# A rare permineralized Sphenophyllum (Sphenophyta, Sphenophyllales) stem containing abundant fungal remains from the Permian of Autun, central France

Thibault Durieux, Carla J Harper, Anne-Laure Decombeix, Michael Krings

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Thibault Durieux, Carla J Harper, Anne-Laure Decombeix, Michael Krings. A rare permineralized Sphenophyllum (Sphenophyta, Sphenophyllales) stem containing abundant fungal remains from the Permian of Autun, central France. Review of Palaeobotany and Palynology, 2025, 343, pp.105416. 10.1016/j.revpalbo.2025.105416. hal-05166653

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Research papers

# A rare permineralized *Sphenophyllum* (Sphenophyta, Sphenophyllales) stem containing abundant fungal remains from the Permian of Autun, central France

Thibault Durieux<sup>a, *, *</sup>, Carla J. Harper<sup>a</sup>, Anne-Laure Decombeix<sup>b</sup>, Michael Krings<sup>c, d</sup>

<figure><img src="image_3.png" /></figure>

## ARTICLE INFO

**Keywords:**

Autun Basin
Clamp connection
Host response
Hypha
Propagule
Saprotrophism
Trace fossil

## ABSTRACT

Present-day sphenophytes, i.e. the species of the genus *Equisetum*, are hosts to a variety of fungi. Although the Sphenophyta have a long evolutionary history and were far more diverse in the past than they are today, little is known about fungi associated with the fossil representatives of this group of free-sporing vascular plants. A permineralized *Sphenophyllum* stem from the early Permian Autun Basin in France contains several types of fungal remains in the xylem and periderm, including a *Perexiflasca*-like chytrid thallus, blastic inflations of hyphal tips resembling simple glomoid spores, basidiomycete hyphae with clamp connections, and compact, three-dimensional hyphal structures of unknown function and systematic affinity. Cell wall appositions in the periderm are evidence that at least one of the fungi colonized the stem while it was alive. A taphonomic peculiarity are trace fossils of hyphae in tracheids filled with an amber-colored to brown substance, perhaps a type of gum. This is only the second report of fungi from the aerial parts of a fossil sphenophyte. It adds to the growing body of evidence that diverse fungal communities were associated with the iconic plants of the Carboniferous and early Permian coal swamp forests.

## 1. Introduction

Fungi are important ecosystem constituents that interact with plants in a wide spectrum of ways. They can be either endophytes, mutualists, parasites or pathogens, and, as saprotrophs, they are among the most important decomposers of dead plant material (e.g., Zeilinger et al., 2016; Geetha and Dathar, 2022; Priyashantha et al., 2023). Fungal interactions with plants in modern ecosystems have long been the subject of intense research, and much is therefore known about their importance for plant performance and ecosystem functioning (Dighton and White, 2017; Case et al., 2025). Although it is assumed that fungi have interacted with plants in very similar ways in the geological past since at least the Early Devonian, relatively little is known about such interactions in most fossil ecosystems (Taylor et al., 2015; Harper and Krings, 2021).

One of the first scholars to document fossil fungi more systematically and to hypothesize about fungal interactions with fossil plants was French paleobotanist Bernard Renault, who studied permineralized

Carboniferous and early Permian floras from various rock deposits in central France (Galtier, 2016). Renault's success in detailing the fungi associated with some of these plants (Renault and Bertrand, 1885; Renault, 1893, 1895a, 1895b, 1896a, 1896b, 1900, 1903) can be attributed to the excellent preservation of the fossils and his ability to produce high quality thin sections (Taylor and Krings, 2010). Since Renault's groundbreaking work, many additional fungi and fungus-like organisms, as well as various fungal associations with plants, have been described from the Carboniferous and Permian of France (Krings et al., 2007, 2009a, 2009b, 2009c, 2010a, 2010b, 2010c, 2010d, 2011a, 2011c, 2012b, 2023; Dotzler et al., 2008, 2011; Taylor et al., 2012; Harper et al., 2016; Strullu-Derrien et al., 2021), including the only record to date of fungi associated with the aerial parts of a fossil sphenophyte (Dotzler et al., 2011).

Previous records of fungi associated with fossil sphenophytes (Sphenophyta) include unidentified hyphal fragments and spores in the cortical tissues of Pennsylvanian calamitalean roots from North America

<footnote><sup>a</sup> Department of Botany, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland</footnote>

<footnote><sup>b</sup> UMR AMAP, Univ. Montpellier, CNRS, CIRAD, INRA, IRD, Montpellier, France</footnote>

<footnote><sup>c</sup> SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Straße 10, 80333 Munich, Germany</footnote>

<footnote><sup>d</sup> Department für Geo- und Umweltwissenschaften, Paläontologie und Geobiologie, Ludwig-Maximilians-Universität, Richard-Wagner-Straße 10, 80333 Munich, Germany</footnote>

<footnote>* Corresponding author.</footnote>

<footnote>E-mail address: durieuxt@tcd.ie (T. Durieux).</footnote>
(Agashe and Tilak, 1970), and *Cashhickia acuminata* T.N. Taylor et al., a root endophyte of Pennsylvanian calamites from France (Taylor et al., 2012). The scarcity of documented evidence of fungi colonizing fossil sphenophytes is somewhat surprising since present-day members of the genus *Equisetum* L. are hosts to a wide variety of fungi (e.g., Holm and Holm, 1981; Koske et al., 1985; Dhillion, 1993; Künkele et al., 2005; Lechat and Baral, 2008; Hodson et al., 2009; Aly et al., 2010; Li et al., 2010; Parkash and Dhungana, 2011; Suwannarach et al., 2013; Baral and Haelewaters, 2015; Abd-Elsalam et al., 2016; Haelewaters et al., 2018; Giesemann et al., 2020; Xu et al., 2020).

