Phakopsora meibomiae (soybean rust)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Habitat List
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Pathway Vectors
- Impact Summary
- Impact: Economic
- Risk and Impact Factors
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Phakopsora meibomiae (Arthur) Arthur 1917
Preferred Common Name
- soybean rust
Other Scientific Names
- Aecidium crotalariae Henn.
- Aecidium crotalariicola Henn. 1899
- Malupa vignae (Bres.) Y. Ono, Buritica & J. F. Hennen 1992
- Phakopsora aeschynomenes (Arthur) Arthur 1917
- Phakopsora crotalariae Arthur 1917
- Phakopsora diehlii Cummins 1974
- Phakopsora psoraleae H.S. Jackson & Holw. 1931
- Phakopsora vignae (Bres.) Arthur 1917
- Physopella aeschynomenes (Arthur) Arthur 1907
- Physopella concors (Arthur) Arthur 1917
- Physopella meibomiae Arthur 1917
- Uredo aeschynomenes Arthur 1905
- Uredo concors Arthur 1915
- Uredo teramni Mayor 1913
- Uredo vignae Bres. 1891
International Common Names
- English: soyabean rust
- Spanish: roya de la soja
- French: rouille du soja
- Chinese: dà do ù xiù jún
- Portuguese: ferrugem da soja
Local Common Names
- Brazil: ferrugem da soja
- Germany: Sojabornenrostpilz
- Japan: daizu-sabibyokin
- PHAKME (Phakopsora meibomiae)
Summary of InvasivenessTop of page
P. 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 soyabean (Glycine max), but is less aggressive on that host than the Asian soyabean rust species, Phakopsora pachyrhizi, which has invaded and spread widely throughout the Americas. Due to the fact that the American species has not caused epidemics on soyabean 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.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Basidiomycota
- Subphylum: Pucciniomycotina
- Class: Pucciniomycetes
- Order: Pucciniales
- Family: Phakopsoraceae
- Genus: Phakopsora
- Species: Phakopsora meibomiae
Notes on Taxonomy and NomenclatureTop of page
Two phakopsoroid fungi were found on legume plants in the Americas at about the same time that Phakopsora pachyrhizi was described on Glycine max (soyabeans) and Pachyrhizus erosus in Asia (Sydow and Sydow, 1915). One on Lablab purpureus was named Uredo concors (Arthur, 1915), and later Physopella concors (Arthur, 1917a). Another on Eriosema sp., Phaseolus spp., Teramnus uncinatus and Vigna spp. was first identified as Uredo vignae, a name based on a uredinial fungus on Vigna marina collected in São Tome, and later named as Phakopsora vignae (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, 1943c). Although Cummins (1943c) 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 P. meibomiae (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 on Aeschynomene spp. and Phakopsora crotalariae 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).
DescriptionTop of page
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) 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 approximately 1 µm 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, one to four (or five) 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.
DistributionTop of page
P. 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; BPI, 2009). P. meibomiae, and not Phakopsora 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 Phakopsora 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 and Heu, 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.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 17 Feb 2021
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Trinidad and Tobago||Present|
|U.S. Virgin Islands||Present|
|United States||Present, Localized|
|-Rio de Janeiro||Present||As Phakopsora crotalariae|
|-Rio Grande do Sul||Present||As Phakopsora crotalariae|
|-Santa Catarina||Present||As Phakopsora crotalariae; Original citation: Gjaerum (1978)|
|-Sao Paulo||Present||As Phakopsora crotalariae; Original citation: Gjaerum (1978)|
Risk of IntroductionTop of page
HabitatTop of page
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 interior valleys that had average annual temperatures between 17 and 230C, and an average annual precipitation of 170 to 260 mm. In these valleys, the perennial Lablab purpureus was heavily infected throughout the year, during both dry and rainy seasons. In a later survey, little or no rust was found on L. purpureus at sea level, and little was found at elevations less than 100 m, which was apparently due to higher temperatures and/or lower precipitation (Vakili, 1981).
