi. Maximum parsimony and Bayesian analyses conducted on separate and combined data sets indicate that ascospore morphol- ogy is extremely homoplastic and not useful for delimiting genera. Genera represented by more than one species were paraphyletic or polyphyletic in nearly all analyses; 17 species of Cercophora segregated into at least nine diVerent clades, while six species of Podos- pora occurred in Wve clades in the LSU tree. However, taxa with similar ascomal wall morphologies clustered in Wve well-supported clades suggesting that ascomal wall morphology is a better indicator of generic relationships in certain clades in the Sordariales. The RPB2 gene possessed over twice the number of parsimony-informative characters than either the LSU or -tubulin gene and conse- quently, provided the most support for the greatest number of clades. 2005 Elsevier Inc. All rights reserved. Keywords: Ascomycota; Bayesian inference; -Tubulin; LSU; Morphological characters; RPB2; Phylogenetics; Sordariales; Systematics 1. Introduction decaying wood, leaf litter, and soil (Lundqvist, 1972). The Sordariales also was one of the most taxonomically The Sordariales is one of the most economically and diverse orders being comprised of 114 genera divided ecologically important groups within the ascomycetes in among 10 families (Eriksson and Hawksworth, 1998; that it contains species of Chaetomium, which are Eriksson et al., 2004), but recently has been reduced to responsible for the destruction of paper and fabrics, and ca. 35 genera within three families, the Chaetomiaceae, the “fruit Xies” of the fungal world (i.e., Neurospora Lasiosphaeriaceae, and Sordariaceae (Huhndorf et al., crassa, Podospora anserina, and Sordaria Wmicola). Taxa 2004). Since only one of these families (Sordariaceae) within the order occur worldwide as saprobes on dung, was shown to be monophyletic by Huhndorf et al. (2004), families within the Sordariales will not be further discussed. ¤ Corresponding author. Fax: +1 217 333 4949. The Sordariales is one of several orders in the Class E-mail address: [email protected] (A.N. Miller). Sordariomycetes (Eriksson et al., 2004). Taxa in the 1055-7903/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2005.01.007 A.N. Miller, S.M. Huhndorf / Molecular Phylogenetics and Evolution 35 (2005) 60–75 61 Sordariomycetes (historically known as pyrenomyce- Ascomal wall morphology also has been suggested as tes) usually form minute fruiting bodies ( D ascomata) an alternative means of delimiting certain genera within containing hymenial layers commonly composed of this group (Lundqvist, 1972) (Fig. 2). All members of sterile hyphae intermixed among asci (with single wall Bombardia and Bombardioidea possess a similar ascomal layers) possessing ascospores (Alexopolous et al., 1996). wall referred to as a bombardioid wall, which contains a Few morphological characters exist with which to putatively stromatic ( D arising from vegetative hyphae) delimit taxa in the Sordariomycetes most likely due to gelatinized layer composed of interwoven hyphae their small stature and simple structure. Taxa within (Lundqvist, 1972) (Fig. 2C). Three other genera (Arnium, the Sordariomycetes have traditionally been distin- Cercophora, and Podospora) also contain species that guished based on characters of the ascomata and possess a similar gelatinized layer in their ascomal wall, ascospores, although centrum and ascus morphologies but since the wall is non-stromatic, it is termed pseudo- also have been used at higher taxonomic levels (Barr, bombardioid (Miller, 2003) (Figs. 2A and B). However, 1990; Luttrell, 1951; Parguey-Leduc and Janex-Favre, all of these species have been placed into diVerent genera 1981). Ascomata can have single- or multi-layered walls based primarily on diVerences in their ascospore mor- and may possess various types of outside covering such phologies (Fig. 1). Certain species of Cercophora and as tomentum, hairs, or setae. Although considerable Lasiosphaeria also have been placed into separate genera variation in ascomal wall morphology exists in the based on diVerences