Here, we describe a permineralized *Sphenophyllum* stem from the early Permian of the Autun Basin in central France. Several different types of fungal hyphae and reproductive units occur in all parts of the primary and secondary xylem, and in the periderm. A host reaction in the form of cell wall appositions in periderm cells is evidence that at least one of the fungi colonized the stem while it was alive. A taphonomic particularity is the in-situ preservation of undistorted hyphae as trace fossils in tracheids filled with an amber-colored to brown substance. This discovery adds to our knowledge of fungal associations with sphenophytes in late Paleozoic ecosystems.

## 2. Geological setting, material, and methods

The fungal remains described in this study are all present in a single cross section of an almost perfectly preserved, permineralized *Sphenophyllum* Brongniet stem. The slide containing the cross section belongs to the historical “collection Roche” (Box D, without number), a set of more than 2000 thin sections prepared during the late 19th and early 20th centuries by Auguste Roche, a friend, co-worker, and biographer of Bernard Renault (Galtier, 2016), that is today housed at the Muséum d’histoire naturelle d’Autun. Parts of the section were previously illustrated by Decombeix et al. (2019: fig. 6F) and Decombeix and Galtier (2021: fig. 7B). The information on the original label is sparse; however, we are fairly confident that the specimen comes from the Autun Basin in central France and was collected in the vicinity of the city of Autun.

In the Autun Basin, there are several fossil sites known for their great diversity of impression/compression fossils and permineralizations of early Permian plants. To date, more than 70 different fossil-species (in 40 genera) of anatomically preserved plants have been described from there (see Broutin et al., 1999; Galtier et al., 2011), including *Sphenophyllum* (Renault, 1873, 1876, 1878, 1896b). Specimens of the latter taxon come from deposits that Renault called “zone 4”. The exact locations where these specimens were found are not known, although Renault himself gives the names “Champs de Borgis” and “Champ de la Justice” for some of them (Renault, 1896b: pp. 505/506; see also Broutin et al., 1999). According to Broutin et al. (1999: fig. 3) and Pellenard et al. (2017: fig. 1b), “zone 4” is late Autunian (an approximate equivalent of the Sakmarian) in age and comprised of the Surmoulin and Millery formations (Text-Fig. 1). The fact that some 75% of the 2212 slides in the ‘collection Roche’ contain fossils from the Autun Basin and from this period of geologic time (Galtier, 1980, 2016) suggests that the *Sphenophyllum* specimen colonized by fungi is early Permian in age and originates from either the Surmoulin or Millery Formation. Because silicified plants in the Autun Basin are so far only known only from the Igornay, Muse, and Millery formations (Galtier, 1980), the specimen from the collection Roche most likely comes from the Millery Formation.

Digital images were taken with a Keyence VX7000 digital microscope and an Olympus BX 51 transmitted light microscope equipped with a Sony XCD-U100CR digital camera at UMR AMAP in Montpellier, France, and with a Leica DM LB2 transmitted light microscope equipped with a Jenoptik Gryphax Naos camera at SNSB-BSPG in Munich, Germany. Images were processed in Adobe Photoshop CS6 for brightness and contrast, and images of the same specimen were recorded at multiple focal planes and stacked into a single image. To make it easier to find the slide in the box, it was marked with a white dot with the letter

<figure><img src="image_4.png" /><figcaption>Fig. 1. Correlation of stratigraphic zones used by Renault (1873, 1876, 1878, 1896b) with the standard chronostratigraphy and the continental European Autunian [based in part on Broutin et al. (1999: fig. 3) and Pellenard et al. (2017: fig. 1b)].</figcaption></figure>

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## 3. Results

### 3.1. The host

The *Sphenophyllum* stem, in which the fungal remains are located, is roughly roundish in cross section and has a diameter of approximately 10 mm (Plate I, 1). The primary xylem is more or less triangular in outline, with three concave sides (Plate I, 1, 2); the protoxylem is located at the tips of the three arms (arrows in Plate II, 2). Protoxylem tracheids have a diameter of 10–30 µm, while the tracheids of the primary xylem are 23–136 µm in diameter. The primary xylem is surrounded by a secondary xylem up to 4 mm thick.

The secondary xylem consists of regular radial rows of cells, is divided into three fascicular segments opposite the protoxylem strands, and three interfascicular segments opposite the sides of the metaxylem (Plate I, 2). The tracheids of the fascicular secondary xylem are square to rectangular in cross section, with rounded corners or nearly oval to circular, and have radial diameters of 31–207 µm and tangential diameters of 19–185 µm; tracheids towards the periphery usually are larger than those closer to the center. The tracheids of the interfascicular secondary xylem are also square to almost circular in cross section, but significantly larger on average (radial diameter 47–292 µm, tangential diameter 97–277 µm). In addition, the radial rows show a less pronounced increase in diameter of the tracheids towards the periphery. A small area of the stem shows partially destroyed tracheids, in which parts of the longitudinal cell walls are visible (Plate I, 4). The walls show what appear to be densely spaced circular to hexagonal bordered pits 8–12 µm wide. In some rows of the fascicular secondary xylem, a pronounced alteration of tracheids with small and large diameters can be observed (Plate I, 7), which does not occur in the interfascicular secondary xylem, with one exception. Cichan and Taylor (1984) attribute this pattern to the fact that the apparently smaller tracheids are cut near their tips, while the larger tracheids are cut in a central area. Between the secondary xylem tracheids are small parenchymatous cells (14–53
<figure><img src="image_5.png" /><figcaption>**Plate I.** *Sphenophyllum* stem (in cross-section view) from the collection Roche, Autun. 1. Overview of specimen. 2. Triangular primary xylem and inner portion of the fascicular and interfascicular secondary xylem; arrows indicate exarch protoxylem. 3. Peripheral secondary xylem, poorly preserved extraxylary tissues (probably phloem and inner cortex), and well-preserved periderm. 4. Partially destroyed secondary xylem tracheids showing pits. 5. Secondary xylem tracheids and clusters of small parenchyma cells. 6. Periderm cells with and without black content. 7. Fascicular secondary xylem showing alternation of narrow and wide tracheids. 8. Radial parenchymatous system (arrows), with radially elongated ray cells. Scale bars: 1 = 2 mm; 2, 3, 6–8 = 200 µm; 4, 5 = 100 µm.</figcaption></figure>

