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Species of the genus Glomites as plant symbionts in Early Devonian ecosystems
Abstract
Members of the genus Glomites played a prominent role as plant mycobionts in the Early Devonian paleoecosystems. Remains of fossil fungi are studied from
silicified tissues of the axial organs of several specimens of the Early Devonian Rhynia gwynne-vaughanii Kidston et Lang and Aglaophyton major (Kidston et Lang) Edwards. Among them a symbiont of vesicular-arbuscular endomycorrhiza, the fungus Glomites, is studied. The morphology of its mycelium, vesicles, glomoid spores, and sporocarps is described in detail. The information
obtained allows the description of a new species, Glomites sporocarpoides Karatygin, Snigirevskaya, K. Demchenko et Zdebska. This is the third species of this genus and the first species with sporocarps
from Devonian deposits. Fungal sporocarps have been found in both dying plant tissues and in dispersed plant remains. Developmental
stages of glomoid spores are revealed. G. sporocarpoides is characterized by the presence of both symbiotic and distinct pathogenic features. Similarities and dissimilarities in
the formation of ancient and modern endomycorrhizae are discussed.
... Remarks: Plant host: diverse early euphyllophytes (trimerophytes). Glomites oqoti differs from four other described species of Glomites: by the presence of spores which are not reported in G. cycestris (Phipps and Taylor, 1996) and G. vertebrariae (Harper et al., 2013); by occasionally possessing a septum that occludes the spores, which is notably lacking in G. rhyniensis (Taylor et al., 1995); by not producing sporocarps, which is what defines G. sporocarpoides (Karatygin et al., 2006). ...
... Moreover, each of these species exhibits a combination of characters that parallels those of the extant genera in the order Archaeosporales, suggesting that this lineage had already reached considerable diversity by the Early Devonian. Along with gigasporoid, glomoid, and acaulosporoid spores, the Rhynie Chert has yielded evidence of sporocarp structures formed by Glomites sporocarpoides, found within the axes of Rhynia gwynne-vaughanii and Aglaophyton majus (Karatygin et al., 2006). These structures resemble those of modern sporocarp-forming species of the Glomeromycotina, such as Glomus microcarpus. ...
... Because the Battery Point Formation spores are found inside plant tissues and have glomeromycete affinities, even though their placement cannot be further refined, the most appropriate taxonomic placement of these fossils is in the genus Glomites. This genus currently includes three additional species, besides the type species, G. rhyniensis described by Taylor et al. (1995): G. cycestris (from the Triassic of Antarctica; Phipps and Taylor, 1996), G. sporocarpoides (from the Rhynie Chert; Karatygin et al., 2006), and G. vertebrariae (from the Permian of Antarctica; Harper et al., 2013). All of these species are preserved within host plants, with which they form some type of intimate relationship (e.g., mycorrhizal, pathogenic). ...
Fossil assemblages in the fluvial to coastal deposits of the Early Devonian Battery Point Formation (400–395 Ma; Gaspé Bay, Quebec, Canada) are among the most diverse occurrences of Early Devonian permineralized plants worldwide. The plants host microbial and fungal material, which was studied in cellulose acetate peels and thin sections. The fossil fungal material includes spores that show affinities to the Glomeromycotina, preserved in trimerophyte axes. The spores fall into two size categories, both characterized by complex wall layering and hyphal attachments. Spores in the small category (40–65 μm) occur in a single axis and exhibit few informative features. The most frequently occurring type is the large spores (90–240 μm) that are placed into the new species Glomites oqoti. These spores exhibit four wall layers (when well preserved), of which two are always present: a thick, dark layer and a thin, membranous layer. Several lines of circumstantial evidence suggest that the spores were metabolically active within their plant hosts at the time of fossilization and that the plants were alive at the time of colonization. These observations, along with comparisons with other fossil glomeromycetes and the life history traits of living glomeromycetes, suggest that G. oqoti held an endomycorrhizal role. The Battery Point Formation fossils represent the only Early Devonian glomeromycete occurrence documented outside the Rhynie Chert hot spring deposits. Their occurrence in fluvial-coastal environments and their putative mycorrhizal role suggest that glomeromycetes were relatively ubiquitous symbionts of tracheophytes, like their extant counterparts, by the Early Devonian.
