Puccinia Pers.

Neues Mag. Bot. 1: 118. 1794.

• For synonyms see Cunningham (1931).
• Classification: Basidiomycota, Pucciniomycotina, Pucciniomycetes, Pucciniales, Pucciniaceae.
• Type species: Puccinia graminis Pers. Designated as type species of Puccinia by Cunningham (1931) on cultivated Triticum; lectotypified by Jørstad (1958).
• DNA barcodes (genus): ITS, LSU.
• DNA barcode (species): ITS (evidence for intraspecific and intra-isolate diversity), LSU.

Spermogonia dark brown to black, often on adaxial leaf surface, subepidermal, concave hymenia with well-developed periphyses at ostiole [Group V, type 4 sensu Hiratsuka & Hiratsuka (1980)]. Spermatia exuded in droplets, small, aseptate, hyaline. Aecia erumpent, usually abaxial, cup-shaped, with well-developed peridium; peridial cells irregular and verrucose. Aeciospores catenulate, globose to subglobose, verruculose. Uredinia subepidermal or erumpent, on both leaf surfaces and stems, without peridium, pale yellow to brown. Paraphyses either absent, peripheral or within the sorus. Urediniospores borne singly on pedicels, mostly echinulate, usually globose, subglobose, ellipsoid to obovoid, germ pores absent or conspicuous. Telia subepidermal or erumpent, mostly dark brown to black, on both leaf surfaces and stems. Teliospores typically 2-celled by transverse or oblique septa (but may have variations of 1–4 cells in some species), borne singly on pedicels, mostly pale to dark brown, cell walls smooth or ornamented. Basidia transversely septate (phragmobasidia), 2–4 celled, external. Basidiospores formed singly from each basidial cell on a sterigma, sometimes ballistosporic.

Distribution:

Worldwide.

Hosts:

Species of Puccinia are obligate plant pathogens that occur on host species in many families, especially Asteraceae, Cyperaceae, Fabaceae, Lamiaceae, Liliaceae s. lat., Malvaceae and Poaceae. Heteroecious species of Puccinia, e.g. Pu. graminis, require two host plant species to complete their lifecycle. The spermogonia and aecia of heteroecious species occur on one host species, while the uredinia and telia occur on another, often unrelated, host species. Autoecious species complete their lifecycle on one host species. There are many variations in the lifecycles of species of Puccinia. For example, some species, e.g. Pu. lagenophorae, do not form spermogonia or uredinia. Other species are known only from their telia, or telia and spermogonia, e.g. Pu. malvacearum and Pu. grevilleae. Frequent host jumps in the evolution of Puccinia and related genera have resulted in closely related species of Puccinia across wide host ranges, as well as phylogenetically unrelated species that occur on the same host plant species (Maier et al. 2007, van der Merwe et al. 2008, Dixon et al. 2010, McTaggart et al. 2016a).

Disease symptoms:

Spermogonia, aecia, uredinia and telia occur on leaves and stems, often associated with chlorotic lesions, sometimes on bullate swellings, solitary or scattered or aggregated in groups, arranged linearly or concentrically or irregularly, often erumpent, in cases of severe infection leaves prematurely wilt and senesce.

Notes:

The starting publication for names of all rust fungi for purposes of priority as provided by Art. 13 of the International Code of Nomenclature for algae, fungi, and plants (ICN) (McNeill et al. 2012) is the Synopsis Methodica Fungorum by Persoon (1801), who listed 11 species of Puccinia, 19 species of Aecidium and 30 species of Uredo. The genera Aecidium, Uredo and Puccinia were established for rust fungi with aecia, uredinia and telia, respectively. Many species described in these three different genera are conspecific, e.g. the lectotype of Aecidium berberidis designated by Clements & Shear (1931) is the aecial stage of Pu. graminis. There is little possibility that Aecidium and Uredo (asexual genera) will displace Puccinia (sexual genus) under Art. 57.2 of the ICN (McNeill et al. 2012). Whether Uredo is a synonym of Puccinia depends on the phylogenetic placement of Uromyces beticola, the lectotype of Uredo (Laundon 1970). A taxonomic working group on the Basidiomycota in 2011 recommended the use of Uredo for uredinial species that could not be assigned to a monophyletic sexual genus (available at: http://www.imafungus.org/Issue/31/05.pdf). Many species of Aecidium and Uredo will need to be transferred to Puccinia, or other monophyletic genera, in order to preserve the one name equals one fungus principle (Hawksworth et al. 2011).

