78
(Chisholm et al. 2006). To become effective as a plant parasite, a fungus must access
the plant interior, either by actively penetrating the surface or by finding, recognizing, and entering through wounds or natural openings such as stomata (Hoch and
Staples 1991; Knogge 1996; Mendgen et al. 1996; Szabo and Bushnell 2001).
Alternatively, a fungus on the plant surface may produce substances that kill (parts
of) the host and subsequently feed on the decaying tissue (Berrocal-Lobo et al.
2002; Dean et al. 2012). Fungal parasites today are found on all parts of plants,
including roots, stems, leaves, reproductive structures, and pollen grains (Money
2016). Interestingly, there are also some 400 species of plants that parasitize fungi
and exploit them as their principle source of carbon (Leake 2005; Merckx 2013),
but that’s another story.
3.3.1.1 Early Land Plants
Several (putative) fungal parasitic interactions with early land plants have been
reported from the Lower Devonian Rhynie chert, including chytrid-like fungi interpreted as parasites that are associated with the spores of several early land plants
(Fig. 3.3a) (Kidston and Lang 1921; Harvey et al. 1969; Illman 1984; Taylor et al.
1992a), and Paleopyrenomycites devonicus, a perithecial ascomycete colonizing the
land plant Asteroxylon mackiei (Taylor et al. 1999, 2005a). Although no host
response has been found, Taylor et al. (2005a) submit that P. devonicus colonized
A. mackiei while it was alive based on the fact that the perithecia often occur within
the substomatal chambers of the host plant, with the ostioles directly beneath the
stomata to facilitate spore dissemination (Fig. 3.3b). Moreover, some of the perithecia contain remains of other fungi believed to represent mycoparasites (Taylor et al.
2005a: fig. 41). Another example of fungal parasitism has been described in rhizomes of the land plant Nothia aphylla (Krings et al. 2007b, c), but this time the
fungal intruders elicit host responses in the form of characteristic cell and tissue
alterations. A hypodermal zigzag line composed of secondarily thickened cell walls
characterizes heavily infected rhizomes (Fig. 3.3c). This line marks the outer
Fig. 3.3 (continued) from ray (r), with fungal hyphae (white arrows) penetrating through tylosis
(Jurassic); University of Kansas paleobotanical collection slide TS-GIX-SB-036-01; scale
bar = 20 μm. (g) Fungus extending into, and subsequently forming coralloid branching systems
within, lumen of Psaronius root mantle cell (Permian); pl. IV, fig. 3 in Krings et al. 2017b; scale
bar = 20 μm. (h) Ascoma surrounded by incompletely thickened ring (arrowheads) formed by host
leaf cuticle (Jurassic); pl. II, fig. 15 in Sun et al. 2015; scale bar = 100 μm. (i) Higher magnification
of Fig. 3.2h, focusing on thickened rim; scale bar = 20 μm. (j) Chytrid-like inclusions in pollen
grain of Striatopodocarpites multistriatus (Permian); fig. 2D in Aggarwal et al. 2015; scale
bar = 20 μm. (k) Angiosperm leaf portion with 5 pycnidia (arrows) of Palaeomycus epallelus in
Myanmar amber (Cretaceous); fig. 1 in Poinar 2018; scale bar = 1 cm. (l) Milleromyces rhyniensis
chytrid zoosporangium extending through cell surface (arrowhead) of the charophyte Palaeonitella
cranii (Devonian); color version of fig. 10 in Taylor et al. 1992b; scale bar=10 μm. (m) Two
Palaeonitella cranii cells showing extensive enlargement (hypertrophy host response; h) when
compared with normal cells at base (Devonian); color version of fig. 26 in Taylor et al. 1992b; scale
bar = 100 μm. (n) Longitudinal section of normal cells (n) of Palaeonitella cranii (Devonian);
color version of fig. 1 in Taylor et al. 1992b; scale bar = 100 μm
C. J. Harper and M. Krings
(Chisholm et al. 2006). To become effective as a plant parasite, a fungus must access
the plant interior, either by actively penetrating the surface or by finding, recognizing, and entering through wounds or natural openings such as stomata (Hoch and
Staples 1991; Knogge 1996; Mendgen et al. 1996; Szabo and Bushnell 2001).
