Phakopsora pachyrhizi
(soyabean rust)

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Identity

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Preferred Scientific Name

• Phakopsora pachyrhizi Syd. & P. Syd.

Preferred Common Name

• soyabean rust

Other Scientific Names

• Malupa sojae (Henn.) Ono et al.
• Phakopsora calothea Syd.
• Phakopsora erythrinae Gäum.
• Phakopsora sojae Fujik.
• Phakopsora sojae Sawada
• Phakopsora vignae (Bres.) Arthur
• Physopella pachyrizi (Syd. & P. Syd.) Azbukina
• Uredo erythrinae Henn.
• Uredo sojae Henn.
• Uromyces sojae (Henn.) Syd. & P. Syd.

International Common Names

• English: rust of soyabean; rust of soybean; rust: soyabean; rust: soybean; soyabean rust fungus; soybean rust; soybean rust fungus
• Spanish: roya de la soja; roya de la soya
• French: rouille; rouille du soja
• Chinese: dà do ù xiù jún
• Portuguese: ferrugem da soja

Local Common Names

• Brazil: ferrugem da soja
• Germany: Rost: Sojabohne; Sojabornenrostpilz
• Japan: daizu-sabibyokin

EPPO code

• PHAKPA (Phakopsora pachyrhizi)

Taxonomic Tree

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• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Basidiomycota
•             Subphylum: Pucciniomycotina
•                 Class: Pucciniomycetes
•                     Order: Pucciniales
•                         Family: Phakopsoraceae
•                             Genus: Phakopsora
•                                 Species: Phakopsora pachyrhizi

Notes on Taxonomy and Nomenclature

Top of page Fungi that cause rust disease of soyabeans and other legumes have long been confused taxonomically largely due to a lack of appropriate comparative studies of their morphological variations and host specificity (Ono et al., 1992). Uredo sojae Henn. was the first to be reported as the soyabean rust fungus in Japan (Hennings, 1903). Subsequently, U. sojae was connected to the telial Phakopsora state on soyabean plants in Taiwan (Sawada, 1931). The fungus was named Phakopsora sojae Sawada (but without a formal description). Meanwhile, another Phakopsora was found on Pachyrhizus erosus in Taiwan and was described and named as Phakopsora pachyrhizi Syd. & P. Syd. (Sydow and Sydow, 1914). Later, Hiratsuka (1932) compared both species and concluded both to be taxonomically identical, with P. pachyrhizi having the nomenclatural priority.

Prior to the correct anamorph-teleomorph connection being discovered, U. sojae was erroneously connected to Uromyces sojae Syd. & P. Syd. (Sydow et al., 1906). Thereafter, the soyabean rust fungus had been reported as Uromyces sojae from various locations in Asia. However, the fungus so described and named was later found to be Uromyces mucunae Rabenh. and the correct host was Mucuna (Butler and Bisby, 1931).

Meanwhile, in the Americas, a new rust fungus was found to occur on Lablab purpureus and another on Eriosema sp., Phaseolus spp., Teramnus uncinatus and species of Vigna. The former was first named as Uredo concors Arthur (Arthur, 1915) and later as Physopella concors (Arthur) Arthur (Arthur, 1917a). The latter fungus was first identified as Uredo vignae Bres. and later as Phakopsora vignae (Bres.) Arthur (Arthur, 1917b). Both fungi are, however, uredinial and no telial state was found when Arthur made nomenclatural changes. Subsequently, by morphological comparisons, Arthur (1925) and Hiratsuka (1935b) concluded both fungi to be conspecific with P. pachyrhizi.

The Phakopsora (telial) state of the fungus that was referred to as P. vignae was found for the first time on Canavalia villosa in Guatemala (Cummins, 1943a). Cummins (1943a) noticed morphological differences between P. vignae and P. pachyrhizi and questioned their taxonomic identity. Further, an additional Phakopsora rust was found on Desmodium incanum in Puerto Rico and named Phakopsora meibomiae (Arthur) Arthur (Arthur, 1917a, b). Cummins (1978) treated P. vignae as a synonym of P. meibomiae which was in turn treated as a synonym of P. pachyrhizi although he stated the need for more detailed study to confirm this conclusion. In the Americas, the rust fungus on cultivated soyabeans was reported for the first time in 1976 in Puerto Rico (Vakili and Bromfield, 1976) and in 1979 in Brazil (Deslandes, 1979) under the name of P. pachyrhizi.

