Host specificity in the fungal plant parasite Anthracoidea sempervirentis (Anthracoideaceae, Ustilaginales) reveals three new species and indicates a potential split in the host plant Carex sempervirens

Abstract

The smut fungal genus Anthracoidea contains more than 100 species that parasitize hosts predominantly in the sedge genus Carex. Anthracoidea species are mainly found in the boreal zones of the Northern Hemisphere and many species have an arctic-alpine distribution. Recent re-organization of the taxonomy of the main host genus Carex questions current understanding of host associations in Anthracoidea. Host specificity for many of the species in this genus is considered to be quite broad and a host spectrum of over 10 host species is common. One aim of the study is to understand the potential influence that host taxonomy has on the evolutionary patterns of Anthracoidea. Additionally, by including more specimens, we clarify host specificity and species delimitation in Anthracoidea sempervirentis, a prevalent species occurring on different host species in different Carex subgroups using molecular data. Host colonization patterns within Anthracoidea are complex, and different subclades of Carex have been colonized several times independently, whereas clades of related Anthracoidea species often occur on Carex species from the same host clade. Parasites previously thought to be Anthracoidea sempervirentis occurring on the different Carex host are shown to be at least four distinct species that are restricted to individual host species. Three new species, Anthracoidea ferrugineae on Carex ferruginea from the Alps and the Carpathians, A. firmae on Carex firma from the Alps, and A. kitaibelianae on Carex kitaibeliana from mountains in the Balkan Peninsula, are described and illustrated. An emended description of Anthracoidea sempervirentis is also provided. Anthracoidea sempervirentis in its emended circumscription consists of two clades that correspond to respective clades within Carex sempervirens. The study shows that host colonization in Anthracoidea is more complex than current host taxonomy suggests. Further, including several specimens per host species results in a much higher diversity within Anthracoidea than previously assumed. Citation: Kemler M, Denchev TT, Feige A, Denchev CM, Begerow D (2024). Host specificity in the fungal plant parasite Anthracoidea sempervirentis (Anthracoideaceae, Ustilaginales) reveals three new species and indicates a potential split in the host plant Carex sempervirens. Fungal Systematics and Evolution 13: 91-110. doi: 10.3114/fuse.2024.13.04.

Keywords: Anthracoidea Anthracoideaceae Carex Cyperaceae; new taxa phylogeny; smut fungi.

Fig. 1

Geographic distribution of the species in Anthracoidea sempervirentis group within European alpine systems (generated with SimpleMappr, Shorthouse 2010): red circles – A. ferrugineae, yellow squares – A. firmae, blue asterisks – A. kitaibelianae, and lilac triangles – A. sempervirentis. Scale bar = 100 km.

Fig. 2

Cladogram of species of Anthracoidea. The different colours show host associations according to Roalson et al. (2021) (more similar colours indicate a closer taxonomic relationship of the hosts).

Fig. 3

Phylogram of the species in Anthracoidea sempervirentis group on the respective Carex species. Different parasite species are indicated by the different colour blocks.

Fig. 4

Tanglegram of Anthracoidea sempervirentis and Carex sempervirens. The two separate clades within Anthracoidea sempervirentis correlate well with two separate clades of Carex sempervirens. Colours (light blue & dark blue) indicate the respective groups and their association.

Fig. 5

Anthracoidea ferrugineae. A. Close-up of sori (SOMF 31429). B, C. Spores in LM (SOMF 29700 – holotype; in median and surface view, respectively). D–H. Spores in SEM (D, G. SOMF 29700 – holotype; E, F, H. SOMF 31430). I. Geographic distribution (generated with SimpleMappr, Shorthouse 2010): red circles – specimens with specified localities, black circles – distribution in Switzerland at cantonal level (after Zogg 1986). Scale bars: B, C = 10 μm; D–H = 5 μm; I = 100 km.

Fig. 6

Anthracoidea firmae. A. Habit (SOMF 30141). B. Close-up of a sorus (SOMF 30141). C, D. Spores in LM (SOMF 31435 – in median and surface view, respectively). E–H. Spores in SEM (E, F. SOMF 30141; G, H. SOMF 31435). I. Geographic distribution (generated with SimpleMappr, Shorthouse 2010): red circles – specimens with specified localities, black circles – distribution in Switzerland at cantonal level (after Zogg 1986). Scale bars: C, D = 10 μm; E–H = 5 μm; I = 100 km.

Fig. 7

Anthracoidea kitaibelianae. A. Close-up of sori (SOMF 30182). B, C. Spores in LM (SOMF 30149 – in median and surface view, respectively). D–H. Spores in SEM (D. SOMF 30144; E–H. SOMF 30150). I. Geographic distribution (generated with SimpleMappr, Shorthouse 2010). Scale bars: B, C = 10 μm; D–H = 5 μm; I = 100 km.

Fig. 8

Anthracoidea sempervirentis. A–E. Spores in LM: A, B. SOMF 31419 (in median and surface view, respectively); C–E. SOMF 31436 (white arrows in C, D and E show internal swellings, black arrow in C indicates a light refractive area). F–J. Spores in SEM (F, H, I. SOMF 31426; G, J. SOMF 31420). I. Geographic distribution (generated with SimpleMappr, Shorthouse 2010). Scale bars: A–E = 10 μm; F–J = 5 μm; K = 100 km.