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 interior valleys that had average annual
temperatures between 17 and 23° C and 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, apparently due to higher temperatures and/or lower precipitation (Vakili,
1981).
NOTES ON CROPS/OTHER PLANTS AFFECTED
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, P. lunatus and P. vulgaris being the
principal hosts.
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, K. striata, Lupinus albus, L. luteus, Melilotus officinalis, Pisum
sativum, Pueraria phaseoloides, Sesbania exaltata, S. sericea, Trifolium incarnatum and T. repens
(Rytter et al., 1984); Calopogonium mucunoides, Crotalaria grantiana, C. juncea, Macroptilium
atropurpureum, M. lathyroides, Vigna mungo and V. aff. wilmanii (Riveiro do Vale et al., 1985); V.
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.
SYMPTOMS - DESCRIPTION
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, are delimited by the vascular bundles. On some hosts, spots are round rather than
angular (Vakili and Bromfeld, 1976). Pustules of urediniospores are formed on both 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 Bromfeld, 1976; Bromfeld 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).
BIOLOGY AND ECOLOGY
For many years the American P. meibomiae was considered to be the same species as the Asian P.
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 and relative
virulence and aggressiveness to soyabeans (Ono et al., 1992). Phakopsora meibomiae is apparently
unadapted to soyabeans and is significantly less virulent and aggressive to that host than is P.
pachyrhizi. 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 23° C and 20-22° C,
respectively, with a range for both processes of between 11 and 30° C (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 Bromfeld, 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
soybean 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, while the Taiwanese isolate, P. pachyrhizi, produced telia
after 21 and 30 days. At low light intensity and 10° C, 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 did the American rust at these low temperatures; only at 15° C under low light did the
American isolate mature sooner. The Taiwanese isolate also produced larger and lighter-coloured lesions
with a higher percentage containing telia; the Puerto Rican isolate caused only 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 Bromfeld, 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, vs 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 (Bromfeld 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 Glycine max.
MOVEMENT AND DISPERSAL
Natural dispersal: Urediniospores are distributed by wind locally and long-distance over land (Stavely
and Pastor-Corrales, 2005). Intercontinental movement of spores of P. 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
United States 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.
Accidental introduction: 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.
ECONOMIC IMPACT
Kuchler et al. (1984) analysed the economic consequences if a virulent race of the soyabean rust fungus
were to become 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 US
economy were forecast to exceed $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 sovabean production in countries such as Brazil and the USA is still
undetermined. Any additional effect of P. meibomiae would likely be minor.
Vakili and Bromfeld (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.
CONTROL
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.
CHEMICAL CONTROL

Asian soybean rust can be controlled with well-timed applications of fungicides (Osathaphant et al., 1980;
          Godoy et al., 2004; Miles et al., 2007b). Because 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.
          Host resistance: Much work is currently being done to select and breed for resistance against P.
          pachyrhizi (Pierozzi et al., 2008; Paul and Hartman, 2009). Phakopsora 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., 2007a).
          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). Because 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 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 NEEDS
          The specific causes of relative lack of virulence, aggressiveness and invasiveness to P. meibomiae could
          be compared with the morphologically similar P. pachyrhizi.
          References

Suggested citation: Chalkley, D..Systematic Mycology and Microbiology Laboratory, ARS, USDA. . Invasive Fungi. American soybean rust -Phakopsora meibomiae. Retrieved December 8, 2021,
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