µm wide), either singly or in groups of two to more than 15 cells (Plate I, 5). In many cases, similar parenchymatous cells also line the rays, which extend through the xylem into the phloem (Plate I, 7, 8). The ray cells are usually radially elongated (arrows in Plate I, 8). All cells of the

protoxylem and primary xylem are filled with an amber-colored to (dark) brown substance of unknown origin and composition (Plate I, 1, 2). Many cells of the inner region of the secondary xylem also have such a filling, although some are only partially filled (e.g., Plate II, 17; Plate
<figure><img src="image_6.png" /><figcaption>**Plate II.** Fungal remains in xylem and periderm – Hyphae, reproductive units, and cell wall appositions. 1. Secondary xylem tracheids containing *type-1* hyphae (arrows). 2, 3. Close-ups of *type-1* hyphae in cross-section view; note granular texture of outer wall layer and stratified wall in the specimen shown in Plate II, 2. 4. Hypha and putative reproductive unit with a thin subtending hypha (arrow) in periderm cells. 5. Periderm cell with cell wall appositions in longitudinal-section view; arrows show penetration hyphae in the center of the appositions. 6. Branched *type-2* hyphae in secondary xylem tracheid; arrow shows septum. 7, 8. *Type-2* hyphae (arrows) passing through a host cell wall (cw). 9. *Type-2* hyphae (in cross-section view; arrows) extending inside a host cell wall (cw). 10. *Type-1* hypha giving off a *type-2* hypha (arrow). 11. *Type-2* hypha with terminal inflation, presumably a chlamydospore; arrow shows septum. 12–15. *Type-3* hyphae (inverted light) passing through host tracheids and tracheid walls (cw); note fragmented hyphae filled with black contents in Plate II, 14. 16. *Type-4* hypha with a septum (arrow). 17. Cell partially filled with an amber-colored to brown substance; note trace fossil hyphae in the filled part (arrow) and body fossil *type-4* hypha in the unfilled part. 18. Detail of Plate II, 17, focusing on *type-4* hypha with closely spaced irregular swellings. Scale bars: 1 = 200 µm; 12, 13, 17 = 50 µm; 11 = 30 µm; 2, 6–10, 14–16, 18 = 20 µm; 3–5 = 10 µm.</figcaption></figure>
IV, 1).

The vascular cylinder is surrounded by a 0.2–0.5 mm thick, poorly preserved layer (Plate I, 3), which probably represents the phloem and inner cortex. A periderm c. 1.2 mm thick is the best preserved extra-xylary tissue of the stem (Plate I, 1, 3, 6). Periderm cells are rectangular, 16–63 µm in radial diameter, and 60–179 µm in tangential diameter. The periderm is stratified and consists of alternating layers of cells with and without black content (Plate I, 6). The tissues outside the periderm were no longer present at the time of fossilization or are not preserved.

## 3.2. Fungal remains

Evidence for colonization by fungi is abundant and diverse in this *Sphenophyllum* stem. Fungal remains are present in all parts of the stem, but colonization appears to have been much more massive in the primary and secondary xylem (more than 85% of the tracheids show some evidence of colonization) than in the extraxylary tissues (less than 20% of the cells with evidence of colonization). However, the extent of colonization of the protoxylem, xylem parenchyma, and rays is generally difficult to assess due to the small size of the cells. The vast majority of fungal remains are found in the lumen of their host cells, but some are also found in the cell walls. Certain hyphae are preserved as trace fossils in tracheids filled with an amber-colored to brown substance.

### 3.2.1. Hyphae

Body fossils of four different types of hyphae regularly occur in the primary and secondary xylem (Plates II, III); however, they are – with one exception (see below) – better preserved and much easier to recognize in the cells not filled with an amber-colored to brown substance (see Plate I, 1). The first hyphal type (*type I*) is thick-walled (Plate II, 1–3; Plate IV, 1), usually (but not always) occurs singly in the host cells, and typically extends in longitudinal direction (i.e. parallel to the long axis of the host plant), as a result of which these hyphae can be seen almost exclusively as cross-sections (arrows in Plate II, 1; Plate IV, 1). The hyphae are between 7.5 and 16 µm wide, and many appear to have stratified walls (Plate II, 3). The outer wall layer(s) in many cases have a granular texture, but this could be an artifact of preservation or reflect partial degradation of the wall prior to fossilization.

The second type of hypha (*type 2*) is thin-walled, regularly branched at angles of less than 90° (Plate II, 6), between 1.5 and 3.5 µm wide, and sparsely and irregularly septate (e.g., arrow in Plate II, 6). These hyphae extend in all directions, and occur both in the lumen of the tracheids and in the tracheid walls. When penetrating the wall of a host cell, the diameter of the hypha typically is not reduced (Plate II, 7, 8); no evidence was found of special structures (e.g., appressorium-like swellings) that could have either released enzymes to chemically alter the host cell walls or generated hydrostatic force to push the hyphae through the walls. In some cases, the hyphae not only appear to grow straight through host cell walls, but even extend and spread inside the walls (Plate II, 9). Some of the *type-2* hyphae form large, terminal inflations, which presumably represent chlamydospores, as they are separated at the base by a septum from the subtending hypha (arrow in Plate II, 11). Evidence that *type-2* hyphae are produced by *type-1* hyphae is provided in the form of organic connections of both types of hyphae (Plate II, 10).