in their ascospore morphologies Sordariomycetes, its potential use in systematics has even though they possess similar three-layered ascomal seldom been recognized (Jensen, 1985). Several work- walls in which the outer layer is composed of hyphae ers, however, have noted similarities in ascomal wall that form a tomentum (Fig. 2D). Finally, certain species characters among taxa (von Arx et al., 1984; Barr, 1978; of Podospora possess ascomata with outer wall layers Carroll and Munk, 1964; Jensen, 1985; Lundqvist, that form swollen protruding cells or agglutinated hairs 1972). (Fig. 2E), and some of these species have been trans- Genera within the Sordariales have been delimited ferred into a separate genus, Schizothecium (Lundqvist, primarily on diVerences in their ascospore morphology 1972). These genera, which contain species that possess (Lundqvist, 1972) (Fig. 1). While ascospore morphology ascomata with obvious morphological diVerences in varies little within a genus, ascospores among genera in their ascomal walls, are the focus of this paper. Addi- the Sordariales range from a cylindrical, hyaline asco- tional genera in the Sordariales (e.g., Apiosordaria, Jugu- spore in Lasiosphaeria (Fig. 1A) to an ellipsoidal, brown lospora, and Triangularia), which contain species that ascospore in Sordaria (Fig. 1I). Intermixed between these possess ascomata with morphologically simple ascomal two extremes are many genera which possess two-celled walls, require further study and will be treated in future ascospores with cylindrical to ellipsoidal, brown cells studies. Our study is the Wrst to evaluate ascomal wall and diVerent degrees of cylindrical to triangular (often characters for their phylogenetic potential in delimiting basal), hyaline cells (Figs. 1B–G) (Lundqvist, 1972). Sev- certain genera in the Sordariales. eral earlier workers (Boedijn, 1962; Chenantais, 1919; Several nuclear and mitochondrial ribosomal and Lundqvist, 1972; Munk, 1953) hypothesized that asco- protein-coding genes have been employed for assessing spore evolution within this group may have occurred phylogenetic relationships of Wlamentous ascomycetes. along this continuum either through the gain or loss of a Nuclear ribosomal genes such as 18S small subunit hyaline cell, resulting in either Lasiosphaeria or Sordaria (SSU) and 28S LSU are commonly used due to their being the derived genus. ease in ampliWcation resulting from their high copy num- Fig. 1. Ascospores of representative genera in the Sordariales. (A) Lasiosphaeria. (B) Cercophora. (C) Podospora. (D) Apiosordaria. (E) Triangularia. (F) ZopWella. (G) Jugulospora. (H) Bombardioidea. (I) Sordaria. Ascospore evolution has been hypothesized to have occurred through the loss (A ! I) or gain (I ! A) of a hyaline tail resulting in either Sordaria or Lasiosphaeria being the derived genus. Ascospores not to scale. 62 A.N. Miller, S.M. Huhndorf / Molecular Phylogenetics and Evolution 35 (2005) 60–75 Fig. 2. Ascomal walls occurring in members of the Wve wall clades (A–E); outer layer to the right. (A) Pseudo-bombardioid wall (Podospora Wmiseda). (B) Pseudo-bombardioid wall (Cercophora scortea). (C) Bombardioid wall (Bombardioidea anartia). (D) Three-layered wall with outer layer of hyphae forming tomentum (Lasiosphaeria ovina). (E) Wall with agglutinated hairs (Schizothecium vesticola). Ascomal walls not to scale. ber and the availability of numerous universal primers The primary purpose of this study was to test whether (Vilgalys and Hester, 1990; White et al., 1990). Most ascospore morphology is phylogenetically informative for studies utilize the Wrst 1100 bp of the 5Ј end of LSU, predicting generic relationships within the Sordariales which contains three variable domains. Nuclear protein- using a multi-gene approach. Multiple species, which pos- coding genes such as -tubulin and RPB2 are increas- sess the range of ascospore morphologies known to occur ingly being used in ascomycete phylogenetic studies in the order, were sampled from each of several genera. To incorporating multiple,
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