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ORIGINAL ARTICLE
Germination shields in Scutellospora (Glomeromycota:
Diversisporales, Gigasporaceae) from the 400
million-year-old Rhynie chert
Nora Dotzler &Michael Krings &Thomas N. Taylor &
Reinhard Agerer
Received: 13 March 2006 / Revised: 27 June 2006 /Accepted: 29 July 2006
#German Mycological Society and Springer 2006
Abstract Glomeromycotan spores from the Lower Devo-
nian Rhynie chert provide the first evidence for germina-
tion shields in fossil fungi and demonstrate that this
complex mode of germination was in place in some fungi
at least 400 million years ago. Moreover, they represent
the first direct marker relative to the precise systematic
position of an Early Devonian endomycorrhizal fungus. In
extant fungi, germination shields occur exclusively in the
genus Scutellospora (Glomeromycota: Diversisporales,
Gigasporaceae). These structures are regarded as a derived
feature within the phylum Glomeromycota, and hence their
presence in the Rhynie chert suggests that major diversifi-
cation within this group of fungi occurred before the Early
Devonian.
Keywords Arbuscular mycorrhiza .Evolution .
Germination .Pragian (Early Devonian) .Spore wall
Introduction
The Early Devonian Rhynie chert has provided a wealth of
insights into the diversity of fungal life some 400
million years ago. As a result, members of the Chytridio-
mycota, Zygomycota, Glomeromycota and Ascomycota are
today known in great detail from this palaeoecosystem;
many of the Rhynie chert fungi have also been demon-
strated in various interactions with other organisms (sum-
marised in Taylor et al. 2004 and Taylor and Krings 2005).
Among these interactions are several examples of arbus-
cular mycorrhizae (e.g. Remy et al. 1994; Taylor et al.
1995,2005). The fungal partners consist of aseptate hyphae
that enter the rhizomatous axes of various land plants and
extend through the intercellular system of the outer cortex.
The formation of intracellular arbuscules within a well-
defined region of the cortex (termed the ‘mycorrhizal
arbuscule zone’) substantiates these fungi as endomycor-
rhizal. The mycorrhizal fungi from the Rhynie chert have
been assigned to the Glomeromycota based on structural
similarities to extant representatives in this phylum of
fungi and corresponding mode of mycorrhiza formation
(cf. Taylor et al. 1995; Helgason and Fitter 2005);
however, to date, none has been classified in greater detail
and related to a particular modern taxon.
Glomeromycota is a monophyletic phylum that includes
the arbuscular mycorrhizal (AM) fungi (Schüßler et al.
2001; Helgason et al. 2003; Corradi et al. 2004). It is
estimated that more than 80% of vascular plants today live
in symbiosis with these fungi (Smith and Read 1997).
Molecular clock estimates based on amino acid sequences
suggest that the Glomeromycota separated from other
Mycol Progress
DOI 10.1007/s11557-006-0511-z
Taxonomical novelties
Scutellosporites Dotzler, M. Krings, T.N. Taylor and Agerer
Scutellosporites devonicus Dotzler, M. Krings, T.N. Taylor and Agerer
Stürmer 1998
N. Dotzler :M. Krings (*)
Bayerische Staatssammlung für Paläontologie und Geologie und
GeoBio-Center
LMU
,
Richard-Wagner-Straße 10,
80333 Munich, Germany
e-mail: m.krings@lrz.uni-muenchen.de
N. Dotzler :R. Agerer
Department Biologie I und GeoBio-Center
LMU
,
Bereich Biodiversitätsforschung: Mykologie,
Ludwig-Maximilians-Universität München,
Menzinger Straße 67,
80638 Munich, Germany
M. Krings :T. N. Taylor
Department of Ecology and Evolutionary Biology,
and Natural History Museum and Biodiversity Research Center,
The University of Kansas,
Lawrence, KS 66045-7534, USA
fungal groups ∼1,200 myBP (Heckman et al. 2001); more
conservative estimates place the divergence at about 600–
700 myBP (Berbee and Taylor 2001). Despite the proposed
antiquity of the Glomeromycota, early fossil representatives
are rare. Thick-walled spores suggested to be those of
Glomeromycota have been reported from Precambrian
sediments (Pirozynski and Dalpé 1989 and references
therein). Similar spores are known from the Ordovician of
North America (Redecker et al. 2000,2002). In none of
these accounts, however, is there any information regard-
ing associations with plants. Glomeromycotan spores in
tissues of late Palaeozoic land plants have been described
from the Upper Devonian of Canada (Stubblefield and
Banks 1983) and the Carboniferous of North America
(Wagner and Taylor 1982). Moreover, hyphae or hyphae-
like structures, aggregated in cortical tissues of the
underground parts of several Carboniferous plants have
variously been interpreted as arbuscules (e.g. Weiss 1904;
Osborn 1909;Halket1930; Agashe and Tilak 1970);
however, most of these reports have later been questioned
and the structures re-interpreted as non-fungal (coalesced
cell contents) or non-mycorrhizal (cf. Stubblefield and
Taylor 1988). The earliest persuasive evidence for glo-
meromycotan mycorrhizae in seed plants occurs in the
form of non-septate hyphae, vesicles, arbuscules and
clamydospores in silicified roots of the Triassic cycad
Antarcticycas schopfii Smoot, T.N. Taylor and Delevoryas
(Stubblefield et al. 1987; Phipps and Taylor 1996). Thus,
the Rhynie chert mycorrhizae represent the earliest fossil
evidence for Glomeromycota in symbiosis with land plants
(Remy et al. 1994; Redecker 2002).
