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Paleomycology of the Princeton Chert. II. Dark-Septate Fungi in the Aquatic Angiosperm Eorhiza Arnoldii Indicate a Diverse Assem

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Paleomycology of the Princeton Chert. II. Dark-Septate Fungi in the Aquatic Angiosperm Eorhiza Arnoldii Indicate a Diverse Assem KU ScholarWorks | http://kuscholarworks.ku.edu Please share your stories about how Open Access to this article benefits you. Paleomycology of the Princeton Chert. II. Dark-septate fungi in the aquatic angiosperm Eorhiza arnoldii indicate a diverse assemblage of root-colonizing fungi during the Eocene by Ashley A. Klymiuk et al. 2013 This is the published version of the article, made available with the permission of the publisher. The original published version can be found at the link below. Ashley A. Klymiuk et al. (2013). Paleomycology of the Princeton Chert. II. Dark-septate fungi in the aquatic angiosperm Eorhiza arnoldii indicate a diverse assemblage of root-colonizing fungi during the Eocene. Mycologia 105(5):1100-1109 Published version: http://www.dx.doi.org/10.3852/13-025 Terms of Use: http://www2.ku.edu/~scholar/docs/license.shtml KU ScholarWorks is a service provided by the KU Libraries’ Office of Scholarly Communication & Copyright. Mycologia, 105(5), 2013, pp. 1100–1109. DOI: 10.3852/13-025 # 2013 by The Mycological Society of America, Lawrence, KS 66044-8897 Paleomycology of the Princeton Chert II. Dark-septate fungi in the aquatic angiosperm Eorhiza arnoldii indicate a diverse assemblage of root-colonizing fungi during the Eocene Ashley A. Klymiuk1 have been integral to the colonization of land by Thomas N. Taylor plants (Pirozynski and Mallock 1975, Humphreys et al. Edith L. Taylor 2010, Bidartondo et al. 2011); in the subsequent University of Kansas, Department of Ecology & , 450 million y, intricate associations have evolved, Evolutionary Biology; Biodiversity Institute, Lawrence, ranging from obligate mutualism through commen- Kansas 66045-7534 salism, parasitism and pathogenicity. A substantial Michael Krings number of vascular plants also are host to internal Department fu¨r Geo- und Umweltwissenschaften, fungal biota with which they form neither typical Pala¨ontologie und Geobiologie, Ludwig-Maximilians- mycorrhizal associations nor produce responses asso- Universita¨t, and Bayerische Staatssammlung fu¨r ciated with infection (Saikkonen et al. 1998, Jumppo- Pala¨ontologie und Geologie, 80333 Munich, Germany nen 2001). There is evidence that relationships between vascular plants and fungal endophytes occur within a continuum: endophytic fungi actively derive Abstract: Tissues of the extinct aquatic or emergent carbon from hosts (Barrow 2003) and their presence angiosperm, Eorhiza arnoldii incertae sedis, were may inhibit herbivory (Saikkonen et al. 1998) and extensively colonized by microfungi, and in this study increase drought tolerance (Rodriguez et al. 2008), we report the presence of several types of sterile but there is also evidence for mutual antagonism mycelia. In addition to inter- and intracellular between endophytes and hosts (Schulz et al. 1999), proliferation of regular septate hyphae, the tissues and these fungi are known to become weak pathogens contain monilioid hyphae with intercalary branching. or saptrophs with the decline of host plants (Schulz These filamentous mycelia are spatially associated and Boyle 2005). Consequently the ecological func- with two distinct morphotypes of intracellular micro- tions of endophytic fungi are of interest, particularly sclerotia. These quiescent structures are morpholog- in that they often are observed in plants growing in ically similar to loose and cerebriform microsclerotia stressed or marginal habitats (Barrow 2003, Newsham found within the living tissues of some plants, which 2011), where they may be more common than have been attributed to an informal assemblage of arbuscular mycorrhizal fungi (Read and Haselwand- dematiaceous ascomycetes, the dark-septate endo- ter 1981, Mandyam and Jumpponen 2005). phytes. While there are significant challenges to Interpreting the ecological role of fungi in the interpreting the ecology of fossilized fungi, these fossil record is a significant challenge. In some specimens provide evidence for asymptomatic endo- instances, there is anatomical or structural evidence phytic colonization of the rooting structures of a 48.7 that interactions between fossil fungi and host plants million year old aquatic angiosperm. were mycorrhizal (Remy et al. 1994) or pathogenic Key words: cerebriform, dark-septate endophytes, (LePage et al. 1994). Given that a hallmark of an Leptodontidium, microsclerotia, monilioid, paleomy- ascomycteous or basidiomycetous endophyte is cology, Phialocephala, Princeton Chert asymptomatic persistence within a host, there is no proximal method by which to differentiate a fossil INTRODUCTION endophyte from a saprotroph, particularly