A third type of hypha (*type 3*) is fine as hair (usually less than 1.5 µm wide) and can only be viewed reasonably well in the cells filled with amber-colored to brown substance under inverted light (Plate II, 12–15). These hyphae are rarely branched and traverse from tracheid to tracheid without changing their structure when passing through a host cell wall. Some of the hyphae are fragmented and, in some cases, also filled with black, opaque material, so that they appear as interrupted lines (Plate II, 14, 15).

The fourth hyphal type (*type 4*) is narrow to wide (2 to more than 10 µm wide), thin-walled, almost colorless or light-brown, and aseptate or sparsely septate (Plate II, 16). Some hyphae are more or less tubular, others are not uniformly wide. Still others consist of a series of closely

spaced ellipsoidal to spherical inflations of very different sizes (up to 25 µm or more in diameter), whereby the entire hypha resembles a string of pearls (Plate II, 17, 18); lateral inflations in the form of greatly enlarged short branches also occur. In some tracheids, the *type-4* hyphae form peculiar, usually compact three-dimensional structures, which may fill the entire host cell lumen (at least in cross section; Plate III, 1–5) and consist of densely packed, irregularly septate or pseudo-septate (arrows in Plate III, 1), more or less tubular hyphal segments and variously shaped and sized sac-like inflations, some of which are distorted or collapsed. A few of the inflations in these structures have a granular-appearing content (Plate III, 4); others contain small spheroidal bodies (up to 6 µm in diameter) of unknown nature (arrow in Plate III, 4).

### 3.2.2. Reproductive units

In addition to the hyphae, various types of reproductive units are also found in the cells of the xylem. One of them is spherical, 40–55 µm in diameter, thin-walled, and usually rests on, or is somehow connected to, the host cell wall (Plate III, 6–8); subtending hyphae have not been observed, with one possible exception (arrow in Plate III, 8), but some specimens are closely associated with *type-2* hyphae in the host cell wall on which they rest (arrow in Plate III, 6). Other spheroidal reproductive units in xylem cells are smaller, 25–35 µm in diameter, and have a relatively thick wall (Plate III, 10); a fragment of the subtending hypha is still present in some of them. In addition, a single specimen of a minute thallus (less than 20 µm in diameter) comprised of a central cavity with a discharge tube surrounded by what appears to be a prominent sheath has been found attached to a host cell wall (Plate III, 12). Finally, a large, ovoid glomeromycotan spore (c. 160 µm long and 125 µm wide) is located in between the secondary xylem and the periderm (Plate III, 13); a short segment of the subtending hypha is still attached (Plate III, 14), suggesting that the spore is glomoid.

### 3.2.3. Fungal trace fossils

Many of the tracheids filled with an amber-colored to brown substance show almost perfectly preserved fungal hyphae, which do not seem to have changed at all in shape and course due to desiccation and biological degradation prior to fossilization and the process of fossilization itself (Plate IV, 3–11). These hyphae are not body fossils, but trace fossils in the form of hollows in the solidified amber-colored to brown substance; only vestiges, if any, of the actual hyphal walls are preserved (e.g., Plate IV, 2). However, body fossils of hyphae (predominantly *types 2* and 3) also occur in some of the filled tracheids, in a few cases together with trace fossils. There are also tracheids that are only partially filled with the amber-colored to brown substance (Plate II, 1). The filled part in some of these cells contain fungal trace fossils, while the unfilled part contains body fossils (Plate II, 17; Plate IV, 1).

Trace fossil hyphae can only be vaguely recognized under the microscope and can only be properly brought out with the help of various color gradients and photo filters in Photoshop (e.g., compare Plate II, 17 [arrow; no color gradient nor photo filter applied] with Plate IV, 3–11). From the images processed in this way, one can see that the hyphae are between 1 and 6.8 µm wide, tubular or somewhat irregular, and un-branched (Plate IV, 3) or irregularly branched (Plate IV, 5, 6, 11), with the branches usually (but not always) being narrower than the hyphae from which they are given off (Plate IV, 5). When penetrating the wall of a host cell, the diameter of the hypha is in most cases slightly to greatly reduced (Plate IV, 3 [arrow] + inset, 4, 6, 7), but returns to its normal width immediately after exiting the wall. Some hyphae form a pear-shaped, appressorium-like swelling (up to 5.5 µm wide) before entering a host cell wall (arrow in Plate IV, 7), and others have a series of consecutive constrictions at some distance before entering the wall (Plate IV, 8). Of particular interest are hyphal formations which are almost certainly clamp connections (arrows in Plate IV, 4, 5 + inset), some of which appear to possess an open slit (black arrow in the inset in Plate IV, 4) between the hyphal septum (lower white arrow in the inset in Plate IV, 4) and the clamp. A few spherical or ovoid intercalary hyphal
<figure><img src="image_7.png" /><figcaption>**Plate III.** Fungal remains in xylem – *Type-4* hyphae and fungal reproductive units. 1–3. Complex three-dimensional structures formed by *type-4* hyphae, each shown in several focal planes; arrows in *Plate III*, 1b, c point to septa, arrows in *Plate III*, 2b show entry site of fungus. 4. Three-dimensional structure containing a spheroidal body of unknown nature (arrow) in a swelling. 5. Three-dimensional structure that almost completely occludes a tracheid. 6. Spherical reproductive unit lying on a tracheid wall (cw) and closely associated with a *type-2* hypha extending through the wall (arrows). 7, 8. Spheroidal to ovoid reproductive units lying on tracheid cell walls; arrow in *Plate III*, 8 indicates short segment of putative subtending hypha. 9, 11. Simple reproductive units in periderm cells, with fragment of subtending hypha (arrows) still attached. 10. Thick-walled (or sheathed) reproductive unit or propagule in lumen of a tracheid. 12. *Perexiflasca*-like thallus attached to a tracheid wall. 13, 14. Large glomoid spore in poorly preserved extraxylary tissue between secondary xylem and periderm. Scale bars: 13 = 200 µm; 5–7, 14 = 50 µm; 1–4, 8, 10 = 20 µm; 9, 11, 12 = 10 µm.</figcaption></figure>
<figure><img src="image_8.png" /><figcaption>**Plate IV.** Fungal remains in xylem – Trace fossils in cells filled with an amber-colored to brown substance. 1. Partially filled tracheid containing body fossils of *type-1* and *type-2* hyphae in the unfilled part and trace fossil hyphae in the filled part. 2. Hyphae with only vestiges of the hyphal walls still preserved. 3. Hypha passing through a cell wall into the lumen of a tracheid; note hyphal diameter greatly reduced in cell wall, but returning to normal width after exiting the wall (arrow + inset in inverted light). 4, 5. Branched hyphae with clamp connections (arrows); inset (inverted light) in *Plate IV*, 5: close-up of clamp connection with open slit between hyphal septum (lower white arrow) and clamp (black arrow); upper white arrow indicates second septum. 6. Irregularly branched hypha showing a reduction in diameter before entering a tracheid wall (cw). 7. Hypha forming an appressorium-like swelling (arrow) before passing through a tracheid wall (cw). 8. Hypha with a series of consecutive constrictions before entering a tracheid wall (cw). 9. Large intercalary hyphal swelling. 10. Ovoid reproductive unit with subtending hypha (arrow) attached to tracheid wall (cw). 11. Bundle of hyphae (arrows) passing through a tracheid wall (cw) and into the cell lumen. Scale bars: 1 = 50 µm; 9 = 20 µm; 2–8, 10, 11 = 10 µm.</figcaption></figure>