Also present in the Rhynie chert are different types
of fungal spores. However, these remains have been
largely neglected as a source of information about the
diversity of fungi in this palaeoecosystem. In this study,
we describe glomeromycotan spores from partially de-
graded axes of the Rhynie chert land plant Asteroxylon
mackiei Kidst. and W.H. Lang that display a complex mode
of germination involving the formation of a germination
shield. The fossil spores can be directly related to a
particular modern taxon because, in extant fungi, this
mode of germination is restricted to species in the genus
Scutellospora C. Walker and Sanders (Glomeromycota:
Diversisporales, Gigasporaceae).
Materials and methods
The Rhynie chert Lagerstätte, an in situ silicified Early
Devonian palaeoecosystem, is located in the northern part
of the Rhynie outlier of Lower Old Red Sandstone in
Aberdeenshire, Scotland. The cherts occur in the upper part
of the Dryden Flags Formation, in the so-called Rhynie
Block, a few hundred metres northwest of the village of
Rhynie. The Lagerstätte consists of at least 10 fossiliferous
beds containing lacustrine shales and cherts that are
interpreted as a series of ephemeral fresh water pools
within a hot springs environment. The chert-bearing
formation is Pragian in age and has been radiometrically
dated to 396±12 Ma. Detailed information about the
geology and palaeontology of the Rhynie chert Lagerstätte
can be found in Trewin and Rice (2004).
Spores were identified in petrographic thin-sections
prepared by cementing a thin wafer of the chert to a glass
slide and then grinding the rock slice with silicon carbide
powder until it becomes sufficiently thin for examination in
transmitted light (cf. Hass and Rowe 1999). Slides are
deposited in the Bayerische Staatssammlung für Paläonto-
logie und Geologie, Munich (Germany), under accession
numbers BSPG 1964 XX 625 and 631, and BSPG 1964
XX 31.003, 31.005 and 31.006. For comparison, spores of
Scutellospora castanea C. Walker (BEG 1: produced on
onion, in neutral soil) were fixed and embedded in PVLG
(Polyvinyllactoglycerol) according to a procedure outlined
in Walker (1979) and studied in transmitted light.
Description
Spores with germination shield occur in cortical tissues of
partially degraded axes of the early lycophyte Asteroxylon
mackiei; a total of 12 specimens of this type of spore have
been discovered to date. Spores are globose to subglobose,
260–350 μm in diameter and possess a non-ornamented
surface (Fig. 1a). The spore wall is subdivided into two
wall groups. The outer wall group is well preserved, up to
18 μm thick and two- or three-layered. A distinct dark layer
(∼3to4μm thick; cf. arrow in Fig. 1a) occurs on the inner
surface of the outer wall group. This layer either represents
the inmost part of the outer wall group or the outmost layer
of the inner wall group. The original thickness and
composition of the inner wall group are difficult to
estimate. A translucent region, up to 30 μm thick, occurs
between the dark layer and outer surface of the spore
lumen. It is not entirely clear, however, whether this region
represents the original thickness of the inner wall group or
is the result of shrinkage of both the inner wall group layers
and spore lumen during fossilisation. The germination
shield extends along the inner surface of the dark layer
(Fig. 1a–e); the original location of the shield is difficult to
reconstruct due to the lack of details about the composition
of the inner wall group. The germination shield is round or
oval in outline, ∼140 μm in diameter and up to 15 μm high.
