The Top 10 fungal pathogens in molecular plant pathology

Abstract

The aim of this review was to survey all fungal pathologists with an association with the journal Molecular Plant Pathology and ask them to nominate which fungal pathogens they would place in a 'Top 10' based on scientific/economic importance. The survey generated 495 votes from the international community, and resulted in the generation of a Top 10 fungal plant pathogen list for Molecular Plant Pathology. The Top 10 list includes, in rank order, (1) Magnaporthe oryzae; (2) Botrytis cinerea; (3) Puccinia spp.; (4) Fusarium graminearum; (5) Fusarium oxysporum; (6) Blumeria graminis; (7) Mycosphaerella graminicola; (8) Colletotrichum spp.; (9) Ustilago maydis; (10) Melampsora lini, with honourable mentions for fungi just missing out on the Top 10, including Phakopsora pachyrhizi and Rhizoctonia solani. This article presents a short resumé of each fungus in the Top 10 list and its importance, with the intent of initiating discussion and debate amongst the plant mycology community, as well as laying down a bench-mark. It will be interesting to see in future years how perceptions change and what fungi will comprise any future Top 10.

Figure 1

Disease resulting from the infection of rice and wheat with Magnaporthe oryzae. (A) Classical symptoms of panicle blast on rice, although the fungus can cause disease on all foliar tissues. (B) Head blast on wheat. The symptoms on wheat are typically restricted to the head and can be mistaken for wheat scab caused by Fusarium graminearum.

Figure 2

Infection cycle of the rice blast fungus. Conidia produced from lesions are splashed onto new plants where they attach firmly and germinate within a few hours. Subsequently, the germ tube ceases polar growth, the tip swells and, by 12 h, forms a highly melanized dome‐shaped structure, the appressorium. Typically within 24 h, turgor pressure increases within the appressorium, forcing a penetration peg into the underlying tissues. Eye‐shaped necrotic lesions do not appear until several days after infection, from which, under appropriate conditions, conidiophores emerge bearing conidia to re‐initiate the infection cycle. (Scanning electron microscope image in bottom right courtesy of Nicholas Talbot and Michael Kershaw, University of Exeter, UK). [Correction added on 5 July 2012, after online publication: The bottom right image has been amended and acknowledgement has been included in the legend].

Figure 3

Sexual fruiting bodies (apothecia) of the teleomorph Botryotinia fuckeliana (de Bary) Whetzel.

Figure 4

Botrytis cinerea on raspberry fruits (from Williamson et al., 2007).

Figure 5

Stem rust‐infected wheat showing uredinial and telial spore stages.

Figure 6

Wheat flag leaf infected with stripe rust caused by Puccinia striiformis f. sp. tritici.

Figure 7

The floral tissues of hexaploid wheat severely infected with Fusarium graminearum. This disease is frequently referred to as Fusarium head blight (FHB), Fusarium ear blight (FEB) or head scab.

Figure 8

A simplified three‐phase model of the Fusarium graminearum (Fg) infection process through wheat rachis tissue. At the advancing hyphal front, deoxynivalenol (DON) mycotoxin inhibits protein translation, which greatly suppresses the burst of plant defence responses (depicted in blue). Once hyphae enter the plant cells, the presence of the released proteins and sugars and the high density of fungal hyphae lead to a strong activation of plant defence responses. Later, within the lesion centre (>10 days), the cellular contents of fungal cells residing deep within the dead cortical tissue are relocated to the hyphae just below the rachis epidermis and asexual sporulation then occurs.

Figure 9

(A) Fusarium oxysporum microconidium (C) germinating on the surface of a tomato root. Penetration occurs by directed growth of the infectious hypha (IH) towards a natural opening between epidermal root cells (penetration site indicated by an arrow). (B) Fusarium oxysporum hypha growing in a xylem vessel of a tomato root (from Di Pietro et al., 2001).

