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Department of Plant Biology, University of Minnesota, Saint Paul, Minnesota 55108
Kelly A. Josephsen
Imaging Center, College of Biological Sciences, University of Minnesota, Saint Paul, Minnesota 55108
Thomas S. Jenkinson
Esther G. McLaughlin
David J. McLaughlin
Department of Plant Biology, University of Minnesota, Saint Paul, Minnesota 55108
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Ultrastructure of the septal pore apparatus and nuclear division of Auriscalpium vulgare (Russulales) was examined with freeze substitution and is presented for inclusion in the AFTOL Structural and Biochemical Database (http://aftol.umn.edu). Previously unreported septal characters for the Russulales (Agaricomycotina) were observed: Septa of the hymenophore had bell-shaped perforated septal pore caps that may extend along the septum and a zone of organelle exclusion surrounded the septal pore apparatus. Metaphase I of meiosis and metaphase of mitosis were similar. Globular spindle pole bodies with electron-opaque inclusions were set within polar fenestrae of the nuclear envelope. The nuclear envelope was mostly intact with occasional gaps. Fragments of endoplasmic reticulum were present near the spindle pole bodies but did not form a polar cap. Structural characters may distinguish one or more clades of the Agaricomycotina and provide additional signal in phylogenetic analyses.
Key words: basidiocarp, basidium, cytology, informatics, phylogeny, sporocarp
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Kimbrough 1994, McLaughlin et al 1995b, Lutzoni et al 2004). Improvements in chemical fixation methods for fungal ultrastructure resulted in better visualization of nuclear division and the spindle pole body (SPB) (see Girbardt 1978). Freeze substitution (FS) protocols were particularly helpful for observing the condition of the nuclear envelope during stages of division (Heath and Rethoret 1982; Kanbe and Tanaka 1985; Tanaka and Kanbe 1986; Berbee and Wells 1988; Berbee et al 1991; Swann and Mims 1991; O’Donnell 1992, 1994; Lü and McLaughlin 1994; Frieders and McLaughlin 1996; Swann et al 1999). Such characters have supplemented or been used as the basis of phylogenetic analyses (Heath 1986, McLaughlin et al 1995a, Swann et al 1999).
The Structural and Biochemical (SB) Database for the Fungi (http://aftol.umn.edu) (Celio et al 2006) associated with the Assembling the Fungal Tree of Life (AFTOL) project is a searchable database containing data primarily from previous ultrastructural studies that have been coded for phylogenetic analyses. Many traits were selected for inclusion in the SB Database, with data on septum/septal pore apparatus and nuclear division, including spindle pole body forms and cycles, among the first to be entered. The distribution of ultrastructural studies is uneven across taxonomic groups, hindering investigations of evolutionary relationships and character evolution. To fill in gaps we investigated taxa and collected data from clades and cell types that are poorly represented within the SB Database. This study presents septal pore and nuclear division data from Auriscalpium vulgare in the Russulales (Agaricomycotina), a species that fruits in the laboratory. This taxon is represented in the AFTOL Molecular Database (http://www.aftol.org) by sequence data for the nuclear internal transcribed spacer regions and the large and small subunits of the ribosomal DNA. Ultrastructural images of septa of some species in the Russulales have been published (Besson and Froment 1968, Flegler et al 1976, Patrignani and Pellgrini 1986, Keller 1997); however low magnification and/or nonmedian sections prevented data entry for many septal characters. In the Russulales only Hericium coralloides (Flegler et al 1976) and Artomyces pyxidatus (= Clavicorona pyxidata) (M Berbee unpubl) have character states entered in the database for more than 50% of the characters that apply to nonbasidial cells in taxa of the Basidiomycota. Also A. pyxidatus is the only russuloid species with data on nuclear division (Berbee and Wells 1989). The results presented here illustrate the extent of data needed to document septal structure and nuclear division. Even within presumably well studied groups such as the Agaricomycotina we report a novel septal character state. The organization of the spindle pole region during nuclear division might provide a morphological feature characteristic of the Russulales.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Two micrometer-thick sections were cut with a glass knife on a JB-4 microtome, collected on glass slides and stained in 0.05% toluidine blue O in borate buffer (pH 9) either at room temperature for 10 min or while heated by passing the slide 6–8x over an alcohol flame, then rinsed with tap water. Sections were air dried and cover slips mounted in Eukitt (Calibrated Instruments Inc., Ardsley, New York). Digital micrographs were processed in Adobe Photoshop® CS2 (Adobe Systems Inc., San Jose, California) with the Smart Sharpen filter at the default setting.