Comparative morphology made possible by the increased number of telial collections of the Phakopsora state both in Asia and the Americas has shown consistent differences between the Asian population (P. pachyrhizi) and the American population (P. meibomiae) of the soyabean rust fungi (Ono et al., 1992). It has also been shown by cross inoculations of isolates on different hosts to various legume species that the American population is less virulent to cultivated soyabeans than is the Asian population (Bromfield, 1984) and that both populations have different host ranges in the field although both have the potential to infect a large number of legume species as common hosts under experimental/greenhouse conditions. Accordingly, Ono et al. (1992) concluded that P. pachyrhizi and P. meibomiae are taxonomically distinct.

Description

Top of page Pycnia and aecia are unknown. Uredinia are amphigenous, mostly hypophyllous, minute, scattered or in groups on discoloured lesions, subepidermal in origin, surrounded by paraphyses arising from peridioid pseudoparenchyma, also with hymenial paraphyses, opening through a central aperture, pulverulent, and yellowish-brown or pale cinnamon-brown. Paraphyses are cylindric to clavate, 25-50 µm long and 6-14 µm wide, slightly to conspicuously thickened (up to 18µm) apically, pale yellowish-brown to colourless. The urediniospores are almost sessile, obovoid to broadly ellipsoid, and 18-34 x 15-24 µm. The spore wall is uniformly ca 1 µm thick, minutely and densely echinulate, and colourless to pale yellowish-brown. Four to eight (mostly six, rarely two or ten) germ pores are equatorial or scattered on the equatorial zone, or occasionally scattered on and above the equatorial zone of the spore wall. Telia are hypophyllus, often intermixed with uredinia, pulvinate and crustose, chestnut-brown to chocolate-brown, subepidermal in origin, and 2- to 7-spore layered. The teliospores are one-celled, irregularly arranged, angularly subglobose, oblong to ellipsoid, and (10-)15-26 x 6-12 µm. The wall is uniformly ca 1 µm thick, sometimes slightly thickened (up to 3 µm) apically in the uppermost spores, colourless to pale yellowish-brown (Ono et al., 1992).

Distribution

Top of page P. pachyrhizi is widespread in Asia and Oceania (but not in New Zealand). In the neotropics, another soyabean rust fungus, Phakopsora meibomiae, occurs, which was once treated as synonymous with P. pachyrhizi but has now been taxonomically segregated (Ono et al., 1992).

African specimens of a Phakopsora species on legumes were retained in P. pachyrhizi. However, the taxonomic decision has been based on morphological comparisons with a limited number of specimens and, therefore, must be confirmed by morphological comparisons with additional specimens and by host-specificity/pathogenicity studies.

The occurrence of P. pachyrhizi in Sri Lanka requires confirmation. Phakopsora mangalorica occurs on Desmodium heterocarpon and Pteroloma triquetrum in Sri Lanka (Petch, 1917; Ono et al., 1992). This species has been reported, as Physopella meibomiae, also on Teramnus labialis from India by Patil and Thirumalachar (1972) who considered that Physopella meibomiae and P. mangalorica were conspecific.

A fungus reported on Desmodium sp. and Uraria lagopoides in Papua New Guinea under the name of P. meibomiae is P. mangalorica (Ono et al., 1992).

P. pachyrhizi has been reported on G. max together with P. meibomiae on Crotalaria incana in Hawaii, USA (Killgore and Heu, 1994). However, the taxonomic identity of the two fungi in Hawaii needs further detailed investigation.

P. pachyrhizi was found in Africa in the late 1990s and spread to South America in 2001. It was detected for the first time in North America in Louisiana in November 2004 and, soon after, in other southeastern states of the USA (Hernández, 2005). It was found on the alternate host kudzu (Pueraria montana var. lobata) in Florida in March 2005 (SPDN, 2005). Many earlier reports of P. pachyrhizi in the Americas are erroneous. Reports prior to 1992 refer instead to the similar looking P. meibomiae (Hernández, 2005).

The occurrence of soyabean rust in a trap crop in south-eastern Zimbabwe in January 2001 was reported by C. Levy, Commercial Farmers' Union, Harare, in a ProMED-mail posting on 7 March 2001 (http://www.promedmail.org). ProMED-mail in 2001 also includes observations of Phakopsora sp. in South Africa. These reports require further confirmation.

Distribution Table

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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.