... Most fungi described to date from the Rhynie cherts were, in some form or another, associated with early land plants. Glomeromycota figure prominently in research on land plant-fungal relationships in the Rhynie paleoecosystem because of their importance for our understanding of the evolutionary history of mycorrhizal symbioses (Remy et al., 1994b;Taylor et al., 1995Taylor et al., , 2005bDotzler et al., 2006Dotzler et al., , 2009Karatygin et al., 2006;Krings et al., 2017b;Brundrett et al., 2018;Walker et al., 2018Walker et al., , 2021Harper et al., 2020). However, often cooccurring with the Glomeromycota are articulated specimens, but far more frequently sterile mycelia and detached reproductive units (e.g., spores, sporangia), of a variety of other fungi, which thrived as parasites of the plants or the mycorrhizal fungi, or were endophytes or saprotrophs (e.g., Taylor et al., 1992Taylor et al., , 2005aRemy et al., 1994a;Krings et al., 2007Krings et al., , 2010aKrings et al., , 2016aKrings et al., , 2016bKrings et al., , 2017aKrings and Taylor, 2015;Strullu-Derrien et al., 2015Harper et al., 2017;Harper, 2018, 2020;Krings, 2022a). ...
... Krings et al. (2012) opined that Glomeromycota were relatively diverse by the Rhynie chert time, and became wellestablished as a group even before true roots evolved since all of the Rhynie chert plants and many other early land plants at that time lacked roots. The description of Glomites sporocarpoides producing spores in sporocarps from the Rhynie chert, adds further support to the early diversification of Glomeromycota (Karatygin et al. 2006). ...
Fungi are an essential component of any ecosystem and have diverse ecological roles, ranging from endophytes to epiphytes
and pathogens to saprobes. The current estimate of fungal endophytes is around 1 million species, however, we estimate
that there is likely over 3 million species and only about 150,000 fungal species have been named and classified to date.
Endophytes inhabit internal plant tissues without causing apparent harm to the hosts. Endophytes occur in almost every
plant from the coldest climates to the tropics. They are thought to provide several benefits to host plants and improve the
hosts’ ability to tolerate several abiotic and biotic stresses. Endophytes produce secondary metabolites with biotechnological,
industrial and pharmaceutical application. Some endophytes appear to be host-specific, while some are associated with a
wide range of hosts. We discuss the importance of endophytes. The ability to switch lifestyles from endophytes to pathogens
or saprobes is discussed. Interactions between endophytes and hosts based on fossil data is also highlighted. Factors that
influence the specificity in endophytes are discussed. We argue that the endophytic lifestyle is a common strategy in most
fungi and that all fungi have endophytic ancestors. We critically evaluate the influence of co-evolution based on fossil data.
We hypothesise the influence of specificity on the estimated number of endophytes and overall species numbers, and present
examples of metabolites that they produce. We argue that studying endophytes for novel compounds has limitations as the
genera recovered are limited. However, if saprobes were chosen instead, this would result in a much higher species diversity
and undoubtedly chemical diversity
... Arbuscular mycorrhiza are among the most frequent plant-microbe mutualistic symbiosis, established with 80% of vascular plants (Wang and Qiu 2006;Smith and Read 2008;Strullu-Derrien et al. 2017). This symbiosis is also one of the most ancient, initiated probably when plants have colonized terrestrial areas more than 400 million years ago (Karatygin and Demchenko 2006;Humphreys et al. 2010;Strullu-derrien et al. 2014). Arbuscular mycorrhizal fungi (AMF) act fundamentally on different mechanisms of plant development, including mineral nutrition, drought resistance and toxic metal tolerance (Smith and Smith 2011;Amir et al. 2014;Augé et al. 2015;Ferrol et al. 2016). ...
