​​The Rust​ Fungi

Hamaspora
Hamaspora (Taiwan), photographer M. Catherine Aime.

Rust fungi (Pucciniales, formerly Uredinales) belong to subphylum Pucciniomycotina, which is considered the basal-most lineage in Basidiomycota (Aime et al. 2014; Padamsee et al. 2012). Other subphyla of Basidiomycota include mushroom-forming fungi (Agaricomycotina) and the smut fungi and their allies (Ustilaginomycotina). All rust fungi are parasites of plants and they are found in all areas where plants grow, including high altitudes and deserts (Arthur 1934; Savile 1971; Smith et al. 2004). In monocultural ecosystems rust fungi may cause considerable damage to their hosts and are therefore important pathogens in agricultural, horticultural and industrial forest habitats. The hosts of rust fungi range from ferns and conifers to dicotyledonous and monocotyledonous plants. Despite the generally wide host range, as a result of a long co-evolution with plants most rust fungi are specific to their host at the species level (Duplessis et al. 2011; Savile 1971). Rust fungi have by far the most complex life cycles within the fungal kingdom and probably among eukaryotes. The general rust fungus life cycle requires five different spore stages and alternation between two taxonomically unrelated host plants for completion. Moreover, at ca. 8000 described species, they also represent the largest natural group of phytopathogens. Pucciniales are obligate parasites, meaning that they need a living host plant for development. 

Rust fungi can cause severe diseases in our​ most important crops. Some examples are: the rusts of wheat, corn and other cereals; forage and range grasses and sugar cane; beans, soybeans, peanuts, and other legumes; various fruits and vegetables; coffee, and forest and plantation timber and pulp trees. Rust fungi probably attack more different kinds of wild and domesticated plants than any other natural fungus order. Rust species are usually highly host specific, i.e. attacking only one or a few closely related plant species, and may have up to six different and dissimilar spore forms and two unrelated hosts while completing its life cycle.

urediniospores of Phakopsora digitariae
A scanning electron microscopy image of urediniospores of Phakopsora digitariae (Physopella digitariae) (Taiwan, 1913) (PUR004235/F15131)​, Photo by Holger Bauch, 1996.

The taxonomy of rust fungi has been based primarily on morphology of certain spore stages (Petersen 1974; Ramsbottom 1912; Sato and Sato 1985). The majority of the taxonomic studies on American rust fungi have been conducted at Purdue University. The present classification system divides rusts into 14 families, with some genera of uncertain affinity (Cummins and Hiratsuka 2003; Minnis et al. 2012). The application of molecular methods to refine taxonomy has not been as widely applied in rust fungal systematics as it has for other groups of Fungi. Primarily this is due to the fact that the rust fungi, as obligate pathogens, cannot be maintained in pure culture and are thus much more difficult to extract and amplify. However,  the last decade has seen the publication of several phylogenetic studies that are advancing our knowledge of rust fungi evolution (Aime 2006; Maier et al. 2003; Wingfield et al. 2004).

What these studies are showing is that the evolution of rust fungi has been largely driven by host associations, although the heteroecism in rust fungi adds an extra layer of complexity to discerning co-evolutionary patterns, and that much revision remains to be done at the family, genus, and species levels (Aime 2006). To date there exist molecular data for only 7–10% of described rust fungal species, as determined from publically available sequence databases such as that of the National Center for Biotechnology Information.​​



References

Puccinia
Puccinia (Louisiana), photographer M. Catherine Aime.
  • Aime MC. 2006. Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience 47: 112–122. http://link.springer.com/article/10.1007%2Fs10267-006-0281-0
  • Aime MC, Toome M, McLaughlin D. 2014. The Pucciniomycotina. In: The Mycota VII. Systematics and Evolution. 2nd Ed. McLaughlin D (Ed), Springer-Verlag. In press.
  • Arthur JC. 1934. Manual of the rusts in United States and Canada. Purdue Research Foundation, Lafayette. 438 pp.
  • Cummins GB, Hiratsuka Y. 2003. The Illustrated Genera of Rust Fungi. APS Press, St. Paul, Minnesota. 225 pp.
  • Duplessis S, Cuomo CA, Lin Y-C, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL, Chiu R, Coutinho PM, Feau N, Field M, Frey P, Gelhaye E, Goldberg J, Grabherr MG, Kodira CD, Kohler A, Kües U, Lindquist EA, Lucas SM, Mago R, Mauceli E, Morin E, Murat C, Pangilinan JL, Park R, Pearson M, Quesneville H, Rouhier N, Sakthikumar S, Salamov AA, Schmutz J, Selles B, Shapiro H, Tanguay P, Tuskan A, Henrissat B, Vande Peer Y, Rouzé P, Ellis JG, Dodds PN, Schein JE, Zhong S, Hamelin RC, Grigoriev IV, Szabo LJ, Martin F. 2011. Obligate biotrophy features unraveled by the genomic analysis of rust fungi.Proceedings of the National Academy of Sciences 108: 9166–1971.
  • Maier W, Begerow D, Weiss M, Oberwinkler F. 2003. Phylogeny of the rust fungi: an approach using nuclear large subunit ribosomal DNA sequences. Canadian Journal of Botany 81: 12–23. http://www.ruhr-uni-bochum.de/imperia/md/content/geobot/2003/maier_2003-phylogeny-of-the-rust-fungi.pdf
  • Minnis AM, McTaggart A, Rossman A, Aime MC. 2012. Taxonomy of mayapple rust: the genus Allodus resurrected. Mycologia 104: ​942–950.​
    http://www.mycologia.org/content/104/4/942.full.pdf​
  • Padamsee M, Kumar TKA, Riley R, Binder M, Boyd A, Calvo AM, Furukawa K,  Hesse C, Hohmann S, James TY, LaButti K, Lapidus A, Lindquist E, Lucas S, Miller K, Shantappa S, Grigoriev IV, Hibbett DS, McLaughlin DJ, Spatafora JW, Aime MC. 2012. The genome of the     xerotolerant mold Wallemia sebi reveals adaptations to osmotic stress and suggests cryptic
    sexual reproduction. Fungal Genetics and Biology 49: 217–226.
    http://www.sciencedirect.com/science/article/pii/S1087184512000242
  • Petersen R. 1974. The rust fungus life cycle. The Botanical Review 40: 453–513.
  • Ramsbottom J. 1912. Some notes on the history of the classification of the Uredinales. Transactions of the British Mycological Society 4: 77–105.
  • Sato T, Sato S. 1985. Morphology of aecia of the rust fungi. Transactions of the British Mycological Society 85: 223–238.
         http://www.sciencedirect.com/science/article/pii/S0007153685801856
  • Savile DBO. 1971. Coevolution of the Rust Fungi and Their Hosts. The Quarterly Review of Biology 46: 211–218.
         http://www.jstor.org/stable/2822510
  • Smith JA, Blanchette RA, Newcombe G. 2004. Molecular and morphological characterization of the willow rust fungus, Melampsora epitea, from arctic and temperate hosts in North America. Mycologia 96: 1330–1338. http://www.jstor.org/stable/3762149
  • Wingfield GD, Ericson L, Szaro T, Burdon JJ. 2004. Phylogenetic patterns in the Uredinales. Australasian Plant Pathology 33: 327–335.
         http://nature.berkeley.edu/brunslab/papers/wingfield2004.pdf​
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