Risk of Introduction

Top of page In any country and region where soyabean production is of great economic importance, great care must be taken not to introduce races from other soyabean-growing areas. In particular, the reciprocal introduction of the soyabean rusts between Asia and the Americas must be avoided.

Hosts/Species Affected

Top of page P. pachyrhizi has been known to infect and sporulate, in the field, on 35 species in 18 genera of the subfamily Papilionoideae in the Fabaceae. Glycine max, G. soja, Pachyrhizus erosus, Pueraria lobata and Vigna unguiculata are the principal hosts. Among the naturally infected hosts, only Crotalaria anagyroides, G. max, P. erosus, Phaseolus lunatus and V. unguiculata serve as hosts of another soyabean rust fungus, Phakopsora meibomiae, which occurs exclusively within the Americas.

P. pachyrhizi has been proven, by artificial inoculations under greenhouse conditions, to infect and sporulate on the following plant species:

Alysicarpus glumaceus, Delonix regina, Glycines canescens, G. falcata, G. tabacina, Lotus purshianus, Lupinus hirsutus, Macrotyloma axillare, Medicago arborea, Melilotus officinalis, Melilotus speciosa, Mucuna cochinchinensis, Neonotonia wightii, Phaseolus vulgaris, Rhynchosia minima, Trigonella foenum-graecum, Vicia dasycarpa, Sesbania exaltata and S. vesicaria (Bromfield, 1984); Alysicarpus vaginalis, Cassia occidentalis, Clitoria ternatea, Coronilla varia, Crotolaria spectabilis, Kummerowia stipulacea, K. striata, Lupinus albus, L. luteus, Macroptilium lathyroides, Pisum sativum, Sesbania sericea, Trifolium incarnatum and T. repens (Rytter et al., 1984); Cajanus cajan, Lablab purpureus, Macroptilium atropurpureum, Psophocarpus tetragonolobus, Vicia faba, Vigna luteola, V. mungo and V. radiata (Poolpol and Pupipat, 1985); Calopogonium mucunoides, Centrosema pubescens and Crotalaria anagyroides (Cueva et al., 1994); Canavalia gladiata (Poonpolgul and Surin, 1980); Canavalia maritima (Kurata, 1960); Crotalaria aff. dissaromoensis, C. linifolia, Desmodium rhytidophyllum, D. varians, Dolichos axillaris, Lespedeza juncea, Lotus major, L. angustifolius, Psoralea tenax and Rhynchosia sp. (Keogh, 1974); Desmodium triflorum (McLean, 1981); Glycine argyrea, G. curvata, G. cyrtoloba, G. latifolia and G. microphylla (Hartman et al., 1992); Glycine latrobeana (Burdon and Marshall, 1981b); and Lespedeza bicolor and Vigna angularis (Sato and Sato, 1982).

Host Plants and Other Plants Affected

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Growth Stages

Top of page Flowering stage, Fruiting stage, Vegetative growing stage

Symptoms

Top 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 are delimited by vascular bundles. Several pustules of urediniospores are formed on both adaxial and abaxial surfaces of the lesion, but more frequently on the abaxial surface. The lesions coalesce, become dark brown and are covered by buff or pale-brown spore masses as sporulation progresses. Later in the season, the lesions become dark reddish-brown and crust-like; these are subepidemal telial clusters. When resistant species/cultivars are infected, minute, reddish-brown spots (RB-type) appear, on which only a few uredinial pustules are formed. Sporulation on RB-type lesions is much less than on TAN-type lesions.

List of Symptoms/Signs

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Biology and Ecology

Top of page P. pachyrhizi is believed to have a heteroecious life cycle. However, pycnial and aecial stages have not been found. In warm regions, volunteer crops, supplementary legume crops and wild species may harbour the fungus throughout the year or during seasons in which soyabeans are not cultivated, and may serve as the primary infection source. In colder regions where above-ground parts of annual hosts die during winter, no source of new infections in the soyabean-growing season has been identified.

A temperature regime at which the maximum rate of urediniospore germination takes place seems to be 15-25°C. At optimum temperatures, urediniospores germinate in 1-1.5 hours. Optimum temperatures for urediniospore germination were reported to be 15-24°C with a minimum of 10 and a maximum of 28.5°C for Indian, Australian, Indonesian and Taiwanese isolates studied, although the optimum temperatures for the Indian isolate was narrower than other isolates (Marchetti et al., 1976). Wang and Hartman (1992) obtained a similar result where the optimum temperatures for urediniospore germination were 15-25°C. Singh and Thapliyal (1977) reported that, in an Indian isolate, the minimum, optimum and maximum temperatures for urediniospore germination on a glass slide were 20, 25 and 30°C, respectively.

