American Soybean Rust -Phakopsora Meibomiae

U.S. Department of Agriculture, Agricultural Research Service Systematic Mycology and Microbiology Laboratory - Invasive Fungi Fact Sheets American soybean rust -Phakopsora meibomiae Phakopsora meibomiae is a rust native to the tropical and subtropical regions of the Americas that has a broad host range among legume species. It infects soybean (Glycine max) but is less aggressive on that host than the Asian soybean rust species, P. pachyrhizi, which has invaded and spread widely throughout the Americas. Because the American species has not caused epidemics on soybean in South America or invaded North America, it can be considered to be much less invasive than the Asian species. Given its broad host range, the possibility exists that strains of P. meibomiae could be a threat to other legumes cultivated in warm parts of the world. Phakopsora meibomiae (Arthur) Arthur 1917 Spermogonia and aecia are unknown. Uredinia on adaxial and abaxial leaf surfaces, mostly on the abaxial surface (hypophyllous), minute, scattered or in groups on discoloured lesions, subepidermal in origin, paraphyses arising from peridioid pseudoparenchyma and hymenium, opening through a central aperture, pulverulent, pale cinnamon-brown. Paraphyses cylindric to clavate, (10-)15-55(-64) µm x 6-12 µm, thin-walled laterally, thickened apically (up to 12 µm). Urediniospores sessile, obovoid to broadly ellipsoid, 16-31 x 12-24 µm. Spore wall ca 1µm thick, minutely and densely echinulate, colourless to pale yellowish-brown. Germ pores four to eight (rarely 10), mostly scattered on, but sometimes on and above, the equatorial zone. Telia hypophyllous, often intermixed with uredinia, pulvinate, crustose, chestnut-brown to chocolate-brown, subepidermal in origin, 1 to 4(-5) spore-layered, chestnut-brown above, paler below. Teliospores angularly subglobose, oblong to ellipsoid, more or less regularly layered in rows or irregularly arranged, 12-26(-28) x 6-12(-14) µm. Wall uniformly 1.5-2 µm thick, slightly to strongly thickened apically (up to 6 µm) in uppermost spores, yellowish-brown to light chestnut-brown. For additional description and illustration, see Bonde and Brown, 1980; Ono et al., 1992. Host range: Various members of the Fabaceae. Geographic distribution: North America (Mexico), Central America, South America, Asia. Notes: Two phakopsoroid fungi were found on legume plants in the Americas at about the same time that Phakopsora pachyrhizi Syd. & P. Syd. was described on Glycine max and Pachyrhizus erosus in Asia (Sydow and Sydow, 1915). One on Lablab purpureus was named Uredo concors Arthur (Arthur, 1915), later Physopella concors (Arthur) Arthur (Arthur, 1917a). Another on Eriosema sp., Phaseolus spp., Teramnus uncinatus and Vigna spp. was first identified as Uredo Vignae Bres., a name based on a uredinial fungus on Vigna marina collected in São Tome, and later named as Phakopsora Vignae (Bres.) Arthur (Arthur, 1917b). Both fungi were known only in the uredinial form and no telial stage had been found when Arthur made nomenclatural changes in 1917. Subsequently, both fungi were considered to be conspecific with P. pachyrhizi (Arthur, 1925; Hiratsuka, 1935). The first reported telia of the fungus referred to as P. vignae were discovered on Canavalia villosa in Guatemala (Cummins, 1943). Although Cummins (1943) noticed morphological differences between P. vignae and P. pachyrhizi and questioned their taxonomic identity, he did not make any taxonomic change. An additional Phakopsora had been found on Desmodium incanum in Puerto Rico and named Phakopsora meibomiae (Arthur) Arthur (Arthur, 1917a, b). Cummins (1978) treated both P. vignae and P. meibomiae as synonyms of P. pachyrhizi, although he stated the need for more detailed study to confirm this conclusion. As a result, rust fungi on cultivated soyabeans observed for the first time in 1976 in Puerto Rico (Vakili and Bromfield, 1976) and in 1979 in Brazil (Deslandes, 1979) were reported under the name of P. pachyrhizi. After extensive morphological studies of a large number of specimens, Ono et al. (1992) concluded that P. meibomiae in the Americas and P. pachyrhizi, at that time only in Asia, Oceania and Africa, are distinct species. Their taxonomic decision was supported by the results of extensive cross inoculations with isolates from various legume species (Bromfield, 1984) and by an isoenzyme study in which only 7% of the alleles were in common between American and Asian Phakopsora isolates from soyabean (Bonde et al., 1988). Further molecular examination (Frederick et al., 2002; Anderson et al., 2008) supports the distinction of these two species. The literature published prior to 1992 remains confusing in that both rusts are called P. pachyrhizi, and one must note the origins of isolates