80
boundary of cells containing one of the intrusive fungi, and hence probably represents a host response effective in separating infected from uninfected tissues.
Moreover, several of the infected rhizomes contain peripheral regions that are
devoid of cells. Krings et al. (2007c) suggest that this tissue degradation may have
been effective as a defense mechanism based on the fact that, in some extant plants,
phytopathogenic microorganisms are deterred by programmed cell death around the
infected areas that inhibit the microbes from spreading (Hammond-Kosack and
Jones 1996; Veronese et al. 2003; Glazebrook 2005; Anderson et al. 2010).
Clusters of globose vesicles attached to branching hyphae characterize
Palaeozoosporites renaultii, another fungus in Asteroxylon mackiei (Strullu-Derrien
et al. 2015). These authors suggest that P. renaultii was a parasite with affinities to
the Chytridiomycota, and report, but do not illustrate, a host response in the form of
secondarily thickened cell walls. We hold the opinion that P. renaultii represents a
cluster of glomoid spores; however, Strullu-Derrien et al. (2015) reject affinities to
the Glomeromycota because “hyphal structures…narrow progressively as they
branch”, which is in fact a common morphology within the Glomeromycota (Walker
et al. 2018).
3.3.1.2 Plant Structural Alterations in Response to Fungal Intrusion
The previous section provided examples of structural defense mechanisms effective
in slowing down or deterring “unwanted” fungal colonization or spreading that
were in place in early land plants by the Devonian. A little later, in the Carboniferous,
vascular plants showed host responses against fungal intrusion in the form of callosities (also called appositions, lignotubers, or papillae, among other terms; see
Stubblefield et al. 1984) that closely resemble defenses employed by plants today
(Akai 1959; Pearce 1996; Schwarze et al. 2000; Schulze-Lefert 2004). One example
of callosity formation occurs in a rachis of the filicalean fern Botryopteris antiqua
(Krings et al. 2011a) from the Mississippian of France (Fig. 3.3d), while another has
been reported in a lycophyte (Lepidodendron sp.), also from the Mississippian of
France (Krings et al. 2009b: pl. II, figs 12–17). The latter specimen even contains
two different types of callosities, namely a narrow form that does not show evidence
of a penetration canal, and a larger form that may be straight or curved and usually
contains a central penetration canal. The presence of two different types of callosities may be evidence that this host recognized two different intruders. Although
putative chytrid zoosporangia occur in the same tissue samples as the callosities,
they have not been found in organic connection, and thus cannot be positively linked
to one another. Other documented evidence of callosity formation in Carboniferous
plants includes lycophyte periderm from the Pennsylvanian of Great Britain
(Krings et al. 2010b: fig. 4J–M) and sphenophyte rootles from the Pennsylvanian of
France (Taylor et al. 2012: pl. I, fig. 1, pl. II, fig. 9, pl. III, figs 1–3). Finally, the
gymnosperm pollen cone Lasiostrobus polysacci from the Carboniferous of North
America contains septate fungal hyphae in the cortex and microsporophylls
(Stubblefield et al. 1984). The host cells are sometimes accompanied by opaque
C. J. Harper and M. Krings
boundary of cells containing one of the intrusive fungi, and hence probably represents a host response effective in separating infected from uninfected tissues.
Moreover, several of the infected rhizomes contain peripheral regions that are
devoid of cells. Krings et al. (2007c) suggest that this tissue degradation may have
been effective as a defense mechanism based on the fact that, in some extant plants,
phytopathogenic microorganisms are deterred by programmed cell death around the
infected areas that inhibit the microbes from spreading (Hammond-Kosack and
Jones 1996; Veronese et al. 2003; Glazebrook 2005; Anderson et al. 2010).
Clusters of globose vesicles attached to branching hyphae characterize
Palaeozoosporites renaultii, another fungus in Asteroxylon mackiei (Strullu-Derrien
et al. 2015). These authors suggest that P. renaultii was a parasite with affinities to
the Chytridiomycota, and report, but do not illustrate, a host response in the form of
secondarily thickened cell walls. We hold the opinion that P. renaultii represents a
cluster of glomoid spores; however, Strullu-Derrien et al. (2015) reject affinities to
the Glomeromycota because “hyphal structures…narrow progressively as they
branch”, which is in fact a common morphology within the Glomeromycota (Walker
et al. 2018).
3.3.1.2 Plant Structural Alterations in Response to Fungal Intrusion
The previous section provided examples of structural defense mechanisms effective
in slowing down or deterring “unwanted” fungal colonization or spreading that
were in place in early land plants by the Devonian. A little later, in the Carboniferous,
vascular plants showed host responses against fungal intrusion in the form of callosities (also called appositions, lignotubers, or papillae, among other terms; see
Stubblefield et al. 1984) that closely resemble defenses employed by plants today
(Akai 1959; Pearce 1996; Schwarze et al. 2000; Schulze-Lefert 2004). One example
of callosity formation occurs in a rachis of the filicalean fern Botryopteris antiqua
(Krings et al. 2011a) from the Mississippian of France (Fig. 3.3d), while another has
been reported in a lycophyte (Lepidodendron sp.), also from the Mississippian of
France (Krings et al. 2009b: pl. II, figs 12–17). The latter specimen even contains
two different types of callosities, namely a narrow form that does not show evidence
of a penetration canal, and a larger form that may be straight or curved and usually
contains a central penetration canal. The presence of two different types of callosities may be evidence that this host recognized two different intruders. Although
putative chytrid zoosporangia occur in the same tissue samples as the callosities,
they have not been found in organic connection, and thus cannot be positively linked
to one another. Other documented evidence of callosity formation in Carboniferous
plants includes lycophyte periderm from the Pennsylvanian of Great Britain
(Krings et al. 2010b: fig. 4J–M) and sphenophyte rootles from the Pennsylvanian of
France (Taylor et al. 2012: pl. I, fig. 1, pl. II, fig. 9, pl. III, figs 1–3). Finally, the
gymnosperm pollen cone Lasiostrobus polysacci from the Carboniferous of North
America contains septate fungal hyphae in the cortex and microsporophylls
(Stubblefield et al. 1984). The host cells are sometimes accompanied by opaque
C. J. Harper and M. Krings