Urediniospore infection of soyabean leaves requires at least 6 hours of dew period at optimum temperatures. Extended dew periods are needed for successful infection by urediniospores at temperatures higher or lower than the optimum. Using urediniospores of Indian, Australian, Indonesian and Taiwanese isolates, Marchetti et al. (1974) reported that the maximum infection of Wayne soyabean leaves occurred at 20-25°C with 10-12 hour dew periods and at 15-17.5°C with 16-18 hour dew periods. Kochman (1979) reported that optimum temperatures for rust development from the urediniospore infection were 17-27°C. According to Wang and Hartman (1992), the minimum dew period for infection was 6 hours at 20-25°C and 8-10 hours at 15-17.5°C. A minimum night temperature below 15°C greatly reduced lesion number or completely prevented lesion development.

Melching et al. (1989) reported that inoculations of susceptible soyabean cultivars with urediniospores at dew periods of less than 6 hours resulted in no infection. In a 6 hour dew period, trace levels of infection occurred at 18-26.5°C. Degrees of infection and intensities of lesion development increased with prolonged dew periods; in an 8 hour dew period at 18-26.5°C, lesion intensities were 10-fold higher than those at 6 hours at the corresponding temperatures. However, increasing dew duration above 13 hours resulted in no significant increase in rust intensity at18-26.5°C. No lesions developed at 9 and 28.5°C, even with dew periods as long as 20 hours.

Germinability and infectivity of urediniospores are reduced by exposure of the spores to dry and high temperature conditions prior to germination. Singh and Thapliyal (1977) reported that, in an Indian isolate, prior exposure of urediniospores to 35°C for 6 hours prevented germination. Similarly, Kochman (1979) reported that germination of urediniospores on water agar at 21°C was significantly reduced by prior exposure of the spores to 28.5-42.5°C for 8 hours. According to Melching et al. (1989), urediniospores on unwetted soyabean leaves progressively lost infectivity during sunny conditions, but exhibited enhanced infectivity after 1 or 2 days on dry foliage under cloudy conditions. After 8 days on dry foliage, no urediniospores were found to cause lesions following a 12 hour dew period at 18°C. Spores on leaves exposed to 4 or 6 hours of dew followed by drying for up to 4 days were able to infect when a 12 hour dew period was provided, but were less infectious than spores that had not been exposed to a brief initial wetting.

The formation of teliospores seems to be induced when infected plants are subjected to a temperature range below 20°C for at least 15 days. Yeh et al. (1981a) reported that, on 20 soyabean cultivars and nine other legume plants, teliospores were successfully induced when the inoculated plants were subjected to 12 hour photoperiods, under 60-100% RH and at temperatures of 15-24°C. In the field, teliospores were produced only when the average daily temperature was below 20°C and the maximum temperature above 29°C. Yeh et al. (1981b) further reported that telia and teliospores were formed on eight legume species when the infected hosts were inoculated and grown under a 12 hour photoperiod (2060 lux), 60-100% RH, at a maximum day temperature of 24±1°C and a minimum night temperature of 15±1°C. Yeh et al. (1982) found that, by artificial inoculations of two cultivars, TK 5 and PI 230971, more telia were formed on TK 5 than on PI 230971. Sources of inoculum from either cultivar did not influence the production of telia. There was a positive correlation between inoculum concentration and telia production. Telia were formed on leaves after 2 weeks at 10°C and 15°C and 3 weeks at 20°C but not at 25°C. In the field, telia production was common when the daily temperatures remained below 20°C for less than 15 hours and average temperatures did not exceed 25°C for at least 15 days. Poolpol and Pupipat (1985) reported that telia and teliospores were successfully induced only on soyabean cultivar SJ. 2 after soyabeans and 23 other leguminous plants were inoculated and kept in an incubator with a 12 hour photoperiod at 6000 lux, 20-22°C day/17°C night cycle at 100% RH for 60 days.

