Phakopsora pachyrhizi, the causal agent of Asian soybean rust

Abstract

The plant pathogenic basidiomycete fungi Phakopsora pachyrhizi and Phakopsora meibomiae cause rust disease in soybean plants. Phakopsora pachyrhizi originated in Asia-Australia, whereas the less aggressive P. meibomiae originated in Latin America. In the New World, P. pachyrhizi was first reported in the 1990s to have spread to Hawaii and, since 2001, it has been found in South America. In 2004, the pathogen entered continental USA. This review provides detailed information on the taxonomy and molecular biology of the pathogen, and summarizes strategies to combat the threat of this devastating disease.

Taxonomy: Phakopsora pachyrhizi Syd. & P. Syd; uredial anamorph: Malupa sojae (syn. Uredo sojae); Domain Eukaryota; Kingdom Fungi; Phylum Basidiomycota; Order Uredinales; Class Urediniomycetes; Family Phakopsoraceae; Genus Phakopsora (http://www.indexfungorum.org). The nomenclature of rust spores and spore-producing structures used within this review follows Agrios GN (2005) Plant Pathology, 5th edn. London: Elsevier/Academic Press.

Host range: In the field, P. pachyrhizi infects leaf tissue from a broad range (at least 31 species in 17 genera) of leguminous plants. Infection of an additional 60 species in other genera has been achieved under laboratory conditions.

Disease symptoms: At the beginning of the disease, small, tan-coloured lesions, restricted by leaf veins, can be observed on infected soybean leaves. Lesions enlarge and, 5-8 days after initial infection, rust pustules (uredia, syn. uredinia) become visible. Uredia develop more frequently in lesions on the lower surface of the leaf than on the upper surface. The uredia open with a round ostiole through which uredospores are released.

Figure 1

Scanning electron micrographs showing soybean leaves colonized by P. pachyrhizi. a) Section through a leaf blade with an uredium. Intercellular spaces are heavily colonized by P. pachyrhizi mycelium and dispersed uredospores are present at the lower leaf surface. b) Branched hyphae (h) are formed in the intercellular space of soybean leaves. Haustorial mother cells (hmc) get in close contact with particular mesophyll cells which are subsequently invaded and mature haustoria are formed. (Permission and copyrights of figures are owned by Bayer CropSience AG, Monheim Germany.)

Figure 2

Interaction of P. pachyrhizi with its host soybean and the nonhost plant Arabidopsis. a) Upon infection P. pachyrhizi forms uredia which are located mainly on the lower side of the leaf. Newly formed uredospores are dispersed by wind. b) Spores landing on leaves germinate and form an appressoria as depicted in the interference contrast micrograph. c) Intercellular hyphae form haustorial mother cells (hmc) from which haustoria (hau) develop inside mesophyll cells. d) The life cycle of P. pachyrhizi is completed with the formation of uredospores in uredia. e) In the nonhost interaction between the fungus and Arabidopsis uredospores germinate, form appressoria and penetrate epidermal cells as known from the host type of interaction. Similarly penetrated epidermal cells of host and nonhost plants die, as indicated after trypan‐blue staining. f) Fungal growth is restricted at the mesophyll boundary. Pictures shown in e and f are optical sections from the same infection site focused either on the epidermal or mesophyll layer. g) P. pachyrhizi is unable to complete its life cycle and does not sporulate on wild‐type Arabidopsis plants. sp, uredospore; app, appressorium; epi, epidermal cell; hau, haustorium; hmc, haustorial mother cell; penh, penetration hypha; meso, mesophyll cell. (Fig. 2c reprinted from Koch et al., 1983).

Figure 3

Initial developmental stages during interactions of P. pachyrhizi with host and nonhost plants (schematic). Germinating uredospores (sp) produce a single germ tube (gt) terminated with an appressorium (app). A funnel‐like structure, the appressorial cone (cone), is built inside the appresorium and continues into a penetration hypha (penh) which traverses epidermal cells (epi). Penetrated cells, in consequence, die (punctated). In the intercellular space of the mesophyll a primary hypha (ph) is separated from the penetration hypha by a septum and branches into several secondary hyphae (sh). Finally , a haustorial mother cell (hmc) is formed from which the pathogen invades a mesophyll cell (meso) forming the first haustorium (hau) are established in the host interaction (modified from Koch et al. 1983). Left side: host interaction showing all developmental stages of infection; right side: nonhost interaction with e.g. wild‐type Arabidopsis plants. Fungal invasion is stopped the latest after transversion of the epidermal cell at the border to the mesophyll.

Figure 4

Infection structures of P. pachyrhizi (race Thai 1) on the adaxial leaf surface of soybean (cv. Erin). a) Early stage of appressorium formation with a short germ tube, six hours post inoculation (h p.i.). b) Subsequent invasion of the fungus into the epidemis causes cell collapse and death of penetrated cells as observed at 24 h p.i. Low temperature cryo scanning electron microscopy by Prof. Kurt Mendgen, University of Konstanz, Germany.