Coevolution with higher taxonomic host groups within the Puccinia/Uromyces rust lineage obscured by host jumps

Abstract

Partial ß-tubulin 1 sequence data were obtained for 80 taxa of Pucciniaceae, with hosts from 33 angiosperm families, covering all major ordinal groups in the Angiosperm Phylogeny Group classification. As in previous studies, most species of Puccinia and Uromyces fell into two main clades (I and II), with P. glechomatis and P. psidii excluded from Pucciniaceae. Results suggest two processes; a coevolution of and hosts in each clade, as well as associated frequent jumps to ecologically close, but taxonomically distant, hosts. Clade I contained all rusts on Cyperaceae and Juncaceae, and most rusts on host orders from rosids to euasterids II. Clade II contained all rusts on Poaceae, and most on host orders from monocots to core eudicots. In both main clades, several well-supported subclades were identified. The grouping in clade I, subclade E of rusts of Cyperaceae and Asteraceae and, in particular, of an Australian isolate of P. dioicae with rusts on Australian families of Asterales, suggested a local radiation, and supported the coevolutionary relationship between rusts on these two families seen with a different range of asteraceous rusts in the Northern Hemisphere. In clade I, two clades contained only rusts of Asteraceae and Fabaceae, respectively, and in clade II, subclade F contained only rusts of pooid hosts. Rusts on non-pooid hosts were separated from them in subclade G. Other subclades contained a range of rusts on distantly related angiosperm families. Urediniospore morphology was often, but not always, correlated with the molecular phylogeny. Most rusts with urediniospores having few (1–5) equatorial germ pores were in clade I, whereas most with spores having several (5–14) scattered pores were in clade II. The distribution of telial host families on the ß-tubulin rust phylogeny was not random. Aecial hosts of heteroecious rusts played an important role in the evolutionary process. Possible examples of host jumps were seen in rusts on Geraniaceae, Polygonaceae, and Apiaceae. Despite such jumps obscuring past host associations, possible ancestral hosts were identified by the pattern of host distribution at higher taxonomic levels along the ß-tubulin phylogeny. Results suggest that clade I diverged with Cyperaceae, Juncaceae, and the more advanced core eudicot orders (rosids and asterids), whereas clade II diversified with earlier angiosperm groups, such as monocots, Poaceae, and Ranunculales. Qualified support was given to the hypothesis that rusts can reveal taxonomic relationships between their hosts, at genus, family, and ordinal levels.