Alternatively, a fungus on the plant surface may produce substances that kill (parts
of) the host and subsequently feed on the decaying tissue (Berrocal-Lobo et al.
2002; Dean et al. 2012). Fungal parasites today are found on all parts of plants,
including roots, stems, leaves, reproductive structures, and pollen grains (Money
2016). Interestingly, there are also some 400 species of plants that parasitize fungi
and exploit them as their principle source of carbon (Leake 2005; Merckx 2013),
but that’s another story.
3.3.1.1 Early Land Plants
Several (putative) fungal parasitic interactions with early land plants have been
reported from the Lower Devonian Rhynie chert, including chytrid-like fungi interpreted as parasites that are associated with the spores of several early land plants
(Fig. 3.3a) (Kidston and Lang 1921; Harvey et al. 1969; Illman 1984; Taylor et al.
1992a), and Paleopyrenomycites devonicus, a perithecial ascomycete colonizing the
land plant Asteroxylon mackiei (Taylor et al. 1999, 2005a). Although no host
response has been found, Taylor et al. (2005a) submit that P. devonicus colonized
A. mackiei while it was alive based on the fact that the perithecia often occur within
the substomatal chambers of the host plant, with the ostioles directly beneath the
stomata to facilitate spore dissemination (Fig. 3.3b). Moreover, some of the perithecia contain remains of other fungi believed to represent mycoparasites (Taylor et al.
2005a: fig. 41). Another example of fungal parasitism has been described in rhizomes of the land plant Nothia aphylla (Krings et al. 2007b, c), but this time the
fungal intruders elicit host responses in the form of characteristic cell and tissue
alterations. A hypodermal zigzag line composed of secondarily thickened cell walls
characterizes heavily infected rhizomes (Fig. 3.3c). This line marks the outer
Fig. 3.3 (continued) from ray (r), with fungal hyphae (white arrows) penetrating through tylosis
(Jurassic); University of Kansas paleobotanical collection slide TS-GIX-SB-036-01; scale
bar = 20 μm. (g) Fungus extending into, and subsequently forming coralloid branching systems
within, lumen of Psaronius root mantle cell (Permian); pl. IV, fig. 3 in Krings et al. 2017b; scale
bar = 20 μm. (h) Ascoma surrounded by incompletely thickened ring (arrowheads) formed by host
leaf cuticle (Jurassic); pl. II, fig. 15 in Sun et al. 2015; scale bar = 100 μm. (i) Higher magnification
of Fig. 3.2h, focusing on thickened rim; scale bar = 20 μm. (j) Chytrid-like inclusions in pollen
grain of Striatopodocarpites multistriatus (Permian); fig. 2D in Aggarwal et al. 2015; scale
bar = 20 μm. (k) Angiosperm leaf portion with 5 pycnidia (arrows) of Palaeomycus epallelus in
Myanmar amber (Cretaceous); fig. 1 in Poinar 2018; scale bar = 1 cm. (l) Milleromyces rhyniensis
chytrid zoosporangium extending through cell surface (arrowhead) of the charophyte Palaeonitella
cranii (Devonian); color version of fig. 10 in Taylor et al. 1992b; scale bar=10 μm. (m) Two
Palaeonitella cranii cells showing extensive enlargement (hypertrophy host response; h) when
compared with normal cells at base (Devonian); color version of fig. 26 in Taylor et al. 1992b; scale
bar = 100 μm. (n) Longitudinal section of normal cells (n) of Palaeonitella cranii (Devonian);
color version of fig. 1 in Taylor et al. 1992b; scale bar = 100 μm
C. J. Harper and M. Krings