A Mechanism for Surface Attachment in Spores of a Plant Pathogenic Fungus

Hamer, John E.; Howard, Richard J.; Chumley, Forrest G.; Valent, Barbara

doi:10.1126/science.239.4837.288

Cited by 449 publications

(274 citation statements)

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“…Appressoria form in response to physical and chemical cues from the plant surface that are detected by membrane components, including the product of the PTH11 gene (DeZwaan et al, 1999). Strong attachment of the germ tube to the leaf surface and alterations in cell wall conformation, mediated in part by the MPG1 hydrophobin, contribute to surface perception (Hamer et al, 1988;Talbot et al, 1996), and the outcome is rapid activation of a G-protein-adenylate cyclase-cAMP-dependent signaling pathway. This, in turn, triggers multiple mitogen-activated protein kinase cascades, resulting in differentiation of the appressorium, transport of lipid and carbohydrate reserves to the infection cell, and generation of appressorial turgor (Mitchell and Dean, 1995;Xu and Hamer, 1996;Choi and Dean, 1997;Liu and Dean, 1997;Xu et al, 1997Xu et al, , 1998Adachi and Hamer, 1998;Dixon et al, 1999;Thines et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

PDE1 Encodes a P-Type ATPase Involved in Appressorium-Mediated Plant Infection by the Rice Blast Fungus Magnaporthe grisea

Balhadère

Talbot

2001

Plant Cell

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Plant infection by the rice blast fungus Magnaporthe grisea is brought about by the action of specialized infection cells called appressoria. These infection cells generate enormous turgor pressure, which is translated into an invasive force that allows a narrow penetration hypha to breach the plant cuticle. The Magnaporthe pde1 mutant was identified previously by restriction enzyme-mediated DNA integration mutagenesis and is impaired in its ability to elaborate penetration hyphae. Here we report that the pde1 mutation is the result of an insertion into the promoter of a P-type ATPase-encoding gene. Targeted gene disruption confirmed the role of PDE1 in penetration hypha development and pathogenicity but highlighted potential differences in PDE1 regulation in different Magnaporthe strains. The predicted PDE1 gene product was most similar to members of the aminophospholipid translocase group of P-type ATPases and was shown to be a functional homolog of the yeast ATPase gene ATC8 . Spatial expression studies showed that PDE1 is expressed in germinating conidia and developing appressoria. These findings implicate the action of aminophospholipid translocases in the development of penetration hyphae and the proliferation of the fungus beyond colonization of the first epidermal cell. INTRODUCTIONOne of the principal reasons why pathogenic fungi are so successful at causing plant disease is their ability to penetrate the plant cuticle directly, often using specialized infection cells called appressoria (Mendgen et al., 1996). A wide variety of fungal pathogens form appressoria, and the development of these cells involves a complex morphogenetic program that results in rapid differentiation of a highly specialized structure (Dean, 1997). The rice blast fungus Magnaporthe grisea is an important pathogen of cultivated rice and has emerged as an experimental model for the study of plant infection processes (for reviews, see Howard and Valent, 1996;Hamer and Talbot, 1998). Magnaporthe develops dome-shaped appressoria, which form at the ends of germ tubes soon after spore germination on the leaf surface. Appressoria attach strongly to the leaf and then generate enormous turgor pressure (up to 8 MPa), which is used to rupture the plant cuticle (Howard et al., 1991). The turgor inside appressoria is generated by a rapid increase in intracellular glycerol levels, which is maintained by a specialized cell wall layer containing melanin (Howard and Ferrari, 1989;de Jong et al., 1997). If melanin biosynthesis is blocked, either by chemical intervention or mutation, then Magnaporthe is unable to penetrate the plant surface and cannot cause disease (Chida and Sisler, 1987;Chumley and Valent, 1990).How such enormous cellular turgor is translated into the substantial invasive force necessary to breach the plant cell wall is not clear, but it appears to involve polarization of the cytoskeleton to the point of infection and localized cell wall modification Howard, 1990, 1992;Bechinger et al., 1999). A narrow penetration hypha forms at t...