Electron microscopy.— – Sporocarps of Auriscalpium vulgare, DJM 225 (Mycological Culture Collection and Herbarium, University of Minnesota) were produced axenically on Difco cornmeal agar and Pseudotsuga menziesii cones under cool white fluorescent light with a 12 h day at 20 C. Cultures were grown in Pyrex deep storage dishes (100 mm diam, 80 mm high) containing 50 mL of half-strength cornmeal agar (8.5 g/L) and a P. menziesii cone separately autoclaved in distilled H2O. The dish was tilted at approximately 15° while the agar solidified to provide a reservoir for water addition during sporocarp formation.
Two to three spines attached to pileal tissue were excised from mature sporocarps from colonies approximately 60 d old and plunged into –178 to –185 C liquid propane (Hoch 1986). Specimens were transferred to substitution fluid consisting of 2% osmium tetroxide and 0.1% uranyl acetate in 100% anhydrous acetone at –80 C, and stored at –80 C at least 48 h. Samples gradually were brought to room temperature (–20 C, 2 h; 0 C, 2 h; room temperature, 1 h), then rinsed three times with 100% HPLC-grade acetone with 1% acidified 2, 2–dimethoxypropane. The specimens were placed in plastic mesh baskets in a polystyrene Petri dish lid and covered with an infiltration solution made up of equal parts 100% Quetol 651 and hardeners (nonenyl sussinic anhydride and nadic methyl anhydride) with an accelerator (2,4,6–tri[dimethylaminoethyl]phenol) equal to 1% of the total solution weight (Abad et al 1988). The samples then were microwave embedded in a vacuum under 20–25 mm mercury pressure at 42 C for 2 min. The resin was replaced with fresh infiltration solution, and this process was repeated twice. Single spines were separated from pileal tissue under a dissecting scope and placed on glass slides coated with Crown dry film lubricant (Crown Industrial Products Co., Hebron, Illinois). Flat embedding was achieved as described in Kleven and McLaughlin (1989) with glass slides instead of cover slips. The resin-infiltrated specimens were polymerized in a 74 C oven for 48 h. Cells were selected with a Zeiss Axioscope at 1250x with an Optivar and a Zeiss diamond scribe in the ocular position, cut from the slides and mounted on resin blocks for sectioning. Ultrathin sections were cut with a Reichart-Jung Ultracut E ultramicrotome equipped with a diamond knife and collected on slot grids using the procedure of Rowley and Moran (1975). Sections were poststained in 3% uranyl acetate followed by Sato’s triple-lead stain (Sato 1968) and examined with a Philips CM 12 transmission electron microscope operating at 60 kV. Detailed protocols for specimen fixation and embedding are at http://aftol.umn.edu/.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Pores were approximately 130 nm wide and appeared unoccluded. No large organelles were observed in the pore or on the adseptal side of the septal pore cap, although ribosomes sometimes were present (FIG. 4). Bell-shaped septal pore caps were present on both sides of the septum (FIGS. 1, 4) and each had circular perforations approximately 70 nm diam uniformly distributed throughout the rounded portion of the cap (100–120 nm between the centers of adjacent pores, FIG. 2). Perforations were present in the area of the cap adjacent to the septal wall but their size and distribution were not determined. The pore caps contained a central electron-opaque layer about 8 nm thick between two less electron-opaque layers. This layering was present in the portion of the cap that extended along the cross wall on both sides of the pore (FIGS. 1–4). The length of the cap that extended along the cross wall varied between septa as well as on either side of a septum (FIG. 4, SUPPLEMENTARY FIGS. 1–3). Some caps terminated at the base of the septal pore swelling but other caps spread out up to 360 nm past the septal pore swelling (FIGS. 2–4). Although septa in clamp connections may be narrower than those of main hyphae, pore caps at these septa were observed extending to the clamp hyphal wall (FIGS. 2, 3). In some sections the area between the cap and septal pore appeared more electron-transparent than the abseptal area of the cap (FIG. 4, SUPPLEMENTARY FIGS. 1–3). A zone of organelle exclusion 50–530 nm thick was observed on the abseptal side of the pore cap and had a textured appearance (FIG. 1).