Our knowledge about New Caledonian serpentine ecosystems has increased greatly during the past half-century, mainly thanks to Jaffré’s group. However, research on soil microflora and plant symbionts started only in the nineties and was mainly published during the last two decades. We aim to synthesize these studies, focusing particularly on arbuscular mycorrhizal fungi (AMF). Research on AMF consists firstly of a global and inventory approach aiming to produce a basic but essential lacking knowledge. These studies showed that AMF are abundant in ultramafic soils and concerned nearly all plant species of these ecosystems. Even Ni-hyperaccumulator plants and sedges, generally considered non-mycorrhizal, were found to be functionally colonized by AMF in New Caledonian ultramafic soils. The adaptation of AMF communities to the extreme conditions of these soils led to high levels of metal tolerance (particularly to Ni) and noticeable originality of the taxa. The influence of these symbionts on plant growth and adaptation was assessed in greenhouse and field conditions. An accurate selection of AMF isolates that improve plant growth, and plant metal tolerance was performed. It was demonstrated that combinations of AMF isolates with complementary functional traits showed highly synergistic effects on plant development. Finally, a partnership with a biotechnological company led to the production of an efficient commercial inoculant now used in the ecological restoration of mine-degraded areas. Today studies are focused mainly on the additive effects of AMF and mycorrhiza-helper bacteria.
... The fossil genus Glomites Taylor et al. 1995 is related to the extant fungal genus Glomus (Kalgutkar & Jansonius 2000). Geological record of Glomites goes back to Early Devonian (Karatygin et al. 2006). Now Glomites is transferred to the genus Palaeomycites (Kalgutkar & Jansonius 2000). ...
Kumar A. 2022. Palynology of the Rockly Bay Formation (mid-Pliocene), Tobago, West Indies. Geophytology 50(1&2): 73-94.
Four samples from the upper section of the Rockly Bay Formation (mid-Pliocene) of Tobago were studied for their palynomorph contents with the objective to carry out a palynological investigation since it was described as unfossiliferous. This study demonstrates that the upper section of the Rockly Bay Formation is fossiliferous because it contains palynomorphs. Preservation of palynomorphs is generally fair to good and exhibit diverse affinities. They are, angiosperm pollen, spores, and non-pollen palynomorphs (NPP) such as dinoflagellate cysts, acritarchs, algal cysts and fungal, crustacean, annelid and arcellinidan palynomorphs. Ascidian spicules are calcareous mineral microfossils; they are reported here because they occur in the same palynological slides. Generally, palynomorphs are of terrestrial origin, but a few are of marine origin as well suggesting that the upper section of the Rockly Bay Formation was deposited under supratidal environment, where lakes and ponds existed in which a variety of algal forms thrived. This environment was periodically influenced by high tides and cyclones. These assemblages indicate tropical climate as also evident from the tropical location of Tobago during mid-Pliocene times. Most non-pollen palynomorphs, observed in this study, have a cosmopolitan distribution.
... Mycelium is believed to have performed the role of roots and provided the plants with water and minerals. AM is an ancestral form of symbiosis between fungi and terrestrial plants and as a mutualistic biotrophic intracellular association is one of the most successful evolutionary strategies which is proved by the fact that it exists fro more than 400 million years and is the most widely spread PMS (Karatygin et al., 2006;Smith, Read, 2008, Provorov, Stark, 2014. Plants used many molecular genetic mechanisms of AM plant-microbe interaction in symbioses that emerged at later stages of evolution, for example, a symbiosis between Fabaceae and Rhizobia. ...
