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Host-Jumps Drove Rust Evolution

figure a

Rust fungi. Left: Hamaspora acutissima; Middle: Phragmidium mucronatum; Right: Uromyces scaevolae. Photos by Alistair McTaggart.

Rust fungi are one of the most diverse groups of plant pathogens and their divergence was thought thought to mirror the evolution of their hosts. Recently ancestral rusts were hypothesized to have angiosperm hosts, which altered the longheld view of rust evolution. Estimates on the age of rust fungi range from 150–300 million years ago (Ma), however, this had not been tested with a molecular clock.

In the study by McTaggart et al. (2015), a molecular clock was calibrated to the evolution of rust fungi on species of Acacia (~20 Mya), which have a rich fossil record in Australia. The ancestral Pucciniales were calibrated to the ages of divergence for either angiosperms (up to 194 Ma), or to the hosts of the most ancestral species of rust on gymnosperms in the cupressophytes (up to 256 Mya). Two ribosomal DNA genes (LSU and SSU) and a mitochondrial gene (CO3) were used for phylogenetic reconstruction with Bayesian evolutionary analyses.

Rust fungi were recovered with a much younger age than previously hypothesized, with a mean age between 113–115 Ma (full range between 70–161 Ma), when calibrated to angiosperms or cupressophytes. This new estimate of age provides evidence that host jumps, rather than coevolution, were the main speciation events that drove the evolution of rust fungi. Genera of rust fungi likely arose from host jump events and then diversified by co-speciation or taxonomically small host-shifts. Perhaps there is more plasticity in the host range of rust fungi, and host expansions on novel host populations that have not developed resistance will be common; this has already occurred with taxa such as Cronartium ribicola, Puccinia lagenophorae, and P psidii.

Sensing Host Plant Signals: A New Role for Pheromone-Sensing Machinery?

Just how plant pathogenic and root-infecting fungi are able to respond and grow towards chemical stimuli from plants has remained obscure. Now David Turrà and colleagues from the Universidad de Cordoba in Spain have been able to elucidate this phenomenon in the case of Fusarium oxysporum and the roots of Solanum lycopersicum (Turrà et al. 2015). They studied the germination of microconidia in the presence of a range of compounds, and elegantly demonstrated that the fungus was able to grow towards the roots as a result of a response triggered by class III peroxidases secreted by the plant roots. This involved a mitogen-activated protein kinase (MAPK) and a transmembrane protein Ste2 in the fungal cell well. Intriguingly, the Ste2 protein is a functional homologue of the sex pheromone α-receptor in Saccharomyces cerevisiae.

In addition, the group went on to demonstrate that hyphal growth towards nutrients, including sugars and amino acids, is controlled by a particular MAPK cascade.

While it is unclear how widespread the phenomenon is in root-infecting fungi, the genes involved would appear to be conserved and they interpret plant-sensing in complex environments such as soil as an unexpected alternative role for the fungal pheromone machinery.

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Fusarium oxysporum.

Fifty Key Events in Fungal Systematics

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  • McTaggart AR, Shivas RG, van der Nest MA, Roux J, Wingfield BD, Wingfield MJ (2015) Host jumps shaped the diversity of extant rust fungi (Pucciniales). New Phytologist: DOI 10.1111/nph.13686.

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  • Turrà D, El Ghalid M, Rossi F, Di Pietro A (2015) Fungal pathogen uses sex pheromone receptor for chemotropic sensing of host plant signals. Nature 527: 521–524.

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  • Crous PW, Hawksworth DL, Wingfield MJ (2015) Identifying and naming plant-pathogenic fungi: past, present, and future. Annual Review of Phytopathology 53: 246–267.

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Hawksworth, D.L. Research News. IMA Fungus 6, A56–A57 (2015).

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