swellings (Plate IV, 9) and reproductive units (Plate IV, 10) have also been preserved in this way.

### 3.2.4. Fungal remains in the periderm

Fungal remains are also found in the periderm, but in much lower frequency than in the xylem. Relatively wide (2–2.5 µm wide) and narrow (less than 1.5 µm wide) tubular hyphae similar to *type 2* and *type 3* were observed in several cells (Plate II, 4, 5), as well as various thin-walled spheroidal or ovoid reproductive units (probably chlamydot-spores) up to 12 µm in diameter (arrow in Plate II, 4; Plate III, 9, 11), the latter in most cases with a short segment of the subtending hypha still attached (arrows in Plate III, 9, 11). In some (less than 10%) periderm cells, conical cell wall appositions up to 6 µm long and proximally 6.5 µm wide have formed in response to the entry of narrow hyphae. In

many of these formations the penetrating hypha can be seen in the center of the apposition (arrows in Plate II, 5).

## 4. Discussion

It is widely believed that the fungi of the Carboniferous and early Permian coal swamp forests formed a wide variety of associations and interactions with the plants that lived in these ecosystems (Cross and Phillips, 1990; Krings et al., 2012a; Nelsen et al., 2016; Naranjo-Ortiz and Gabaldón, 2019; Harper and Krings, 2021). Because many of these plants were large, long-lived, and complex in their morphology and internal organization (Taylor et al., 2009; Wilson et al., 2017), they provided numerous contact sites and ecologically different habitats for fungal biotrophs and saprotrophs. It is therefore not surprising that
diverse assemblages of fungal remains have been discovered within a number of structurally preserved Carboniferous–early Permian plants. For example, different types of hyphae, reproductive units, and propa-gules (spores), as well as evidence of a host response in the form of elongated conical cell wall appositions, co-occur in Carboniferous lycophyte xylem and periderm from France and Great Britain (Krings et al., 2007, 2009a, 2010e), and similarly diverse assemblages have been found in Carboniferous cordaite and seed fern foliage (Krings et al., 2011c, 2014). The best-preserved fungal community to date has been described from the root mantle of a Psaronius gimmii M. Barthel et al. stem from the lower Permian of Germany (Barthel et al., 2010; Krings et al., 2017b). The majority of these discoveries were made in historical thin sections of plant fossils described in the late 19th and first half of the 20th century. In principle, this is also the case for the fungal assemblage presented in this study in a Sphenophyllum stem from the Autun Basin, except that neither the fungi nor the host plant had been comprehen-sively described before.

## 4.1. Host: Affinities and comparisons

The genus Sphenophyllum was originally established based on impression and compression fossils (e.g., Brongniart, 1822, 1828; Coe-mans and Kickx, 1864; Williamson, 1892), but Renault (1873, 1876, 1878) accommodated in this taxon also permineralized stems charac-terized by (i) a triangular primary xylem; (ii) an exarch protoxylem; and (iii) a fascicular and interfascicular secondary xylem (for details, refer to Batenburg, 1982; Rößler et al., 2021). The affiliation of the stem cross section described in this study to Sphenophyllum is undoubted based on these characters.