It is distinctly lobed, with each of the lobes 25–33 μm
wide, or displays a complex infolding along the margins
(appearing in section to consist of compartments,
Mycol Progress
cf. Fig. 1a,b). In one of the spores, the connection of the
germination shield to the spore lumen is apparent
(Fig. 1a–c). Another specimen shows what we interpret as
a germ tube that is formed by the germination shield and
penetrates the outer wall group (Fig. 1e). Unfortunately,
none of the spores with germination shield displays a
subtending hypha or suspensor-like base. However, in
one of the A. mackiei axes, a structurally similar but
somewhat smaller (i.e. 190×150 μm in diameter) spore
without germination shield occurs that is attached to a
slightly bulbous subtending hypha (Fig. 1f), which is up to
18 μm in diameter and remotely resembles the character-
istic suspensor-like base seen in extant Scutellospora
species (e.g. Fig. 1g).
Relationships
The fossil spores are similar to spores produced by species
in the extant genus Scutellospora (Glomeromycota: Diver-
sisporales, Gigasporaceae). Scutellospora consists of some
20 species of arbuscular mycorrhizal fungi, all of which
Fig. 1 Scutellosporites devonicus Dotzler et al. from the Rhynie chert
(a–f) and spores of the extant Scutellospora castanea C. Walker (g–k).
aSection through a fossil spore with germination shield. Arrow
indicates the distinct dark layer that either represents the inmost
portion of the outer wall group or outmost layer of the inner wall
group. Bar=50 μm. bDetail of a, focusing on the germination shield.
Bar=35 μm. cGermination shield in near median longitudinal section.
Bar=35 μm. dGermination shield in oblique surface view, showing
lobes/infoldings along the margin. Bar=20 μm. eGerm tube
penetrating the outer wall group. Bar=30 μm. fSlightly bulbous base
of a smaller glomeromycotan spore in Asteroxylon mackiei.Bar=20μm.
gSame as f, but from the extant S. castanea. Bar=30 μm. hSpore of S.
castanea with germination shield. Bar=50 μm. iDetail of h, focusing
on the germination shield. Bar=30 μm. jGermination shield of a second
S. castanea spore in optical longitudinal section. Bar=30 μm.
kGermination shield in oblique surface view. Arrows indicate the
margins of the shield. The infoldings are visible as narrow dark lines.
Bar=30 μm
Mycol Progress
produce large spores (between 120 and 640 μmin
diameter) with multi-layered walls. Germination includes
the formation of a germination shield, which is a
specialised structure that distinguishes Scutellospora from
the closely related genus Gigaspora Gerd. and Trappe
(Walker and Sanders 1986) and all other members of the
Glomeromycota. There are several other genera within the
Glomeromycota, e.g. Acaulospora Gerd. and Trappe
(Diversisporales, Acaulosporaceae) and Pacispora Oehl
and Sieverd. (Glomerales, Glomeraceae), in which spore
germination also includes the formation of a specialised
structure between two layers of the spore wall (e.g. Stürmer
1998; Stürmer and Morton 1999; Oehl and Sieverding
2004). However, this structure, termed the ‘germination
orb’, is more delicate, usually smaller (e.g. 14–26×20–
38 μminP. franciscana Oehl and Sieverd., cf. Oehl and
Sieverding 2004), less complex and clearly distinguishable
morphologically from the germination shields produced by
the Rhynie chert spores and extant Scutellospora. It is still
being debated whether germination orbs and germination
shields are heterologous structures or synapomorphies of
the Diversisporales lineage.
For comparison of the fossils with extant representa-
tives of Scutellospora, specimens of Scutellospora casta-
nea C. Walker were analysed (Fig. 1h–k). A complete
description of S. castanea is provided in Walker et al.
(1993) and we restrict our discussion to a brief character-
ization of the germination shield: In S. castanea, this
structure is oval in outline (Fig. 1k) and occurs on the inner
spore wall group. It is up to 210 μm long, 185 μm wide,
10–15 μm high and characterised by a complex infolding
along the margins (appearing in optical section to consist of
compartments, cf. Fig. 1h–j). Optical longitudinal sections
through shields of S. castanea are virtually indistinguish-
able from sections through the fossil germination shields
(compare Fig. 1a,b with Fig. 1i,j).
Based on the striking similarities in germination shield
morphology between the fossils and S. castanea, as well as
other species of Scutellospora detailed in the literature (e.g.
Koske and Walker 1986; Walker and Sanders 1986; Walker
and Diederichs 1989; Walker et al. 1998; Herrera-Peraza et
al. 2001), we interpret the fossils as belonging to an early
member of the genus Scutellospora. However, the fossil
spores only provide an incomplete picture of this fungus.