Habitat ListTop of page
|Terrestrial||Managed||Cultivated / agricultural land||Present, no further details||Harmful (pest or invasive)|
|Terrestrial||Natural / Semi-natural||Natural grasslands||Present, no further details||Natural|
Hosts/Species AffectedTop of page
In the field, P. meibomiae infects and sporulates on 51 species in 20 genera of the subfamily Papilionoideae of the Fabaceae (Ono et al., 1992), with Aeschynomene americana, Canavalia villosa, Crotalaria anagyroides, Lablab purpureus, Phaseolus coccineus, Phaseolus lunatus and Phaseolus vulgaris being the principal hosts.
Neonotonia wightii is one of several alternate hosts of P. meibomiae in Brazil (Carvalho and Figueiredo, 2000).
In addition to these naturally-infected hosts, the following legume species have been shown to be susceptible to this rust species by artificial inoculations: Alysicarpus vaginalis; Cajanus cajan; Cassia occidentalis; Clitoria ternatea; Coronilla varia; Crotalaria spectabilis; Kummerowia stipulacea; Kummerowia striata; Lupinus albus; Lupinus luteus; Melilotus officinalis; Pisum sativum; Pueraria phaseoloides; Sesbania exaltata; Sesbania sericea; Trifolium incarnatum; Trifolium repens (Rytter et al., 1984); Calopogonium mucunoides; Crotalaria grantiana; Crotalaria juncea; Macroptilium atropurpureum; Macroptilium lathyroides; Vigna mungo; and Vigna aff. wilmanii (Ribeiro do Vale et al., 1985); Vigna unguiculata; and Phaseolus aff. longepedunculatus (Vakili and Bromfield, 1976). Although the level of susceptibility observed was low for some species, other isolates of the fungus or other test conditions might have produced more disease.
See Ono et al. (1992) for additional hosts, based on reports and specimens in collections.
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page
SymptomsTop of page
Infections occur mostly on leaves, often on petioles, and less frequently on stems. On susceptible species/cultivars, infections result in small yellowish-brown or greyish-brown spots or lesions (TAN-type), which, on soyabean [Glycine max], are delimited by the vascular bundles. On some hosts, spots are round rather than angular (Vakili and Bromfield, 1976). Pustules of urediniospores are formed on both the adaxial and abaxial surfaces of lesions, but are more frequent on the abaxial surface. The angular lesions coalesce, turn dark-brown and are covered by buff or pale-brown spore masses as sporulation progresses. When resistant species/cultivars are infected, minute angular reddish-brown spots (RB-type) appear, on which no or only a few uredinial pustules are formed. Sporulation on the RB-type lesions is much less than on the TAN-type lesions (Vakili and Bromfield, 1976; Bromfield et al., 1980; Bonde et al., 2006). Later in the season, lesions may become dark reddish-brown and crust-like; these contain subepidemal telial clusters. The telial stage has been found only occasionally on a few species and not on cultivated soyabeans in the field (Ono et al., 1992).
List of Symptoms/SignsTop of page
|Leaves / abnormal colours|
|Leaves / abnormal leaf fall|
|Leaves / fungal growth|
|Leaves / necrotic areas|
|Leaves / yellowed or dead|
|Stems / mould growth on lesion|
Biology and EcologyTop of page
For many years, the American P. meibomiae was considered to be the same species as the Asian Phakopsora pachyrhizi thus, the biology of the American fungus has not been fully investigated. It is assumed that the biology of the Asian fungus, which threatens soyabean crops worldwide, is basically applicable to the American fungus.
Clear differences between P. meibomiae and P. pachyrhizi exist in their host ranges, relative virulence and aggressiveness to soyabeans [Glycine max] (Ono et al., 1992). P. meibomiae is apparently unadapted to soyabeans and is significantly less virulent and aggressive to that host than P. pachyrhizi is. Nevertheless, the effects of temperature on urediniospore germination and germ tube growth in P. meibomiae on soyabean does not appear to differ from that of the Asian species. Mean optimum temperatures for germination and germ tube growth of one American isolate were 230C and 20-220C, respectively, with a range for both processes of between 11 and 300C (Bonde et al., 2007). At one field test site in Puerto Rico, lesions developed on various hosts in 3-7 days, uredinia after 6-12 days, and sporulation after 7-14 days (Vakili and Bromfield, 1976). Differences in virulence among the three isolates of the American rust on the species and cultivars tested indicated that pathogenic variation exists within P. meibomiae.