Seven species of structurally preserved Sphenophyllum stems have been formally described from Europe and North America, namely S. insigne Williamson et Scott (Williamson, 1874; Williamson and Scott, 1894), S. plurifoliatum Williamson et Scott (Williamson, 1874; Wil-liamson and Scott, 1894), S. stephanense Renault (=S. quadrifolium Renault, S. renaultii Phillips [Renault, 1873, 1876; Phillips, 1959; Boureau, 1964; Doubinger et al., 1995]), S. gilkinetii Leclercq (Leclercq, 1924), S. perforatum Koopmans (Koopmans, 1928), S. minus Koopmans (Koopmans, 1928), and S. constrictum Phillips (Phillips, 1959). However, S. gilkinetii, S. minus, and S. perforatum are very similar to S. plurifoliatum, and therefore cannot be considered as separate species (e.g., Baxter, 1948; Phillips, 1959; Schabilion and Baxter, 1971). In addition, S. constrictum has been found in physical connection with S. plurifoliatum (Good, 1973), leaving three "good" species for permineralized Spheno-phyllum stems. Sphenophyllum insigne has protoxylem lacunae and rays crossing the entire thickness of the interfascicular secondary xylem (Williamson and Scott, 1894; Baxter, 1948; Rößler et al., 2021), while the stem described here lacks evidence of protoxylem lacunae, and its rays do not cross the entire secondary xylem. Sphenophyllum stephanense is vaguely defined. The main characters are the number of leaves per node and the pattern of leaf emission (Renault, 1878), which cannot be determined on the fossil discussed here due to the inherent limitations of the specimen. The third species, S. plurifoliatum (Williamson, 1874; Williamson and Scott, 1894), has secondary xylem with parenchyma between cells connected by elongated cells that rarely cross the entire thickness of the secondary xylem, true phloem, and an internal periderm layer that can form regular scale-bark (i.e. banded aspect of the peri-derm [Eggert and Gaunt, 1973; Decombeix and Galtier, 2021]). Tra-cheids in this species are on average 160 µm in diameter (Cichan, 1985). The species appears to be highly variable, however, which has led to the majority of anatomically preserved large specimens of Sphenophyllum found in North America, Europe, and Russia being assigned to this taxon (Good, 1973). The cross section described in this study seems to be more closely related to S. plurifoliatum than any other permineralized Sphe-nophyllum stem.

Sphenophyllum plurifoliatum has been hitherto unknown from the Autun Basin, Grand-Croix, and the Montagne Noire, the three French

regions where anatomically preserved specimens of Sphenophyllum have been found (Galtier, 2008; Terreaux De Felice et al., 2019). If the stem described here is indeed S. plurifoliatum, then it would be of interest not only as a host for a well-preserved fungal community, but also because it would represent the first record of this species from France.

## 4.2. Fungal remains

### 4.2.1. Affinities and comparisons

There is only one report to date of fungi associated with the aerial parts of a fossil sphenophyte, namely Sphenophyllum leaves from the Upper Pennsylvanian Grand'Croix chert of France that house several types of fungal remains, including putative chytrid zoosporangia, propagules, and mycelia with intercalary swellings (Dotzler et al., 2011). However, none of these fossils morphologically match the fungal remains described in his study.

Interpreting the systematic affinities of the fungal remains in the Sphenophyllum stem from Autun is difficult, if not impossible in some cases, because, with one possible exception (see below), they are not complete organisms, but individual parts or life history stages of or-ganisms. For the same reason, it is not possible to determine the exact number of biological species represented in the assemblage. The different fungal remains are most certainly not all separate species. Conversely, it is also possible that the more common remains represent several morphologically similar species. For some of the fungal remains, however, we can make cautious assumptions about their systematic placement based on morphological characteristics and comparisons with other fossil and present-day fungi.

The *type-1* and *type-2* hyphae (Plate II, 1–11; Plate IV, 10), as well as the terminal hyphal inflations physically connected to (Plate II, 11), or closely associated with (Plate III, 6, 7), some of the *type-2* hyphae, belong to the same fungal species, perhaps a member of the Glomer-omycota (arbuscular mycorrhizal fungi) or zygomycete fungi if the hy-phal inflations are actually sporangia or spores. One of the few structural features by which fossil zygomycete fungi can be reliably distinguished from Glomeromycota is the sexual stage of the life cycle, which occurs in the former through zygosporogenesis after gametangial fusion, but is unknown in the latter (Krings et al., 2013). The fossils discussed here cannot be identified as a zygomycete fungus, as there is no evidence of zygosporangium-gametangia complexes. The occurrence terminally on a tubular hypha rather suggests that the inflations are glomoid chla-mydospores (e.g., compare the fossils to Magurno et al., 2024: figs. 1A, B, F, 2B), which have formed asexually by blastic inflation and thick-ening of a hyphal tip. Likewise, the single large ovoid spore located in the ill-preserved tissue between the xylem and the periderm (Plate III, 13, 14) probably also belongs to the Glomeromycota. However, there is no evidence to date that Sphenophyllum and glomeromycotan fungi formed mycorrhizal symbioses, as is known for some other coal swamp plants, including marattialean ferns (Wagner and Taylor, 1982), arbo-rescent lycophytes (Krings et al., 2011b), and cordaites (Strullu-Derrien et al., 2009).

The affinities of the *type-3* (Plate II, 12–15) and *type-4* hyphae (Plate II, 16–18) remain unknown. However, the latter are interesting because of the catenulate hyphal swellings (Plate II, 18) and the peculiar three-dimensional structures formed in some host cells (Plate III, 1–5). Although they have a very different structure and are much larger, the latter structures are still somewhat reminiscent of the coralloid struc-tures found in root cortical cells of the early Permian Psaronius gimmii (Krings et al., 2017b), which are assumed to have been produced by a member of the fungus-like Oomycetes (Peronosporomycetes). It has been hypothesized that these structures in *P. gimmii* were effective as some type of physiological interface. They may have functioned as haustoria, which form inside a living host cell as a branch of an extra-cellular (or intercellular) hypha or thallus (Bushnell, 1972; Szabo and Bushnell, 2001; Judelson and Ah-Fong, 2019; Mapuranga et al., 2022). However, the tracheids in which the fossil structures occur are not living
cells (at maturity), and there is no evidence of intercellular *type-4* hyphae in the *Sphenophyllum* stem. Alternatively, the three-dimensional structures could be irregularly swollen sporangia, similar to those of the present-day oomycete *Pythium catenulatum* V.D. Matthews (Androusse et al., 2007: figs. 10–15), or comparable to the sporangia of *Pythium torulosum* Coker et Patterson and *Pythium kashmirensis* Paul, among other taxa, which all consist of inflated branched outgrowths of the mycelium forming toruloid complexes of varying size (Cooker and Patterson, 1927: figs. 2–4; van der Plaats-Niterink, 1981: figs. 3b, 84b; Paul and Bala, 2008: fig. 1c). In addition, a few of the fossil swellings have a granular-appearing content and look very similar to the imma-ture sporangia of some present-day oomycetes (e.g., compare Plate III, 4 with Salmaninezhad et al., 2024: fig. 5e). Nevertheless, the location of the structures in tracheids renders this option rather unlikely. Yet another possibility is that these structures served as storage sites, perhaps in a similar manner as vesicles in present-day Glomeromycota (e.g., Herrmann, 1995; Walker et al., 2018). Vesicles are structures in which these fungi store energy as lipids for use in times of limited re-sources. Moreover, by accumulating phosphorus in these structures, they may have an important resource that they can make available to the plant host if phosphorus is scarce (Helgason and Fitter, 2009; Olsson et al., 2011; Bach et al., 2018). However, there is currently no direct evidence that the *type-4* hyphae belong to the Oomycetes or the Glomeromycota.

