Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes

Abstract

Grass-associated fungi (grass symbionts) in the family Clavicipitaceae (Ascomycota, Hypocreales) are species whose host range is restricted to the plant family Poaceae and rarely Cyperaceae. The best-characterized species include Claviceps purpurea (ergot of rye) and Neotyphodium coenophialum (endophyte of tall fescue). They have been the focus of considerable research due to their importance in agricultural and grassland ecosystems and the diversity of their bioactive secondary metabolites. Here we show through multigene phylogenetic analyses and ancestral character state reconstruction that the grass symbionts in Clavicipitaceae are a derived group that originated from an animal pathogen through a dynamic process of interkingdom host jumping. The closest relatives of the grass symbionts include the genera Hypocrella, a pathogen of scale insects and white flies, and Metarhizium, a generalist arthropod pathogen. These data do not support the monophyly of Clavicipitaceae, but place it as part of a larger clade that includes Hypocreaceae, a family that contains mainly parasites of other fungi. A minimum of 5-8 independent and unidirectional interkingdom host jumps has occurred among clavicipitaceous fungi, including 3-5 to fungi, 1-2 to animals, and 1 to plants. These findings provide a new evolutionary context for studying the biology of the grass symbionts, their role in plant ecology, and the evolution of host affiliation in fungal symbioses.

Introgression and gene family contraction drive the evolution of lifestyle and host shifts of hypocrealean fungi

“…Using the divergence time for Ascomycota at 600 million years ago (Mya) (Lücking et al 2009) for calibration, the divergence time for Hypocreales was estimated to be 217 Mya by BEAST (Figure S1). The resulting phylogeny had high boot-strap support for all families and was mostly consistent with results of a previous multilocus phylogeny (Spatafora et al 2007). Verticillium spp.…”

“…Fusarium, Trichoderma , etc.). However, due to the limited availability of genomes, only one species in each family of Stachybotryaceae and Bionectriaceae was included in the present analysis, which is less than that of the previous phylogenetic study using multilocus sequencing of ribosomal and protein coding genes (Spatafora et al 2007). Although insufficient genomic data limited the depth of analysis of some evolution mechanisms such as the host jumping in these fungi (Sung et al 2007), this study highlights evolutionary processes involved in nutrient-based lifestyles and a comprehensive understanding of the phylogenetic relationships of different lineages.…”

“…Species within hypocreales have evolved various lifestyles including saprophytism, endophytism and parasitism on plants, insects, nematodes and other fungi (Berbee 2001). The evolution of plant and animal pathogens and the origin of the grass endophytes from insect pathogens in Clavicipitaceae were documented by multigene phylogenetic analysis (Spatafora et al 2007; Sung et al 2008). Generally, different families display distinct host associations.…”

Cordyceps industry in China

“…It phylogenetically affiliates with Bionectriaceae, Hypocreales, and its relationship with cordyceps fungi is not clear. Multigene and phylogenomic analysis indicated that the fungi in Hypocreales originated from insect association and subsequently evolved to plants and fungi associations (Nikoh and Fukatsu 2000; Spatafora et al 2007). C. rosea as fungicolous fungus might be diverged from ancient insect-associated fungi and still remained the medicinal function similar to C. sinensis and to Chinese cordyceps.…”

“…C. rosea and C. sinensis are not cordyceps fungi but affiliated with Hypocreales, and their medicinal function may imply that all of the fungi in Hypocreales possess the potential for medicinal tonic activities. The fungi in Hypocreales were considered to be originated from insect association and subsequently jumped to hosts of plants and fungi (Nikoh and Fukatsu 2000; Spatafora et al 2007). The medicinal function of fungi associated with plants and fungi in Hypocreales might be remained and their medicinal and tonic functions should be extensively studied in future.…”