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). Nucleoli were electron opaque with a granular texture. Small electron-opaque patches presumed to be condensed chromatin were visible in some sections (FIG. 11). The size of the fusion nucleus observed with TEM (n = 4) increased to 2.6–3.8 µm diam (FIG. 6, SUPPLEMENTARY FIG. 4) and synaptonemal complexes were present. SPB were not observed in interphase or prophase.
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, SUPPLEMENTARY FIG. 5), although it sometimes appeared in greater volume on one side. The one complete spindle observed was 1.7 µm long (not illustrated). Globose to ovoid SPB (n = 4) were 140–240 nm h x 210–350 nm w and had an electron-opaque narrow ovoid area (70–140 nm h x 160–240 nm w) in the center. This area usually was oriented with its long axis oblique to perpendicular to the spindle and was surrounded by a more electron-transparent layer (FIG. 12). Each SPB was set in a loose fenestra at opposite ends of the nucleus and was attached to astral microtubules (MT) and kinetochore and nonkinetochore spindle MT (FIG. 13). The connections between kinetochores and MT were difficult to observe; they did not appear differentiated although they often were found at the terminal end of MT that expanded slightly. Astral MT projected away from the dividing nucleus into the cytoplasm. Some nonkinetochore MT traversed the condensed chromatin, emerging through the nuclear envelope at the opposite fenestra. Except at the poles the nuclear envelope usually remained intact with occasional gaps. However the nuclear envelope sometimes appeared absent adjacent to the cell wall (SUPPLEMENTARY FIG. 5). Fragments of endoplasmic reticulum (ER) were visible near the SPB. A meta-phase plate was absent.
The transition from metaphase I to anaphase I was difficult to distinguish. We observed nuclei (n = 2) with increased spindle length (2.7 µm, n = 1) compared to that of metaphase I but it was unclear whether the chromatin had started to migrate toward the poles. The nuclear envelope displayed wider and more frequent gaps, and the amount of ER increased both at the poles and around the nucleus (FIG. 14). Nucleoli were not observed during metaphase I and meta-anaphase I.
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). Their nuclear envelopes were reformed almost completely except for the area around the SPB and a remnant of the degrading spindle. One ovoid SPB (190 nm high x 300 nm wide) with an internal electron-opaque area 120 nm high x 210 nm wide appeared adjacent to the cell wall and was estimated to be 3.6 µm from the other SPB.
Events from the second stage of nuclear division rarely were seen. One possible metaphase II basidium was observed with the light microscope (FIG. 8) and showed two areas of condensed chromatin, each with a central chromatin-free area. These areas were interpreted to be spindles oriented parallel to each other and perpendicular to the long axis of the cell suggesting a chiastic division. At interphase II the four daughter nuclei were observed congregated subapically, each having distinct nucleoli (FIGS. 9, 17). Nuclei subsequently separated and could be seen migrating into the sterigmata (FIG. 10).
Mitotic metaphase (n = 2) observed in basidiospores appeared similar to metaphase I. We also observed what was likely mitotic metaphase in one basidium with two nuclei that were dividing during migration into the developing spores (SUPPLEMENTARY FIGS. 6, 7). Globoid SPB (140–210 nm high x 210–310 nm wide) (n = 6) had a central ovoid electron-opaque area (70–120 nm high x 90–190 nm wide). SPB were located in polar fenestrae and the nuclear envelope had occasional gaps but was mostly continuous (FIGS. 18, 19). Spindles (n = 3) were 1.6–1.8 µm long and chromatin was distributed both symmetrically and asymmetrically around the central spindle. As in metaphase I, kinetochore and nonkinetochore spindle MT and astral MT were present. Fragments of ER were present near the poles of the nucleus but a SPB cap was absent. Neither a metaphase plate nor the nucleolus was observed.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Except for Hericium coralloides (Flegler et al 1976) and Artomyces pyxidatus (M Berbee unpubl) detailed comparisons with other taxa in the Russulales is not possible because of the incompleteness of the septal data. The diameter of pore cap perforations in A. vulgare appears to be greater than those reported for select species from the Phallomycetidae, Polyporales, Agaricales and Boletales and closer in size to the perforations ofLaetisaria fuciformis (= Corticium fuciforme) (Patton and Marchant 1978, Orlovich and Ashford 1994). However Coprinopsis stercorea (= Coprinus stercorarius) and Schizophyllum commune in the Agaricales have pore cap perforations similar in size to those observed in this study (Ellis et al 1972, Müller et al 1998). Some of these studies used chemical fixation (CF) while others employed FS. Tangential sections of pore caps preserved by both methods that display measurable perforation diameters are rarely presented for comparison, so it is not clear whether the diameter of pore cap perforations varies with fixation method.