Some of the hyphae preserved as trace fossils show structures that are almost certainly clamp connections (Plate IV, 4, 5 + inset). Clamp connections are hyphal protrusions known exclusively in Basidiomycota that develop during cell division to maintain the binucleate (dikaryon) condition (Furtado, 1966; Oberwinkler, 2012). More recently, it has been hypothesized that they are also effective as screening devices for the quality of nuclei, with both nuclei continuously testing each other for fusion capability (Aanen et al., 2023). Clamp connections are clas-sified based on, among other features, the ratio of clamp size to hyphal diameter (Stalpers, 1978; Buchalo et al., 1983, 2011). The structures described here can be identified as large clamps, in which the hypha and the clamp have approximately the same width. A recent phylogenomic analysis suggests that the subphyla of the Basidiomycota diverged in the Ordovician, in a time range of 490–443 million years (He et al., 2024). However, the oldest fossil evidence of hyphae with clamp connections comes from the Mississippian of France (in *Botryopteris antiqua* Kidston; Krings et al., 2011a) and the Pennsylvanian of North America (in *Zygopteris illinoiensis* (Andrews) Baxter; Dennis, 1969, 1970). Slightly younger, early Permian hyphae with clamp connections have been re-ported from Germany (in *Psaronius gimmii*; Krings et al., 2017b) and China (in *Shanxioxylon* sp.; Wan et al., 2017). So far there has been no fossil evidence of Basidiomycota in association with sphenophytes.

Finally, a minute but nonetheless noteworthy fossil in the stem is shown in Plate III, 12. Based on morphology, this fossil can be attributed with confidence to the fossil-genus *Perexiflasca* M. Krings et al., first described from the Lower Devonian Rhynie cherts of Scotland (Taylor et al., 1992; Krings et al., 2017a; Krings and Harper, 2019). *Perexiflasca* occurs singly or in clusters of up to more than 100 specimens attached to the walls of plant cells and large fungal spores. The fossil has been interpreted as a sheathed zoosporangium of a eucarpic, monocentric chytrid-like organism (Krings et al., 2017a). There are also two Carboniferous microfossils that correspond to the morphology of *Per-exiflasca*, one from the Mississippian and one from the Pennsylvanian of France (Krings et al., 2009a, 2011c). Krings and Harper (2019) point out that the occurrence of *Perexiflasca*-like fossils in the Devonian, Missis-sippian, and Pennsylvanian may provide a very rare opportunity to study microbial life through deep time. The specimen described here adds the first early Permian record to this inventory.

### 4.2.2. Formation of trace fossils

Trace fossils of fungal structures in permineralized plants have, to our knowledge, never been reported. Their abundance in the

*Sphenophyllum* stem from Autun therefore raises the question of how they originated. Almost all fungal body fossils in this stem show at least some degree of structural change compared to their in vivo state, e.g., in the form of fragmentation, collapse, shrinkage, displacement within the host cell, or partial decay. The almost perfect preservation of certain hyphae as trace fossils exclusively in tracheids that are filled with an amber-colored to brown substance indicates that this substance may have played a role in trace fossil formation. We speculate that the amber-colored to brown substance was already present in the cells during the lifetime of the fungi and, at some point, it solidified and enshrined every fungal structure in these cells. In this way, the original shape and course of the hyphae could have been preserved even after the decay of the hyphal walls. The fact that body fossils of hyphae also occur in some of the filled cells might be due to the intrusion of other fungi into the cells containing the already solidified substance at a later stage. However, it is more likely that the hyphae later to become body fossils were in the cells at the same time as those that became trace fossils, but that they are different fungi whose hyphal walls are differently resistant to decay. Support for this hypothesis is the fact that no evidence of hyphae with clamp connections was found in any of the cells that are not filled with the amber-colored to brown substance.

All these considerations naturally raise the question of what the special substance in the filled cells might be. Plants produce a variety of occlusions in their vascular tissues in response to biotic and abiotic stresses, which can be divided into two main categories, namely tyloses on the one hand and gels or gums on the other (Sun et al., 2008; De Micco et al., 2016). Both are produced by the parenchyma cells in the xylem. Tyloses are outgrowths of parenchyma cells into the lumen of neighboring conducting cells, while gels (or gums) are amorphous substances secreted by parenchyma cells that fill the conducting cells (Sun et al., 2008). Although tyloses are known in plants from the Late Devonian (Decombeix et al., 2023), and have been observed in sphe-nophytes since the Carboniferous, they have not yet been found in *Sphenophyllum* (Decombeix et al., 2022). Plants today can produce either only tyloses, or only gel, or both, and this can also vary depending on the time of year when colonization with the pathogen begins (Sun et al., 2008). No tyloses were observed in the *Sphenophyllum* stem described here, despite extensive fungal colonization, but the occluding material in this case may have been a gel, as it has a uniform texture and shows an outline when the cell is only partially filled (Plate IV, 1). Hyphae in a present-day plant vessel filled with gel have been illustrated by Muta-wila et al. (2011: fig. 1D), but these hyphae appear to have grown through the gel, rather than being enshrined by the gel. To our knowl-edge, there is no published report of hyphae trapped inside a gel. The amber-colored or brown substance in the fossil is therefore probably a solidified gel, but more analyses (e.g., geochemical) are needed to un-derstand this phenomenon in detail.