studied in order to determine the identity. Ono et al. (1992) also concluded that Phakopsora diehlii Cummins on Aeschynomene spp. and P. Crotalariae Arthur on Crotalaria spp., both widely distributed in the Americas, are conspecific with P. meibomiae. Inoculation tests have shown several species of Crotalaria to be hosts for isolates of the rust from soyabean (Ono et al., 1992). DISTRIBUTION Phakopsora meibomiae, described initially under a number of different names, is distributed widely in the tropical and subtropical regions of the Americas (Ono et al., 1992) but not in North America north of Mexico (Cummins, 1978; Farr and Rossman, 2009). Phakopsora meibomiae, and not P. pachyrhizi, was found on wild legumes in a recent survey in Mexico and Central America (Hernandez, 2005). Reports of P. meibomiae on Desmodium species in Asia are attributed to P. mangalorica or P. pachyrhizi by Ono et al. (1992). Rust reported on Crotalaria incana and Glycine max in Hawaii could have been the result of invasion by either P. meibomiae or P. pachyrhizi (Killgore et al., 1994). The molecular analysis of the genomes of two Hawaiian isolates using simple sequence repeat markers (Anderson et al., 2008) showed their similarity to other P. pachyrhizi isolates. Risk of Introduction: In any region where soyabean production is of economic importance, care must be taken not to introduce virulent/aggressive races from other soyabean-growing areas. In particular, the reciprocal introduction of strains of the soyabean rusts between Asia and the Americas must be avoided. SIMILARITIES TO OTHER SPECIES/CONDITIONS Bacterial pustules caused by Xanthomonas axonopodis pv. glycines and bacterial blight caused by Pseudomonas savastanoi pv. glycinea generate spots similar to those formed by the soyabean rust fungus on leaves. However, the bacterial spots are at first water-soaked in appearance and later ooze out a bacterial slime instead of the powdery spore masses of the rust. The conical uredinia with an apical pore are another distinctive morphological sign of the Phakopsora species on legumes (Vakili and Bromfeld, 1976) The Asian soybean rust, P. pachyrhizi Syd. & P. Syd, cannot be distinguished morphologically from P. meibomiae in the uredinial form (Bonde and Brown, 1980), but the telial forms differ in that P. pachyrhizi has a greater range of spore layers in the telium, with lighter, coloured spore walls, and the teliospores apically thickened up to 6 um in the uppermost layer (Ono et al., 1992). Four other Phakopsora species on legumes are accepted by Ono et al. (1992). These are distinguished primarily by their anamorphs. The Malupa anamorph of P. meibomiae differs from Milesia and Physopella in the form of the peridium surrounding the urediniospores (Ono et al., 1992). Cerotelium species on legumes have the same anamorphic uredinial forms as do species in Phakopsora (Ono et al., 1992) but Cerotelium teliospores are produced in discrete short chains within erumpent telia rather than in uneven layers in telia that remain subepidermal (Cummins and Hiratsuka, 1983; Ono et al., 1992). Hernandez et al. (2009) provide descriptions, illustrations and other data on other rusts found on legumes in or near the United States. DETECTION AND INSPECTION METHODS The pathogen is detected by inspecting the abaxial surface of the leaves for angular necrotic spots containing uredinial pustules that are powdery and buff or pale brown. DIAGNOSTIC METHOD Bonde and Brown (1980) provided SEM pictures of uredinia and urediniospores, though these are not useful for differentiating between the two Phakopsora species on soyabean. Ono et al. (1992) identified differences between the two species in telial structures, but these are rarely available in the field. Sequences of ITS and LSU regions of rDNA for both P. meibomiae and P. pachyrhizi are available in GenBank for comparison (NCBI, 2009). The immunofluorescence assay developed by Frederick et al. (2002) can be used to identify either species in infected plant tissue within five hours. It was applied in the identification of the Asian rust invading the southern USA (Schneider et al., 2005), Argentina (Ploper et al., 2005) and Uruguay (Stewart et al., 2005). Isozyme analysis can also be used to distinguish the species (Bonde et al., 1988), but is a slower process using purified isolates. Anderson et al. (2008) have developed primer pairs to analyze whole genomes of soybean rust isolates using simple sequence repeat markers; these proved to be specific to P. pachyrhizi in that no significant product was amplified from P. meibomiae genomes. NOTES ON HABITAT Vakili (1979) surveyed regions on the Caribbean island of Puerto Rico for Phakopsora on legumes. The rust now known to be P. meibomiae occurred predominantly in

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