because endophytic microfungi can persist as saprotrophs Fungi are major ecological drivers in extant plant upon the death of their host (Menkis et al. 2005). communities, where they play vital roles in decompo- Ecological interpretations of fossils therefore must sition and nutrient mobilization (Cromack and take into account secondary lines of evidence, which Caldwell 1992, Hoffland et al. 2004) and contribute include the taphonomic profile of host tissue, to niche partitioning and plant species diversity systematic affinities of fossils and associational data. (Gustafson and Casper 2006, Vogelsang et al. 2006). This task is further complicated by the tendency of Mutualistic relationships with fungi are thought to some fungi, particularly within Ascomycota, to exhibit multiple conidial and mycelial anamorphs (Seifert Submitted 15 Jan 2013; accepted for publication 2 Apr 2013. and Samuels 2000). In this study we describe several 1 Corresponding author. E-mail: [email protected] sterile structures systemically distributed within the 1100 KLYMIUK ET AL.: EOCENE DARK-SEPTATE ENDOPHYTES 1101 rhizomes of an aquatic angiosperm, Eorhiza arnoldii what appear to be inconspicuous lateral scars Robison et Person. We interpret these fungal fossils to (FIG. 1C, upper arrow) but could be taphonomic as monilioid and regular simple-septate sterile hy- artifacts. Intercalary branching within monilioid phae, which are in spatial association with two types of hyphae occurs frequently, and there is obvious septal intracellular microsclerotia. These Eocene fungi are constriction of cells at branching loci (FIG. 1D, E, H). similar to the extant ascomycetes commonly referred The regularly septate hyphae from which monilioid to as dark-septate endophytes (DSE, Stoyke and cells initially are produced may remain micronema- Currah 1991), which inhabit the rhizosphere and tous (FIG. 1A, D), or hyphal elements may be living tissues of some vascular plants. somewhat inflated, up to 7–8 mm diam (FIG. 1C, G). Within the pith of some E. arnoldii specimens, regular hyphae are absent or rare and proliferation of MATERIALS AND METHODS monilioid hyphae is extensive (FIG. 1E, F). This is in Fungal body fossils described in this study occur within contrast to the cortex, where regular hyphae are tissues of the extinct aquatic or emergent angiosperm frequently associated with monilioid growth (FIG. 1A– Eorhiza arnoldii, which is known from anatomically pre- D, G–I), and also contrasts with the distribution of served vegetative organs (Stockey and Pigg 1994) present in other fungal remains previously observed within these many of the individual bedding planes that constitute the plants (Klymiuk et al. 2012), which likewise are Princeton Chert locality of southern British Columbia, restricted to cortical tissues. Canada (UTM 10 U 678057 5472372; 49u229400N, 120u329480W). This well known paleobotanical locality Loose microsclerotia.—Monilioid hyphae are in close comprises 49 layers of silicified peat interbedded with sub- spatial association with clusters of monilioid cells that bituminous coal; it has been K-Ar dated to , 48.7 Ma and are constrained to host parenchyma cells (FIG. 1H, I). thus is latest Ypresian to earliest Lutetian in age (Smith and In this manner, aggregations of monilioid cells form Stockey 2007, Mustoe 2011, Klymiuk et al. 2013). m m Slabs of chert containing E. arnoldii rhizomes were loose microsclerotia, up to 65 m long by 25 m wide, selectively sectioned into 3–5 cm2 samples and mounted that show no evidence of differentiation into rind or on glass slides with Hillquist two-part mounting medium medullary zones (FIG. 1I). Microsclerotial initiation (Hillquist, USA). Serial thin sections, 50–200 mm thick, were occurs via the production of monilioid cells con- cut with a Buehler PetrothinH. Serial photomicrographs, strained to the host parenchyma cell (FIG. 1H) and taken at different focal planes, were captured directly from proceeds until the host cell is filled. Initiation occurs the rock surface under oil immersion, with a Leica DC500 from normal hyphae (FIG. 1H, arrow), but closely CCD attached to a Leica DM5000B transmitted-light associated inflated hyphal elements (FIG. 1I, arrow) compound microscope. Photomicrographs were compiled suggest that microsclerotia also may develop concur- as composite focal-stacked images, optimizing visualization rent with growth phases in which monilioid hyphae of specimens in z-space (after Bercovici et al. 2009); image predominate. processing was performed in Adobe Photoshop CS5 12.1. Specimens and slides are deposited in the Paleobotanical Cerebriform microsclerotia.—Densely interwoven hy- Collections, Natural History Museum and Biodiversity phal strands form cerebriform microsclerotia, 20– Institute, University of Kansas at Lawrence, under specimen 45 mm diam (FIG. 2). They are differentiated into accession numbers 17030 Bbot 001, 17030 Cbot 001,
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