Arbuscular mycorrhiza (AM) is one of the most common terrestrial plant-microbe symbioses. The interest in studying AM is caused by its importance for the growth and nutrition of plants and its ecological role in preserving biological diversity. At present, 92% of plant families are known to form AM. Fungi in AM are obligate symbionts and belong to a monophyletic group – Glomeromycotina subdivision. Some researchers believe that formation of AM-symbiosis with fungi by ancient plants allowed them to inhabit land, which has led to the formation of the biosphere as we know it. AM is studied by researchers from around the world including Russia. This overview presents in brief the results of AM research in Russia during the Soviet period which did not receive international coverage due to its classified nature; the most prominent research schools and works of AM researchers are identified; main stages and lines of this research are listed, such as: distribution of AM in plant communities and different climatic zones, mycorrhiza anatomy and morphology, fungi species composition on different soils, collection of AM fungi and growing AM in vitro, physiological role of AM for agricultural plants, the impact different ecological factors have on AM fungi species composition and AM development, conditions for effective use of Am fungi to increase productivity and quality of agricultural plants as well as to perform biological recultivation of toxic soils and restore the fertility of degraded soils.
... Other Rhynie chert Glomeromycota, such as Glomites rhyniensis T.N. Taylor (Taylor et al., 1995;Karatygin et al., 2006;Strullu-Derrien et al., 2014), and Scutellosporites devonicus Dotzler, M. Krings, T.N. Taylor et Agerer in the Diversisporales (Dotzler et al., 2006), have been placed in later-evolving lineages or, as in the case of the various forms currently placed in Palaeomyces (Kidston and Lang, 1921;Krings et al., , 2017a, still need to be critically evaluated. ...
Glomeromycotan propagules (spores) are morphologically diverse in the Early Devonian Rhynie chert; however, only relatively few of these fossils have been documented and critically evaluated. This study re-examines propagules previously described informally as ‘reproductive unit 1’, and identified as glomeromycotan acaulospores borne within the neck of a sporiferous saccule. Size and morphology, spore wall structure, and the close association of specimens in land plant axes with small glomoid spores, are solid arguments for affinities of ‘reproductive unit 1’ to the Ambisporaceae (Archaeosporales). Moreover, the acaulospores correspond morphologically to Mycokidstonia sphaerialoides, a Rhynie chert fossil originally interpreted as an ascomycete perithecium that, consequently, is redefined here as a member of the Glomeromycota conspecific with ‘reproductive unit 1’. The diagnosis for M. sphaerialoides is emended to be compliant with glomeromycotan taxonomy; features of the saccule, acaulospore wall, and associated glomoid spores are included. An epitype is also designated. Mycokidstonia sphaerialoides adds to an increasing body of fossil data depicting Devonian Glomeromycota as a diverse fungal lineage which is likely to have been an ecologically important constituent of early terrestrial ecosystems.
... Taxonomically rich early Devonian flora are known in the Dniester basin (Volhynian Podolia) [25], Eastern Siberia (the Altai-Sayan region) [27, Table II, [4][5][6], (the Rhynie Chert Bed, Aberdeenshire) [28], Britain (Wales) [20], Scotland, Central Kazakhstan, Southern China, and some other regions. Early Devonian higher plants formed stable symbiotic bonds with endomycorrhizal fungi [29]. Ecologically, those land communities were already deeply diversified and formed complex catenial systems [28, Fig. 6]. ...
The preconditions of an ecosystem for and major phases of colonization of land by higher plants are considered. The most important finds of higher plants in pre-Silurian deposits are discussed. A new plant, Volkhoviella primitiva Naug., Gen. et sp. nov., from Ordovician deposits of Leningrad oblast is described. General questions of the early evolution of land vegetation are considered.
A catalogue of fossil plants collected and/or described by the famous Russian palaeobotanist, an employee of the Komarov Botanical Institute RAS, Natalia Snigirevskaya is presented. The materials are stored in the Laboratory of Palaeobotany of the BIN RAS. References are provided to publications based on these collections. The catalogue is accompanied by images of some holotypes made with modern equipment. A short essay on the life and work of Natalia Snigirevskaya precedes the catalogue.
