83
3.3.1.5 Epiphyllous Fungi
The cuticle, a waxy coating of all aerial plant parts before secondary growth (Pollard
et al. 2008), is the first line of physical defense and barrier against pathogenic fungi
(Martin 1964; Serrano et al. 2014). However, many fungi have evolved strategies to
breach this barrier, pass into the interior of the plant, and spread out (Kolattukudy
1985; Nicholson and Epstein 1991), while others grow on the plant surface and
locally penetrate the cuticle to extract nutrients from the underlying tissues
(Mendgen and Deising 1993; Tucker and Talbot 2001). Still other fungi reside on
the plant surface without ever entering the host (e.g., Hongsanan et al. 2016). Fungi
that grow on leaves are termed epiphyllous, regardless of whether they are parasites
or just surface residents. Since leaf cuticles often survive fossilization and diagenesis relatively unaltered, they can be freed from the surrounding rock matrix and
cleared through chemical maceration processes and studied in transmitted light
(Kerp 1990; Kerp and Krings 1999). Fossil leaf cuticles provide information on
epidermal anatomy, including cell pattern and stomatal morphology, but may also
contain information on leaf-associated fungi. There are numerous reports of fossil
epiphyllous fungi, mostly microthyriaceous types, for which details of the fungus
and the host are known (e.g., Dilcher 1965; Elsik 1978; Phipps and Rember 2004;
Limaye et al. 2007; Bannister et al. 2016). For the most part, the nutritional modes
of these fungi remain unknown; some authors indicate there are morphological
similarities to modern plant pathogens such as Asterina, Vizella, and Trichothyrina,
thus inferring the nutritional mode as parasitism (Ellis 1977; Phipps 2007; Khan
et al. 2015). Evidence suggestive of a host response to the presence of an epiphyllous fungus in the form of a rim of thickened cuticle has been described in a Jurassic
Sphenobaiera (Ginkgophyta) leaf from China (Fig. 3.3h, i) (Sun et al. 2015: pl. II,
fig. 15). Other examples of cuticle alterations interpreted as a host response include
Metrosideros leunigii (Myrtaceae) leaves from the Eocene-Oligocene of Australia
that appear to have produced cuticle thickenings to divert the growth of the hyphae
of a fungal parasite (Tarran et al. 2016: fig. 8A). Another interesting epiphyllous
fungus, Meliolinites buxi (Meliolaceae), occurs on the cuticles of Oligocene Buxus
leaves from China (Ma et al. 2015: fig. 3A–H). These authors offer the hypothesis
that M. buxi is a parasite based on the thickening and twisting of epidermal cell
walls in the host leaf, along with the parasitic life style of the extant Meliolaceae.
The earliest fossil evidence in plant cuticles of a host response to the presence of
epiphyllous fungi occurs in the form of impressions of rosette-like fungal thalli on
a dispersed plant cuticle of unknown systematic affinity from the Carboniferous of
Germany (Hübers et al. 2011). The host reaction occurs in the form of extensive
cutinizations around the thallus margins. The thalli are interpreted as hyphopodia or
some other epiphyllous structure of a parasitic fungus that facilitated host attachment and penetration.
3 Fungi as Parasites: A Conspectus of the Fossil Record
3.3.1.5 Epiphyllous Fungi
The cuticle, a waxy coating of all aerial plant parts before secondary growth (Pollard
et al. 2008), is the first line of physical defense and barrier against pathogenic fungi
(Martin 1964; Serrano et al. 2014). However, many fungi have evolved strategies to
breach this barrier, pass into the interior of the plant, and spread out (Kolattukudy
1985; Nicholson and Epstein 1991), while others grow on the plant surface and
locally penetrate the cuticle to extract nutrients from the underlying tissues
(Mendgen and Deising 1993; Tucker and Talbot 2001). Still other fungi reside on
the plant surface without ever entering the host (e.g., Hongsanan et al. 2016). Fungi
that grow on leaves are termed epiphyllous, regardless of whether they are parasites
or just surface residents. Since leaf cuticles often survive fossilization and diagenesis relatively unaltered, they can be freed from the surrounding rock matrix and
cleared through chemical maceration processes and studied in transmitted light
(Kerp 1990; Kerp and Krings 1999). Fossil leaf cuticles provide information on
epidermal anatomy, including cell pattern and stomatal morphology, but may also
contain information on leaf-associated fungi. There are numerous reports of fossil
epiphyllous fungi, mostly microthyriaceous types, for which details of the fungus
and the host are known (e.g., Dilcher 1965; Elsik 1978; Phipps and Rember 2004;
Limaye et al. 2007; Bannister et al. 2016). For the most part, the nutritional modes
of these fungi remain unknown; some authors indicate there are morphological
similarities to modern plant pathogens such as Asterina, Vizella, and Trichothyrina,
thus inferring the nutritional mode as parasitism (Ellis 1977; Phipps 2007; Khan
et al. 2015). Evidence suggestive of a host response to the presence of an epiphyllous fungus in the form of a rim of thickened cuticle has been described in a Jurassic
Sphenobaiera (Ginkgophyta) leaf from China (Fig. 3.3h, i) (Sun et al. 2015: pl. II,
fig. 15). Other examples of cuticle alterations interpreted as a host response include
Metrosideros leunigii (Myrtaceae) leaves from the Eocene-Oligocene of Australia
that appear to have produced cuticle thickenings to divert the growth of the hyphae
of a fungal parasite (Tarran et al. 2016: fig. 8A). Another interesting epiphyllous
fungus, Meliolinites buxi (Meliolaceae), occurs on the cuticles of Oligocene Buxus
leaves from China (Ma et al. 2015: fig. 3A–H). These authors offer the hypothesis
that M. buxi is a parasite based on the thickening and twisting of epidermal cell
walls in the host leaf, along with the parasitic life style of the extant Meliolaceae.
The earliest fossil evidence in plant cuticles of a host response to the presence of
epiphyllous fungi occurs in the form of impressions of rosette-like fungal thalli on
a dispersed plant cuticle of unknown systematic affinity from the Carboniferous of
Germany (Hübers et al. 2011). The host reaction occurs in the form of extensive
cutinizations around the thallus margins. The thalli are interpreted as hyphopodia or
some other epiphyllous structure of a parasitic fungus that facilitated host attachment and penetration.
3 Fungi as Parasites: A Conspectus of the Fossil Record