There are about 4 000 described species of Puccinia (Kirk et al. 2008), which have mostly been delimited by host taxon. Many of these species have diversified in the last 50 million years as a result of host jumps (McTaggart et al. 2016b), with the aecial host serving as a pathway for further speciation (van der Merwe et al. 2008). The morphology of teliospores and urediniospores is often sufficient to distinguish species of Puccinia that occur on the same host. Molecular approaches have uncovered cryptic diversity in some species of Puccinia (Liu & Hambleton 2013) as well as linked aecia to telia in the life cycle of heteroecious rusts (Jin et al. 2010). Other studies have shown there is less species biodiversity in some rusts than previously thought, e.g. Pu. lagenophorae and closely related species (Scholler et al. 2011, McTaggart et al. 2014). Intraspecific and intra-isolate diversity of the ITS region was found in Pu. horiana and Pu. kuehnii (Virtudazo et al. 2001, Alaei et al. 2009). Multiple haplotypes and paralogous copies of the ITS region within species of rust must be considered for phylogenetic and molecular barcode studies.

Phylogenetic studies have recovered several sexual genera as potentially congeneric with Puccinia. Puccinia is either paraphyletic or polyphyletic with respect to Ceratocoma (McTaggart et al. 2016b), Cumminsiella (Maier et al. 2003), Dietelia (Wingfield et al. 2004), Diorchidium (Beenken & Wood 2015), Endophyllum (Maier et al. 2003), Macruropyxis (Beenken & Wood 2015), Miyagia (Wingfield et al. 2004), Sphenospora (Aime 2006) and Uromyces (Maier et al. 2003). Three major clades that contained Puccinia and related genera were identified in molecular phylogenetic studies (van der Merwe et al. 2008, Dixon et al. 2010). One clade diversified on Cyperaceae, Juncaceae and orders of plants in the asterids and rosids (The Angiosperm Phylogeny 2016), and the another on Poaceae and Ranunculaceae (van der Merwe et al. 2008). A third clade included species of Puccinia on Poaceae (Dixon et al. 2010). An example of the relationships of the major clades in Puccinia is shown in Fig. 59.

Uromyces requires particular consideration as it has long been thought an aseptate variant of Puccinia (Sydow & Sydow 1904, Savile 1978). Morphology alone does not reliably separate Puccinia and Uromyces, because puccinioid (2-celled) and 1-celled spores and characteristics of the pedicel are homoplasious in the Pucciniales (Maier et al. 2007, Minnis et al. 2012, Beenken & Wood 2015). Several studies have shown that Puccinia and Uromyces are polyphyletic, and furthermore that Puccinia is paraphyletic with respect to the type of Uromyces (U. appendiculatus) and other species of Uromyces on Fabaceae (Maier et al. 2007, van der Merwe et al. 2008). Consequently, either a taxonomy that accepts Puccinia as a paraphyletic group is adopted or Uromyces is synonymised with Puccinia. In the latter case, many important species of Uromyces will require name changes. The traditional use of Uromyces for species with aseptate teliospores has been replaced by a phylogenetic approach; for example, Demers et al. (2017) used a phylogenetic approach to describe two species of Puccinia with aseptate teliospores, which would have been described as Uromyces based on morphology.

The future of Puccinia depends on whether it can be divided into monophyletic genera or sub-genera that reflect synapomorphies or ecological relationships on which a natural classification can be based. A broad concept of Puccinia that accepts species with puccinioid spores that are recovered in closely related clades as defined by van der Merwe et al. (2008) and Dixon et al. (2010) is adopted here. Based on this molecular phylogenetic taxonomic concept, we have transferred four species of Uredo from the Australasian region to Puccinia. Further examples of taxa recovered in Puccinia, include Aecidium kalanchoe (Hernádez et al. 2004) and Uredo guerichiani (Maier et al. 2007). We have chosen not to make new combinations of these species without examination of a specimen. Molecular phylogenetic support must be an essential requirement for the description of new species or new combinations in Puccinia because several species known from an anamorphic stage have an affinity with other genera of rust fungi, e.g. Uredo rolliniae (now Phakopsora rolliniae) (Beenken 2014).