For example, none of the spores with germination shields
display a subtending hypha or specialised base. Because
extant Scutellospora spores are always borne on a charac-
teristic bulbous, suspensor-like base (Fig. 1g), documenta-
tion of this feature would strengthen the proposed affinities
of the fossil spores. A somewhat smaller fossil spore
(lacking germination shield), which co-occurs with the
large spores with germination shield, displays a slightly
bulbous base (Fig. 1f). We cannot establish at present
whether this spore belongs to the fungus that produced the
spores with germination shield. As a result, we refrain from
including the fossil spores with germination shield in
Scutellospora, but rather introduce a new genus, for which
the name Scutellosporites is proposed.
Taxonomy
Glomeromycota C. Walker and A. Schüßler
Diversisporales C. Walker and A. Schüßler
Gigasporaceae J.B. Morton and Benny
Scutellosporites Dotzler, M. Krings, T.N. Taylor and
Agerer, gen. nov.
Derivation of generic name. The name underscores the
similarity to the extant genus Scutellospora; the ending -ites
is used to designate a fossil taxon.
Generic diagnosis. Spores globose to subglobose, up to
350 μm in diameter, with non-ornamented surface; spore
wall composed of two wall groups; outer wall group >15 μm
thick, two- or three-layered; distinct dark layer present on
inner surface of outer wall group; germination by means of
germination shield extending along inner surface of dark
layer; shield round or oval, >100 μm long and >10 μmhigh,
distinctly lobed or with infolded margins.
Type species.Scutellosporites devonicus Dotzler et al.
Scutellosporites devonicus Dotzler, M. Krings, T.N.
Taylor and Agerer, spec. nov. Fig. 1a–f
Specific diagnosis. As for the genus
Derivation of specific epithet. Indicating the geologic
age of the fossil.
Holotype. BSPG 1964 XX 631 (Fig. 1a in this paper)
Type locality. Rhynie, Aberdeenshire, Scotland, National
Grid Reference NJ 494276
Age and stratigraphic position. Early Devonian (Pragian,
∼400 myBP)
Remark. Glomeromycotan spores that resemble Scutel-
losporites devonicus have been described from degraded
tissues of various Rhynie chert plants by Kidston and Lang
(1921)asPalaeomyces gordoni Kidst. and W.H. Lang.
However, in none of these spores is a germination shield
obvious. Because it is most likely that there existed more
than one taxon of mycorrhiza-forming glomeromycotan
fungi in the Rhynie chert, we refrain from assigning the
spores with germination shields specifically to P. gordoni.
Discussion
One of the remarkable discoveries in the Early Devonian
Rhynie chert is the presence of arbuscular mycorrhizae
that are strikingly similar to mycorrhizae today and were
produced by the same group of fungi, i.e. members of
Mycol Progress
the Glomeromycota (Remy et al. 1994; Taylor et al. 1995;
Helgason and Fitter 2005). Despite the detailed analyses
that have been carried out on these ancient mycorrhizae,
an exact systematic placement of the fungal partners has
not been possible to date, due primarily to the fact that
diagnostic features necessary in establishing the affinities
of a glomeromycotan fungus (e.g. spore wall structure
and colour, auxilliary cells) could not be determined with
the fossils.
The prominent germination shields described in this
study correspond to germination shields produced by the
extant Gigasporaceae genus Scutellospora,andthus
represent the first direct diagnostic marker that can be used
to determine the systematic position of one of the Rhynie
chert mycorrhizal fungi. In extant Glomeromycota, prom-
inent and well-recognizable germination shields are known
to occur exclusively in Scutellospora. Similar pre-germina-
tion structures (germination orbs) found in genera such as
Pacispora and Acaulospora are much more delicate and
become rarely visible, even in broken specimens or after
specific preparations of the inner wall (Spain 1992; Oehl
and Sieverding 2004). Members of Scutellospora display a
complex mode of germination, in which, before germ tube
formation, a germination shield is developed between two
layers of the spore wall. The position of the germination
shield varies between species of Scutellospora and may
occur between the individual layers of the inner wall group
(e.g. in S. scutata C. Walker and Dieder., cf. Walker and
Diederichs 1989) or on the surface of the inmost wall layer
(e.g. in S. castanea, cf. Walker et al. 1993). At maturity,
the germination shield produces one to several germ
tubes that penetrate the outer portion of the spore wall
(Walker and Sanders 1986). A satisfactory interpretation
with regard to the nature and function of the germination
shields has not been published to date. One interpretation is
that they are either sexual or parasexual, or perhaps asexual
vestiges of some previously sexual structure (C. Walker,
personal communication).