Many septal pore caps contain internal layers and are continuous with the ER adjacent to the septal wall. The transition between layered pore cap and unlayered ER occurs at the base of the septal swelling (Bracker and Butler 1964, Ellis et al 1972, Müller et al 1998). Pore caps of A. vulgare displayed internal layering that extended along the cross wall identical to that seen but undescribed in chemically fixed A. vulgare (Keller 1997). Limited observations in the phylogenetically related Artomyces pyxidatus do not show such layering along the cross wall (M Berbee unpubl).
Extended internal layering in A. vulgare was more pronounced in pore caps in clamp connections than in main hyphae and more likely was to be found in the hymenophore trama than in the subhymenium. This variation may indicate tissue and/or cell type-specific pore cap differentiation. Keller (1997) presents only one micrograph of the septal pore cap in A. vulgare and its cell type is not mentioned. Also septal pore occlusions were absent from the hymenophore hyphae we examined in A. vulgare. Flegler et al (1976) observed differences in septal pore occlusions between vegetative hyphae and sporocarp tissue in various Basidiomycota including Hericium coralloides (Russulales); occlusions were imperforate in vegetative hyphae and perforate or absent in the hymenium and lamellae.
A zone of organelle exclusion was observed on the abseptal side of pore caps in the trama of A. vulgare. Similar zones have been reported so far only for subhymenial and basal septa in basidia of the Agaricales (Thielke 1972, Craig et al 1977, McLaughlin 1974) and Boletales (McLaughlin 1982) and may be a synapomorphy for the group containing these clades. McLaughlin (1982) associates such outer zones with basidiocarp tissue, although their presence may depend on developmental stage and type of cell within the basidiocarp (Gull 1976).
Nuclear division.— –
The nuclear division and spindle pole body data presented here are not intended to be a comprehensive study. Our original goal was to examine the septal pore apparatus and cystidia, but preservation of basidia by FS exceeded our expectations and a comparison with the single study of nuclear division in the Russulales (Berbee and Wells 1989) was possible and desirable. Microtubules and the nuclear envelope were well preserved. Reports differ on improved nuclear envelope fixation with FS compared to CF (see O’Donnell 1994). SPB structure appeared somewhat diffuse. Chemically fixed SPB may display better internal definition than those undergoing FS (Lü and McLaughlin 1994, Frieders and McLaughlin 1996).
The basic shape of the SPB of A. vulgare was globular, corresponding to those observed in the Agaricomycotina (Celio et al 2006). The stages of meiosis I reported here share similarities with A. pyxidatus (Russulales) (Berbee and Wells 1989). Both taxa have globular SPB during meiosis I and in A. vulgare a SPB often contained an electron-opaque area whose long axis was oblique to perpendicular to the spindle. This area described as an inclusion in A. pyxidatus also was observed at angles ranging from perpendicular to parallel to the spindle but did not appear in the monoglobular SPB of meiosis II and mitosis until late telophase. Berbee and Wells (1989) compare the inclusion to the electron-opaque codisk found in Puccinia malvacearum (Pucciniomycotina) (OrDonnell and McLaughlin 1981). The codisk in P. malvacearum is generated within the disk-shaped SPB during meiosis I; at prometaphase II it is presumed to fuse with the SPB, which subsequently splits into two SPB. Berbee and Wells (1989) suggest that the inclusion in A. pyxidatus could be the half middle piece that joins the duplicated SPB during prophase and that it is homologous to the codisk in P. malvacearum.