Dufresne et al. (1987) reported telial production in Taiwanese and Puerto Rican isolates. The two isolates were cultured on Williams soyabeans at two temperature and three light intensities. The Taiwanese isolate produced telia after 21 and 30 days and the Puerto Rican isolate produced telia after 34 and 35 days at 10 and 15°C, respectively. At low light intensity (3.9 µE/m²/sec), the Taiwanese and Puerto Rican isolates produced telia after 29 and 33 days, respectively; at intermediate light intensity (5.3 µE/m²/sec) after 26 and 36 days, respectively; and at high light intensity (6.1 µE/m²/sec) after 22 and 34 days, respectively. The Taiwanese isolate produced larger lesions with a higher percentage of telia than the Puerto Rican isolate.

Saksirirat and Hoppe (1991) reported germination of teliospores. After treatment with 10-12 cycles of 24 hour wetting and 24 hour drying periods at room temperature, 65-70% of teliospores germinated at 20°C under artificial illumination of 5000 lux at 12 hour light/dark intervals. Only 25% of teliospores germinated when the telia were treated with seven wetting and drying cycles. Higher germination rates were observed when telia were stored at 5°C for 5-6 months.

Plant Trade

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Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Growing medium accompanying plants
Roots
Seedlings/Micropropagated plants
True seeds (inc. grain)
Wood

Impact

Top of page Estimated yield losses due to the rust infection were 15-40% in southern Japan and up to 70-80% in individual fields and 20-30% in the total crop in Taiwan (Bromfield, 1976). In field trials in Taiwan, yield losses were 18-57% (Chen, 1989).

In a plot trial in Thailand, yield losses were 100% in the most susceptible cultivars and 0-38% in the most tolerant cultivars (Sangawongse, 1973). In Thailand, seed-yield losses in the wet season were 100% for the most susceptible cultivars, while the losses were reduced to 10-15% in the dry season (Sangawpmgse et al., 1977).

In a field trial in Korea, yield losses were 68.7% in a susceptible cultivar and 22.3% in a tolerant cultivar (Shin and Tschanz, 1986).

In a field trial conducted in Austria, seed-yield losses were 60-70% in the most severely infected plots without chemical control (Ogle et al., 1979).

Kuchler et al. (1984) analysed the potential 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 USA economy are 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.

Diagnosis

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The disease is diagnosed both macroscopically by the characteristic symptoms described in Detection and Inspection Methods and microscopically by abundantly paraphysate uredinia with pale yellowish-brown or almost colourless, echinulate urediniospores. However, Harmon et al. (2005) were unable to distinguish between Phakospora pachyrhizi and P. meibomiae on soybean using light microscopy, relying instead on rapid DNA extraction and PCR amplification protocol for diagnosis of the two species. Gevens et al. (2008) diagnosed the pathogen using a real-time PCR protocol.

ELISA protocol has also been used to identify P. pachyrhizi (Koenning et al., 2007). Mendes et al. (2009) developed an electrochemical immunosensor for the early diagnosis of P. pachyrhizi in soybean leaf extract.

An analysis of the various diagnostic protocols for P. pachyrhizi is given by Jurick et al. (2007).

Detection and Inspection

Top of page The disease is detected by inspecting the abaxial surface of the leaves for uredinial pustules that are powdery and buff or pale brown.

Similarities to Other Species/Conditions

Top of page Bacterial pustules caused by Xanthomonas axonopodis pv. glycines and bacterial blight caused by Pseudomonas savastanoi pv. glycinea produce spots similar to those formed by the soyabean rust fungus on discoloured leaf lesions. However, the bacterial spots are at first water-soaked in appearance and later ooze out slimy bacterial masses instead of powdery spore masses as in the rust.

Prevention and Control

Top of page Introduction

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 successful disease management. In each of the soyabean-growing areas, a specific management programme must be developed according to the economic factors, the type of soyabeans to be grown (grain vs. vegetable), time when soyabeans are to be grown, climatic conditions, soil types, and the number and frequency of prevalent rust races.

Chemical Control

No single class of fungicides has emerged as uniquely effective in suppressing the rust fungus (Bromfield, 1984). The application of formulations of the zinc ion-maneb complex periodically throughout the growing season gives favourable control (Bromfield, 1984). The application of Piperazin W524, oxycarboxin, mancozeb and maneb spray was effective in reducing seed-yield losses of soyabeans in Thailand (Sangawongse et al., 1977).

References

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Delaney MA, Sikora EJ, Delaney DP, Palm ME, Roscoe J, Haudenshield JS, Hartman GL, 2011. First report of soybean rust caused by Phakopsora pachyrhizi on Pachyrhizus erosus in the United States. Plant Disease, 95(8):1034. http://apsjournals.apsnet.org/loi/pdis

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