Because germination shields represent complex struc-
tures that consistently occur between distinct layers of
the spore wall, this feature is regarded as derived within
the Glomeromycota (Bentivenga and Morton 1996). As a
result, the presence of spores with germination shield in
the Rhynie chert suggests that major diversification
within this group of fungi occurred before the Early
Devonian. It is interesting to note, however, that the
derived state of the germination shield in the family
Gigasporaceae (i.e. Gigaspora and Scutellospora) has been
questioned based on molecular studies (Simon et al. 1993;
Redecker 2002). These authors hypothesise that Gigaspora
is an advanced rather than a plesiomorphic genus; species
in Gigaspora form a very narrow clade compared to the
large variation within Scutellospora (Schwarzott et al.
2001). It has also been suggested that Scutellospora may
be paraphyletic (Redecker 2002). Berbee and Taylor (2001)
estimate the divergence time between Gigaspora and two
species in the genus Glomus Tul. and C. Tul. at approxi-
mately 300 myBP based on a nucleotide substitution rate of
1.26%. Although Scutellospora was not included in their
data set, the occurrence of spores with germination shields
in deposits that are 100 million years older than the
estimated divergence of Gigaspora from other Glomero-
mycota supports the hypothesis that the germination shield
is an ancestral feature within the Gigasporaceae. If in fact
Gigaspora is advanced, the mode of germination involving
a germination shield was lost during the evolution of this
genus (Redecker 2002). In addition, the complex system of
spore walls composed of one to several wall groups seen in
Scutellospora was also lost because members of Gigaspora
display a much simpler wall organisation (Walker and
Sanders 1986). The inner wall group in Scutellosporites
devonicus is not preserved, and thus its original thickness is
difficult to estimate. However, we suggest that the inner
wall group was quite massive because one of the spores
(the holotype specimen) clearly shows that the germination
shield does not occur close to the surface of the spore
lumen, but rather appears stalked (Fig. 1a). This suggests
that the shield had to pass through a massive inner wall
group before extending along the inner surface of the dark
layer. The fact that the surface boundary lines of both the
spore lumen and erect portion of the shield (‘stalk’) are not
wrinkled or otherwise unnaturally distorted (cf. Fig. 1a–c)
indicates that the erect portion of the shield does not
represent a preservational artefact. As a result, this feature
substantiates that the inner wall group was of considerable
thickness because the ‘stalk’of the germination shield
could not be explained if the inner wall group were only a
few micrometre thick. In extant representatives of Scutello-
spora the inner wall group is usually only 0.6–2μm thick
(INVAM homepage). However, for a few species, up to
18 μm thick inner wall groups have been recorded, but
these are based on material mounted in PVLG, which
results in expansion of the wall (e.g. from 2 to 15 μm
within a few minutes in S. spinosissima C. Walker and
Cuenca, cf. Walker et al. 1998). The considerable thickness
of the inner wall group of S. devonicus in comparison to
that seen in extant Scutellospora suggests that perhaps the
inner wall group was gradually reduced and eventually lost
in Gigaspora.
Time estimates for the appearance of individual
lineages and taxa within the Glomeromycota are typically
based on molecular and genetic studies of modern taxa.
In many cases the more general results from these
studies are supported by the fossil record (e.g. Simon et
al. 1993; Helgason and Fitter 2005; Taylor and Krings
2005). At a finer scale of resolution, however, the fossil
Mycol Progress
record has to date mostly failed in producing suitable
evidence in support for or against hypotheses based on
molecular data, due primarily to the inherent incomplete-
ness of the fossil record. As a result, Scutellosporites
devonicus from the Rhynie chert is an important discovery
because it displays the first direct marker that can be used
to establish the precise systematic position of an Early
Devonian mycorrhizal fungus. As the molecular phylogeny
of the Glomeromycota is continuously refined, it will be
interesting to see how the characters attributed to S.
devonicus fit character states based on molecular data.
Acknowledgements This study was supported in part by funds from
the Alexander von Humboldt-Foundation (V-3.FLF-DEU/1064359 to
M.K.) and the National Science Foundation (EAR-0542170 to T.N.T.
and M.K.). We thank A. Schüßler and C. Walker for providing
valuable information that contributed to this study and two anony-
mous reviewers for their insightful comments and suggestions.
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