References:

• Sydow & Sydow 1904 (morphology); Cummins & Hiratsuka 2003 (biology, morphology and taxonomy).
• Aime MC (2006). Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience 47: 112–122.
• Alaei H, de Backer M, Nuytinck J, et al. (2009). Phylogenetic relationships of Puccinia horiana and other rust pathogens of Chrysanthemum x morifolium based on rDNA ITS sequence analysis. Mycological Research 113: 668–683.
• Beenken L (2014). Pucciniales on Annona (Annonaceae) with special focus on the genus Phakopsora. Mycological Progress 13: 791–809.
• Beenken L, Wood A (2015). Puccorchidium and Sphenorchidium, two new genera of Pucciniales on Annonaceae related to Puccinia psidii and the genus Dasyspora. Mycological Progress 14: 1–13.
• Clements FE, Shear CL (1931). The genera of fungi. The H.W. Wilson Company, New York, USA.
• Cummins GB, Hiratsuka Y (2003). Illustrated Genera of Rust Fungi. American Phytopathological Society, St. Paul, Minnesota, USA.
• Cunningham GH (1931). The rust fungi of New Zealand: together with the biology, cytology and therapeutics of the Uredinales. John McIndoe, Dunedin, New Zealand.
• Demers JE, Liu M, Hambleton S, et al. (2017). Rust fungi on Panicum. Mycologia: In Press.
• Dixon LJ, Castlebury LA, Aime MC, et al. (2010). Phylogenetic relationships of sugarcane rust fungi. Mycological Progress 9: 459–468.
• Hawksworth DL, Crous PW, Redhead SA, et al. (2011). The Amsterdam Declaration on fungal nomenclature. IMA Fungus 2: 105–112.
• Hernádez JR, Aime MC, Newbry B (2004). Aecidium kalanchoe sp. nov., a new rust on Kalanchoe blossfeldiana (Crassulaceae). Mycological Research 108: 846–848.
• Hiratsuka Y, Hiratsuka N (1980). Morphology of spermogonia and taxonomy of rust fungi. Reports of the Tottori Mycological Institute 18: 257–268.
• Jin Y, Szabo LJ, Carson M (2010). Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology 100: 432–435.
• Jørstad I (1958). The genera Aecidium, Uredo and Puccinia of Persoon. Blumea - Biodiversity, Evolution and Biogeography of Plants 9: 1– 20.
• Laundon GF (1970). The lectotype for Uredo. Taxon 19: 947.
• Liu M, Hambleton S (2013). Laying the foundation for a taxonomic review of Puccinia coronata s.l. in a phylogenetic context. Mycological Progress 12: 63–89.
• Maier W, Begerow D, Weiss M, et al. (2003). Phylogeny of the rust fungi: an approach using nuclear large subunit ribosomal DNA sequences. Canadian Journal of Botany 81: 12–23.
• Maier W, Wingfield BD, Mennicken M, et al. (2007). Polyphyly and two emerging lineages in the rust genera Puccinia and Uromyces. Mycological Research 111: 176–185.
• McNeill J, Barrie FR, Buck WR, et al. (2012). International Code of Nomenclature for algae, fungi and plants (Melbourne Code) adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. Koeltz Scientific Books, Germany.
• McTaggart AR, Geering ADW, Shivas RG (2014). The rusts on Goodeniaceae and Stylidiaceae. Mycological Progress 13: 1017–1025.
• McTaggart AR, Shivas RG, Doungsa-ard C, et al. (2016a). Identification of rust fungi (Pucciniales) on species of Allium in Australia. Australasian Plant Pathology 45: 581–592.
• McTaggart AR, Shivas RG, van der Nest MA, et al. (2016b). Host jumps shaped the diversity of extant rust fungi (Pucciniales). New Phytologist 209: 1149–1158.
• Minnis D, McTaggart AR, Rossman A, et al. (2012). Taxonomy of mayapple rust: the genus Allodus resurrected. Mycologia 104: 942–950.
• Persoon CH (1801). Synopsis Methodica Fungorum. Henricus Dieterich, Göttingen, Germany.
• Savile DBO (1978). Paleoecology and convergent evolution in rust fungi (Uredinales). Biosystems 10: 31–36.
• Scholler M, Lutz M, Wood A, et al. (2011). Taxonomy and phylogeny of Puccinia lagenophorae: a study using rDNA sequence data, morphological and host range features. Mycological Progress 10: 175–187.
• Sydow P, Sydow H (1904). Monographia Uredinearum seu Specierum Omnium ad hunc usque Diem Descriptio et Adumbratio Systematica. Volume 1. Genus Puccinia. Verlag Von J. Cramer, Lipsiae, Germany.
• Van der Merwe MM, Walker J, Ericson L, et al. (2008). Coevolution with higher taxonomic host groups within the Puccinia/Uromyces rust lineage obscured by host jumps. Mycological Research 112: 1387–1408.
• Virtudazo E, Nakamura H, Kakishima M (2001). Ribosomal DNA-ITS sequence polymorphism in the sugarcane rust, Puccinia kuehnii. Mycoscience 42: 447–453.
• Wingfield BD, Ericson L, Szaro T, et al. (2004). Phylogenetic patterns in the Uredinales. Australasian Plant Pathology 33: 327–335.