### 4.2.3. Nature of the associations

The nature of the biological relationship between the various fungi and the host plant remains largely unknown in detail, as both the host and the fungi are only incompletely preserved. The fungi could be either biotrophs or saprotrophs. The only evidence of a biotrophic (parasitic) relationship occurs in the form of small conical cell wall appositions found in several of the periderm cells (Plate II, 5). Cell wall appositions (also called lignotubers, papillae, or Röhrentüpfel, among other terms; see Leroux et al., 2011) are inwardly directed projections consisting of newly synthesized wall material that are formed by living plant cells (but also by certain fungal spores, where they are called callosities; see Swart, 1975; Purin and Rillig, 2008) in response to invading fungi or some other biotic cause. They encase the infection hyphae or filaments and, in this way, prevent or at least decelerate the penetration of the parasite (e.g., Pearce, 1996; Schulze-Lefert, 2004; Collinge, 2009). This type of host reaction has previously been documented in several Car-boniferous-early Permian plant lineages, including arborescent lyco-phytes (Krings et al., 2009a, 2010e), marattialean and filicalean ferns
(Krings et al., 2011a, 2017b), gymnosperms (Stubblefield et al., 1984), and calamitalean sphenophytes (Taylor et al., 2012). The cell wall appositions described here are the first evidence in sphenophyllalean sphenophytes.

The nutritional mode of the fungi in the xylem is far more difficult to assess. There is no evidence of a host response nor of any particular fungal features that might indicate a relationship with a living host, perhaps with the exception of the compact three-dimensional structures formed by the *type-4* hyphae (Plate III, 1–5), if one assumes that these structures are indeed functionally similar to haustoria. Harper and Krings (2021) state that a distribution pattern of fungi in an intact host that reflects forced invasion and a consistent pathway of colonization (e. g., along the vascular bundles or rays), or that is restricted to specific parts or tissue types of the host, is indicative of colonization of a living host, whereas colonization of dead and decaying plant parts is more likely to result in random fungal distribution. The numerous fungal remains, likely from multiple fungal species, throughout the primary and secondary xylem of the *Sphenophyllum* stem, as well as evidence of incipient mechanical destruction and degradation of the stem, would therefore be indicative of post mortem colonization by saprotrophic fungi. However, a reliable evaluation of fungal distribution on the basis of a single cross section is not possible. For example, the section does not provide any information about where and how the fungi have entered the stem and how they have spread from there.

## 5. Conclusions

A thin section from the collection Roche in Autun, France, of a permineralized early Permian *Sphenophyllum* stem in cross section from the Autun Basin shows the presence of a variety of fungi, including a *Perexiflasca*-like chytrid, greatly inflated hyphal tips resembling gloomoid spores, hyphae with clamp connections, and three-dimensional hyphal formations of unknown function and affinity. Cell wall appositions in periderm cells are evidence that at least one of the fungi colonized the stem while it was alive. Most of the fungal remains are body fossils, but some hyphae in tracheids filled with an amber-colored to brown substance, perhaps a type of gel or gum, appear as trace fossils. There are a number of comprehensive descriptions of structurally preserved *Sphenophyllum* stems in the literature (e.g., Renault, 1873, 1876, 1878, 1896b; Williamson and Scott, 1894; Baxter, 1948; Reed, 1949; Snigirievskaya, 1959; Schabilion and Baxter, 1971; Good and Taylor, 1972; Eggert and Gaunt, 1973; Good, 1973; Cichan and Taylor, 1982; Wang et al., 2009; Terreaux De Felice et al., 2019; Rößler et al., 2021), but none that also report on the presence of fungi. Whether fungi were observed but not described, or whether there are no fungal remains in all these specimens, remains to be clarified. The present study is a good example of how worthwhile it can be to revisit old collections and reanalyze specimens that, one should assume, have already been intensively studied. The fact that the fungi in the *Sphenophyllum* stem from Autun have not been described is all the more surprising given that the specimen was prepared by Auguste Roche, a close collaborator of Bernard Renault, who was a pioneer in the study not only of structurally preserved *Sphenophyllum*, but also of fossil fungi. Our discovery contributes to the knowledge of fungal associations in Carboniferous-early Permian sphenophytes, a group of free-sporing vascular plants that today comprises only a single genus, *Equisetum*, with less than 20 species of herbaceous perennials, but was then much more diverse, both in terms of species number and growth habits (Husby, 2013). Because sphenophyte cell walls are characterized by an uncommon polysaccharide composition and the deposition of silica (e.g., Perry and Fraser, 1991; Fry et al., 2008), it would be especially interesting to find out how similar or dissimilar the fungal communities associated with fossil representatives of this group of plants are compared to the fungal communities in other plants of the same habitats. We therefore hope that in the course of further research on structurally preserved plants, more specimens of *Sphenophyllum* and other sphenophytes colonized by fungi

will be discovered and described, which may lead to a more complete documentation of fungal relationships in this group of plants over time.

## Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

## Acknowledgments

This work is part of the Trinity College Dublin (TCD), Ireland, PhD project "Early woody plant diversity and biology: An integrative evolutionary and palaeoenvironmental study" of TD, which is funded by a TCD Provost's Award to CJH. We gratefully acknowledge D. Chabard (Autun, France) for making the collection Roche available for study and J. Galtier (Montpellier, France) who noticed this particular slide of *Sphenophyllum* in the collection. We also thank A.M.F. Tomescu (Arcata, USA) and an anonymous referee for insightful comments on the manuscript.

## Data availability

The authors confirm that all data necessary for supporting the scientific findings of this paper have been provided.

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