Pigments in Rust Fungi: Biosynthesis, Role in Plant-Pathogen Interactions, and Evolution

Abstract

Diseases caused by rust fungi represent critical constraints to global plant production. A characteristic feature of these pathogens is the striking pigments they produce in one or more spore forms, which give them a rusty appearance. These pigments are thought to protect rust fungi against UV radiation and oxidative stress, and possibly act as virulence factors. The cytoplasmic carotenoid pigment composition and relative abundance of 14 rust species were studied, including Puccinia graminis f. sp. tritici (Pgt), P. striiformis f. sp. tritici, P. triticina, P. hordei, P. psidii, P. thaliae, P. oxalidis, Uromyces viciae-fabae, and Phragmidium rubi-idaei, along with colour mutants of several rust species with white, chocolate, pale yellow, dark brown, black, grey, yellow, yellow-orange, dark red and orange urediniospores. Four carotenoids had been found in rust fungi: phytoene, lycopene, -carotene and -carotene. The carotenoid composition did not vary much within rust species but, Among the 14 species investigated, the ratios of -/-carotene varied from 0.14 to 4.49, which might be used as an additional taxonomic character in rust fungi. Candidate genes for carotenoid biosynthesis in Pgt were identified, cloned and functionally complemented using specifically engineered strains of Escherichia coli. The carotenoid biosynthesis pathway in rust fungi was elucidated, with only two genes, CrtYB and CrtI, catalysing the reactions from GGPP to -carotene. Our understanding of carotenoid pigmentation evolution in rust fungi was improved by phylogenetic analysis. Both CrtYB and CrtI are closely related among rust fungi, other pathogenic fungi, and some aphids. A blackish-brown pigment was extracted from the wall of wild-type Pgt urediniospores. The spectrophotometric analysis results suggested that the spore wall pigment extracted from urediniospores of Pgt resembled the DOPA type melanin. Plausible structures of the fragments from this pigment were tentatively proposed.