The spindle pole body cap is a membranous structure found on the cytoplasmic side of the SPB in many Basidiomycota. Among members of the phylum the cap may be continuous with the nuclear envelope with or without perforations or distinct from the nuclear envelope. Membrane fragments also may be present near the SPB that together do not form a distinct cap. SPB caps that are continuous with the nuclear envelope have been reported for those Agaricomycetes in members of the Boletales (Yoon and McLaughlin 1987), Agaricales (Lerbs 1971, Raju and Lu 1973, Wells 1978), and Polyporales (Girbardt 1968). In contrast species in the Auriculariales (Lü and McLaughlin 1994), Cantharellales (Taylor 1985), Hymenochaetales (Setliff et al 1974) and Russulales (Berbee and Wells 1989) lack SPB caps. Mapping the SPB cap character states onto an abbreviated cladogram based on molecular data (Matheny et al 2007) demonstrates the potential phylogenetic signal of this ultrastructural character (FIG. 20). James et al (2006) and Matheny et al (2007) reported weak to moderate support for the branch leading to a group containing the Russulales, Agaricales, Atheliales and Boletales, while other multigene analyses have resulted in slightly different topologies but also with weak support (Binder and Hibbett 2002, Lutzoni et al 2004). The existing nuclear division data, representing a small portion of the Agaricomycotina, either suggest that the SPB cap is a highly homoplastic character or support an alternative, more parsimonious topology. Specifically if the Russulales and Hymenochaetales share a most recent common ancestor, then the most parsimonious explanation would be a single gain of the SPB cap on the branch leading to the group containing the Polyporales through Boletales and one reversal on the branch leading to the Russulales and Hymenochaetales (FIG. 20). However it is critical that the presence or absence of a SPB cap in the Thelephorales be known before we can have confidence in this alternative phylogenetic hypothesis.
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) and is present in Russulales (Berbee and Wells 1989), Hymenochaetales (Setliff et al 1974), Polyporales (Girbardt 1968) and Cantharellales (Taylor 1985) as well as in the Tremellomycetes (Taylor and Wells 1979).
Nucleoli could be seen in premeiotic fusion nuclei but were not observed in A. vulgare during meiotic metaphase I and meta-anaphase I, or in mitotic metaphase. Berbee and Wells (1989) reported a nucleolus during meiotic prophase I that was not evident during meta-anaphase I and II and that reappeared at telophase I and II; prophase II was not observed. Whether the nucleolus is discarded wholly or dispersed in A. vulgare is uncertain. Data regarding nucleolus behavior within the Agaricomycotina is scarce, although some studies describe the disappearance of the nucleolus between prophase and meta-phase (e.g. Pholiota terrestris, Agaricales; Wells 1978) or after metaphase (e.g. Chalciporus rubinellus, Boletales; Yoon and McLaughlin 1987).
Spindle orientation in A. vulgare appears to be chiastic during meiosis I and II. This pattern has been observed in most Agaricomycotina studied, including A. pyxidatus (Berbee and Wells 1989), while both chiastic and stichic division are reported in many members of the Cantharellales, Auriculariales and Dacrymycetales (see Hibbett and Thorn 2001).
Structural and Biochemical (SB) Database.— –
It presently contains 18 characters for the septal pore apparatus in nonbasidial cells and nonascogenous hypha/ascus (Celio et al 2006). The 16 nuclear division characters, four of which address the SPB, include many of the characters and states developed by Heath (1980, 1986) with modifications specific to the Fungi. Characters address both the general form and detailed features of some structures because different characters may be phylogenetically informative at varying taxonomic levels. This range of specificity allows for greater customization of data for phylogenetic analyses. Finalizing characters and states involved consideration of the homology of various structures, such as the numerous forms of septal pore occlusions, and the developmental stage and type of cell from which data were taken (e.g. the transition of the septal pore occlusion from immature to mature ascogenous hypha/ascus of Sordaria humana) (Beckett 1981).
The ultrastructure data collected from A. vulgare provided character states for many of the characters found in nonbasidial cells and nuclear division. However the coding of the species for the SB Database remains incomplete due to the potential need to add a new character state to the SB Database’s list and to documentation gaps in nuclear division stages. In cases where the interpretation of data is uncertain or features are observed but not present among the existing character states list, the SB Database allows supplemental notes to be added to a species entry. Extended septal pore cap margins as seen in A. vulgare is not a character state at this time and thus is described in the notes field of its database entry. Further examination of other species of Russulales will determine whether this character state is phylogenetically informative. Examination of nuclear division was not exhaustive, but data for almost 50% of the characters for both meiosis and mitosis could be entered in the database. Interphase SPB and the fate of the nucleolus were not observed during this study and meiosis II and mitotic stages were rare. However the success encountered with FS of A. vulgare indicates that future acquisition of the remaining data is feasible.
Ultrastructural characters can provide significant data for phylogenetic analyses at various taxonomic levels and have the potential to strengthen weakly supported relationships determined with molecular data (FIG. 20; Swann et al 1999, Lutzoni et al 2004). As taxon sampling widens the SB Database will adapt to new data and hypotheses to provide an up-to-date and flexible resource. Continued analyses performed with both types of data will facilitate more comparisons within and among related clades, resulting in a better understanding of the evolutionary history of the Fungi.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: celio001{at}umn.edu
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LITERATURE CITED |
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