Dufresne et al. (1987) compared telial production between Taiwanese and Puerto Rican isolates of soyabean rust under laboratory conditions. The two isolates were cultured on ‘Williams’ soyabeans at two temperatures and three light intensities. The Puerto Rican isolate, P. meibomiae, produced telia after 34 and 35 days at 10 and 15°C, respectively, whereas the Taiwanese isolate, P. pachyrhizi, produced telia after 21 and 30 days, respectively. At low light intensity and 100C, the Taiwanese and Puerto Rican isolates produced telia after 29 and 33 days, respectively; at intermediate light intensity after 26 and 36 days, respectively; and at high light intensity after 22 and 34 days, respectively. Thus the Asian rust generally produced telia sooner than the American rust did at these low temperatures; the American isolate matured sooner only at 150C, under low light. The Taiwanese isolate also produced larger and lighter-coloured lesions with a higher percentage containing telia; the Puerto Rican isolate only caused the RB-type of lesions.
Because both species survive and spread well in the uredinial form, the existence and role of the sexual forms and the identity of a possible alternate host have not been recorded or investigated. Bonde et al. (1988) observed isozyme uniformity among Asian isolates, as well as among those from America representing P. meibomiae, which suggests an absence of sexual recombination. Races of the Asian P. pachyrhizi, on the other hand, have been identified in Taiwan (Yeh, 1983), so new genetic combinations may be generated there. Variation in the American species has not been examined.
Physiology and Phenology
The American soyabean rust has been described as “less virulent” (Vakili and Bromfield, 1976; Ono et al., 1992) and “less aggressive” (Bonde et al., 2006; Rossman, 2009) than the Asian species on soyabean. The former character can be measured in terms of the lesion type on susceptible soyabean cultivars; RB, a somewhat hypersensitive host response to infection, versus TAN, where development appears unchecked for Asian isolates (Bonde et al., 2006). The latter character is measured in rates of development on the infected host, with lesions of the more aggressive fungus increasing in size more rapidly and producing greater numbers of uredinia (Bromfield et al., 1980). Greater numbers of uredinia are presumed to produce more spores, thus enabling the fungus to spread wider and faster on the same or different plants.
The American fungus could also be considered as 'less invasive'. Despite a similar urediniospore morphology (Bonde and Brown, 1980) and a longer period of existence on legumes in South and Central America and Caribbean islands, presumably subject to the same winds and storms that brought P. pachyrhizi to the USA within a few years of its arrival in South America (Schneider et al., 2005), P. meibomiae has not been reported from the USA, either on native legumes or on introduced species such as G. max.
ClimateTop of page
|Af - Tropical rainforest climate||Preferred||> 60mm precipitation per month|
|Cf - Warm temperate climate, wet all year||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
Means of Movement and DispersalTop of page
Urediniospores are distributed by the wind locally and over long-distances, over land (Stavely and Pastor-Corrales, 2005). Intercontinental movement of spores of Phakopsora pachyrhizi is apparently due to major air currents, including hurricanes (Schneider et al., 2005). Krupa et al. (2006) determined that urediniospores of P. pachyrhizi were transported in the troposphere from southern Texas or the Yucutan Peninsula of Mexico before being deposited in raindrops in east Texas and from the Gulf Coast of the USA to locations in the upper Midwest. The highly similar spores of P. meibomiae (Bonde and Brown, 1980) could be transported in a similar manner, although the extent of their survival during transport and deposition might differ.
Hartman and Haudenshield (2009) found that urediniospores of P. pachyrhizi can be carried on clothing from North America to Europe; the same means of transport between continents can be expected for those of P. meibomiae.