Background and aims:
Structurally preserved arbuscular mycorrhizas from the Lower Devonian Rhynie chert represent core fossil evidence of the evolutionary history of mycorrhizal systems. Moreover, Rhynie chert fossils of glomeromycotan propagules suggest that this lineage of arbuscular fungi was morphologically diverse by the Early Devonian; however, only a small fraction of this diversity has been formally described and critically evaluated.
Methods:
Thin sections, previously prepared by grinding wafers of chert from the Rhynie beds, were studied by transmitted light microscopy. Fossils corresponding to the description of Archaeospora spp. occurred in 29 slides, and were measured, photographed, and compared to modern-day species in that genus.
Key results:
Sessile propagules <85 µm in diameter, some still attached to a sporiferous saccule, were found in early land plant axes and the chert matrix; they developed, in a similar manner to extant Archaeospora, laterally or centrally within the saccule neck. Microscopic examination and comparison with extant fungi showed that, morphologically, the fossils share the characters used to circumscribe the genus Archaeospora (Glomeromycota; Archaeosporales; Archaeosporaceae).
Conclusions:
The fossils can be assigned with confidence to the extant family Archaeosporaceae, but because molecular analysis is necessary to place organisms in these taxa to present-day genera and species, they are placed in a newly proposed fossil taxon, Archaeosporites rhyniensis.
Fungal sporocarps are described from Triassic silicified peat deposits from Antarctica. Sporocarps possess a two-layered wall and contain a single spore. The outer layer is mycelial; the inner layer, noncellular. The combination of primitive and advanced features suggests that this fungus is intermediate in complexity between the lower and evolutionarily more advanced fungi. The Antarctic fungus and morphologically similar fossils resemble extant members of the Endogonaceae, but appear to have been saprophytes rather than mycorrhizal symbionts.
Arbuscular mycorrhizae are the most ubiquitous of mycorrhizal fungi, that have formed mutualistic relationships with virtually almost all major groups of vascular plants. Five genera of arbuscular endomycorrhizal fungi are currently delineated, but fossil arbuscular mycorrhizae have been allied with only two, Glomus and Sclerocystis. A Triassic arbuscular mycorrhiza described inhabiting the roots of Antarcticycas was originally allied with Glomus. It is now known to be a mixed colony comprised of fungi attributable to the suborders Glomineae and Gigasporineae of the Glomales, described as two new species. The fossil Gigasporinean mycorrhiza is characterized by irregularly swollen intercellular and intracellular hyphae that are coiled extensively within the cells. Arbuscules have thick trunks and narrow branches. In the Glominean form, hyphal diameter is more uniform, with coiling rarely present. Arbuscules have thin trunks and fine branches. Vesicles may be lateral or terminal. Spores are not present; therefore, the probability of more than one species of each suborder being represented cannot be conclusively demonstrated. This provides the first fossil representative of the Gigasporineae and supports current rDNA estimates of the age of the lineage. Moreover, it is the first reported instance of a mixed colony of arbuscular endomycorrhizae in the fossil record.
Recent progress in the palaeomycological studies are presented in this review. The span of geologic time extending from the Precambrian examined for many sources of information in relation to major taxonomic groups of fungi. The complexity of the fungus-host interactions during the geological times suggests the most modem groups should extend well back to Precambrian. Both the fossil record and molecular sequences data suggest that the Glomeromycota and Ascomycota are older than previously thought. The fungal-plant root associates known as a mycorrhizal symbiosis appear to have evolved in the Early Devonian. The distribution of fungi in, space and time based on fossil evidence, together with rapidly accumulating molecular data, will provide the continuing impetus to characterize more accurately the phylogeny on the fungi.
We report structure and properties of fossil hyphae and spores from the Ordovician Guttenberg formation of Wisconsin. The fossils strongly resemble present-day arbuscular mycorrhizal fungi (Glomales) and are described as Palaeoglomus grayi gen. et spec. nov.