Table 18. DNA barcodes of accepted Puccinia spp.

¹CDL: US Department of Agriculture, Agricultural Research Service, Cereal Disease Laboratory; BPI: US National Fungus Collections, Beltsville, Maryland, USA; BRIP: Queensland Plant Pathology Herbarium, Brisbane, Australia; HSZ: Cereal Disease Laboratory collection, St. Paul, Minnesota, USA; PBM: P. Brandon Matheny (personal collection); PRC: Charles University in Prague, Prague, Czech Republic; PRM: National Museum, Prague, Czech Republic; PUR: Purdue University, west Lafayette, Indiana, USA. ^T and ^LT indicate ex-type and ex-lectotype, respectively.

²ITS: internal transcribed spacers and intervening 5.8S nrDNA; LSU: partial 28S large subunit RNA gene. *Whole genome sequence. ^#ITS2–LSU sequence.

•  Aime MC (2006). Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience 47: 112–122.
• Alaei H, de Backer M, Nuytinck J, et al. (2009). Phylogenetic relationships of Puccinia horiana and other rust pathogens of Chrysanthemum x morifolium based on rDNA ITS sequence analysis. Mycological Research 113: 668–683.
• Bruckart WL, Eskandari FM, Berner DK, et al. (2012). Comparison of Puccinia acroptili from Eurasia and the USA. Botany 90: 465–471.
• Crouch JA, Szabo LJ (2011). Real-time PCR detection and discrimination of the southern and common corn rust pathogens Puccinia polysora and Puccinia sorghi. Plant Disease 95: 624–632.
• Dixon LJ, Castlebury LA, Aime MC, et al. (2010). Phylogenetic relationships of sugarcane rust fungi. Mycological Progress 9: 459–468.
• Duplessis S, Cuomo CA, Lin Y-C, et al. (2011). Obligate biotrophy features unravelled by the genomic analysis of rust fungi. Proceedings of the National Academy of Sciences (USA) 108: 9166–9171.
• Flores RC, Loyo JR, Ojeda RA, et al. (2009). First report of orange rust of sugarcane caused by Puccinia kuehnii in Mexico, El Salvador, and Panama. Plant Disease 93: 1347.
• Jin Y, Szabo LJ, Carson M (2010). Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology 100: 432–435.
• Kiran K, Rawal HC, Dubey H, et al. (2016). Draft genome of the wheat rust pathogen (Puccinia triticina) unravels genome-wide structural variations during evolution. Genome Biology and Evolution 8: 2702–2721.
• Langrell SRH, Glen M, Alfenas AC (2008). Molecular diagnosis of Puccinia psidii (guava rust) – a quarantine threat to Australian eucalypt and Myrtaceae biodiversity. Plant Pathology 57: 687–701.
• Liu M, Hambleton S (2013). Laying the foundation for a taxonomic review of Puccinia coronata s.l. in a phylogenetic context. Mycological Progress 12: 63–89.
• Marin-Felix Y, Groenewald JZ, Cai, L, et al. (2017). Genera of phytopathogenic fungi: GOPHY 1. Studies in Mycology xxxx.
• McTaggart AR, Geering ADW, Shivas RG (2014). The rusts on Goodeniaceae and Stylidiaceae. Mycological Progress 13: 1017–1025.
• McTaggart AR, Shivas RG, Doungsa-ard C, et al. (2016). Identification of rust fungi (Pucciniales) on species of Allium in Australia. Australasian Plant Pathology 45: 581–592.
• Pedley KF (2009). PCR-based assays for the detection of Puccinia horiana on Chrysanthemums. Plant Disease 93: 1252–1258.