Figure 10

Barley leaves infected with Blumeria graminis f. sp hordei. The typical powdery ‘pustules’ produced by the mildew colonies which grow on the outer surface of the host plant consist of hundreds of thousands of highly infectious asexual conidia blown by air currents to propagate the disease. The epiphytic colonies are fed by intracellular haustoria which develop inside the epidermal cells (see Fig. 11).

Figure 11

Blumeria graminis f. sp. hordei haustorium. This haustorium was isolated by manually dissecting the epidermis of an infected barley leaf and digesting away the host cell wall with a protoplasting cocktail; it was stained with a lectin (wheatgerm agglutinin) bound to Alexa‐288. The multidigitate structure is surrounded by the perihaustorial membrane of host origin. In common with other mildews, this specialized membrane is continuous with the host plasma membrane, but has very different biochemical properties (Micali et al., 2011). In mildews, the perihaustorial membrane is thought to be the gateway for nutrients and effectors. Bar, 10 µm.

Figure 12

Septoria tritici blotch (STB) disease of wheat caused by Mycosphaerella graminicola.

Figure 13

A model for wheat leaf infection by Mycosphaerella graminicola. Early symptomless colonization (<7 days post‐leaf inoculation, DPI) involves the release of plant defence‐suppressing apoplastic effectors (red and blue triangles) from slow‐growing intercellular hyphae. After 7 days, leaf cell death and the loss of membrane permeability occur, allowing nutrient release into the apoplast. Defence‐suppressing effectors are ‘switched off’, although other potentially toxic effectors (blue diamonds) may be produced. Extensive hyphal growth and asexual sporulation (pycnidia and pycnidiospore formation) are now supported within leaf lesions.

Figure 14

Transmission electron micrograph showing hemiotrophic growth of Colletotrichum destructivum during cowpea infection. Note the thick biotrophic infection vesicle (IV) following appressorium penetration. The host cell is still alive and its plasma membrane can be seen surrounding the hypha. Subsequently, thinner necrophic penetrating hyphae (PH) degrade tissue whilst growing inside the cell. A, appressorium; C, conidium. Photograph courtesy of Dr Richard O'Connell (Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne. With permission).

Figure 15

Developmental stages of Ustilago maydis, tools and disease symptoms. (A) Haploid cells display budding growth. (B) Compatible haploid U. maydis strains expressing cytoplasmic red fluorescent protein (RFP) (red) and green fluorescent protein (GFP) (green) under a constitutive promoter mate and produce a filamentous dikaryon (yellow). (C) A solopathogenic strain expressing cytoplasmic RFP from a constitutive promoter and an appressorial marker gene fused to triple GFP efficiently forms appressoria on a hydrophobic surface, after stimulation with hydroxy‐fatty acids. (D) Macroscopic U. maydis disease symptoms on a maize leaf 12 days post‐infection (left) and fungal hyphae in tumour tissue 10 days post‐infection (right) are visualized by confocal microscopy; fungal hyphae are stained with WGA‐AF488 (green); plant cell walls are stained with propidium iodide (red). (E) Affymetix gene chips allow genome‐wide expression studies. (F) Visualization of F‐actin through LifeAct‐YFP in budding cells. (G) Highly efficient homologous recombination is used for gene replacement employing hygromycin resistance (HygR), nourseothricine resistance (NatR), carboxin resistance (CbxR) or phleomycin resistance (PhleoR) as dominant selectable markers. (H) Phylogenetic tree of U. maydis and its closest relatives. Figures were kindly provided by Patrick Berndt and Rolf Rösser (U. maydis disease symptoms in infected maize cob, centre), both at the Max Planck Institute for Terrestrial Microbiology. Also, please note that their permission for using these Figures has been obtained.

Figure 16

Life cycle of flax rust, Melampsora lini. Genetic analysis in flax rust depends on the ability to replicate all stages of the life cycle under controlled conditions to produce selfed and outcrossed progeny from flax rust isolates, and is complicated by the rust being an obligate biotroph, requiring all manipulations to be undertaken on the living host plant.