Pathway VectorsTop of page
Impact SummaryTop of page
Impact: EconomicTop of page
Kuchler et al. (1984) analysed the economic consequences if a virulent race of the soyabean rust fungus became established in the USA, using an econometric-simulation model under two alternative environmental and grower-response assumptions. Total losses to consumers and other sectors of the USA economy were forecast to exceed US$ 7.2 billion/year, even with a conservative estimate of potential damage, while profits to some soyabean farmers and producers of other feed grains would rise. However, the rust would not become a serious obstacle to soyabean production unless virulent races were introduced to the Americas from Asia. Since that has happened in this century, the full extent of the impact of the Asian rust on soyabean production in countries such as Brazil and the USA is still undetermined. Any additional effect of P. meibomiae is likely to be minor.
Vakili and Bromfield (1976) noted various levels of rust disease on other cultivated legumes in Puerto Rico, but did not discuss their possible impact. Significant sporulation occurs on Phaseolus lunatus (lima bean) (Vakili, 1979). Introduced to new areas with suitable environmental conditions, the American species could apparently produce significant disease on certain crops.
Risk and Impact FactorsTop of page
- Has a broad native range
- Highly mobile locally
- Has high reproductive potential
- Reproduces asexually
- Host damage
- Negatively impacts agriculture
- Negatively impacts livelihoods
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
DiagnosisTop of page
Bonde and Brown (1980) provided SEM pictures of uredinia and urediniospores; however, these are not useful for differentiating between the two Phakopsora species (P. meibomiae and Phakopsora pachyrhizi) on soyabean [Glycine max]. Ono et al. (1992) identified differences between the two species in telial structures, but these are rarely available in the field. A DNA extraction and PCR amplification protocol was able to rapidly distinguish between P. meibomiae and P. pachyrhizi (Harmon et al., 2005).
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 5 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 between 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 soyabean 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.
Detection and InspectionTop of page
Similarities to Other Species/ConditionsTop of page
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 Bromfield, 1976).
The Asian soyabean rust, Phakopsora pachyrhizi, 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 µm 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 USA.
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Successful rust disease management can be achieved by selecting durable resistant/tolerant cultivars with desirable agronomic properties, employing necessary good husbandry, and applying appropriate fungicides at the correct stages of soyabean growth and disease development. No single measure can provide disease management. In every soyabean-growing area, a specific management programme must be developed according to the economic factors, the type of soyabeans to be grown (grain vs. vegetable), the time when soyabeans are to be grown, climatic conditions, soil types, and the number and frequency of prevalent rust races.
Asian soyabean rust can be controlled with well-timed applications of fungicides (Osathaphant et al., 1980; Godoy and Canteri, 2004; Miles et al., 2007a). Due to the fact that morphology and infection-related growth of urediniospores of the two species are so similar (Bonde and Brown, 1980; Bonde et al., 2007), the same chemicals and applications should be effective against P. meibomiae under similar conditions.
Much work is currently being done to select and breed for resistance against Phakopsora pachyrhizi (Pierozzi et al., 2008; Paul and Hartman, 2009). P. meibomiae is less virulent on soy varieties susceptible to both fungi, as well as on those containing genes identified for resistance to the Asian species (Bonde et al., 2006). Some differences were evident between the Puerto Rican and Brazilian isolates of P. meibomiae tested, suggesting effectiveness of the R genes and their availability for breeding resistant varieties if needed. Resistance may need to be found in other crops; genes for resistance to P. pachyrhizi in Phaseolus vulgaris are different from those effective against the common bean rust, Uromyces appendiculatus (Miles et al., 2007b).
Monitoring and Surveillance
Immunofluorescent antisera developed against ungerminated urediniospores of P. pachyrhizii can be used in spore traps to detect airborne spores in the field (Baysal-Gurel et al., 2008). Due to the fact that the same antisera also reacted with P. meibomiae in ELISA and IFSA tests, the American species could be monitored as well, in certain areas, but the use of a more specific agent, such as that developed against germinated spores (Baysal-Gurel et al., 2008), would be necessary where the two species occur together.
Gaps in Knowledge/Research NeedsTop of page
ReferencesTop of page
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