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Section: Discussionmentioning

confidence: 99%

PDE1 Encodes a P-Type ATPase Involved in Appressorium-Mediated Plant Infection by the Rice Blast Fungus Magnaporthe grisea

Balhadère

Talbot

2001

Plant Cell

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“…lnfection is dependent on the elaboration of an appressorium, a specialized attachment cell that develops in response to specific environmental cues. Appressorium formation is initiated when the tip of the germ tube emerging from a conidium ceases apical extension and swells into a dome-shaped melanized structure, which becomes firmly attached to the plant surface (Hamer et al, 1988). Hydrostatic pressure increases inside this cell and provides the force necessary to drive a penetration hypha through the plant cuticle ' Current address: Department of Plant Pathology, North Carolina State University, Box 6716, Raleigh, NC 276957616, *To whom correspondence should be addressed.…”

Section: Introductionmentioning

confidence: 99%

The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea.

1995

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Magnaporthe grisea, the causal agent of rice blast disease, differentiates a specialized infection cell, an appressorium, that is required for infection of its host. Previously, cAMP was implicated in the endogenous signaling pathway leading to appressorium formation. To obtain direct evidence for the role of cAMP in appressorium formation, the gene encoding the catalytic subunit of the cAMP-dependent protein kinase (cpkA) was cloned, sequenced, and disrupted. Polymerase chain reaction primem designed after highly conserved regions in the same gene from other organisms were used to amplify genomic DNA fragments. The cloned amplification products were used to identify genomic clones. DNA blot analysis indicated that cpkA is present as a single copy in the genome. cpkA consists of 1894 bp, including three short introns sufficient to encode a protein of 539 amino acids with a predicted molecular mass of 60.7 kD. The deduced peptide shares >45% identity with other catalytic subunits and contains all functional motifs and residues with the addition of a glutamine-rich region at the N terminus. Two transformants, L5 and T-182, in which cpkA had been replaced with a hygromycin resistance gene cassette, were unable to produce appressoria, could not be induced to form appressoria by cAMP, and were nonpathogenic on susceptible rice, even when leaves were abraded. These results were confirmed by analysis of 57 progeny from a cross between transformant W and the wild-type laboratory strain 70-6. Other aspects of growth and development, including vegetative growth as well as asexual and sexual competence, were unaffected when measured in vitro. These results provide direct evidence that the cAMP-dependent protein kinase is necessary for infection-related morphogenesis and pathogenesis in a phytopathogenic fungus.

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“…1. Infections occur when fungal spores land and attach themselves to leaves using a special adhesive released from the tip of each spore 4 . The germinating spore develops an appressorium-a specialized infection cell-which generates enormous turgor pressure (up to 8 MPa) that ruptures the leaf cuticle, allowing invasion of the underlying leaf tissue 5,6 .…”

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confidence: 99%

The genome sequence of the rice blast fungus Magnaporthe grisea

Dean

Talbot

Ebbole

et al. 2005

Nature

1,486

1,194

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Magnaporthe grisea is the most destructive pathogen of rice worldwide and the principal model organism for elucidating the molecular basis of fungal disease of plants. Here, we report the draft sequence of the M. grisea genome. Analysis of the gene set provides an insight into the adaptations required by a fungus to cause disease. The genome encodes a large and diverse set of secreted proteins, including those defined by unusual carbohydrate-binding domains. This fungus also possesses an expanded family of G-protein-coupled receptors, several new virulence-associated genes and large suites of enzymes involved in secondary metabolism. Consistent with a role in fungal pathogenesis, the expression of several of these genes is upregulated during the early stages of infection-related development. The M. grisea genome has been subject to invasion and proliferation of active transposable elements, reflecting the clonal nature of this fungus imposed by widespread rice cultivation.Outbreaks of rice blast disease are a serious and recurrent problem in all rice-growing regions of the world, and the disease is extremely difficult to control 1,2 . Rice blast, caused by the fungus Magnaporthe grisea, is therefore a significant economic and humanitarian problem. It is estimated that each year enough rice is destroyed by rice blast disease to feed 60 million people 3 . The life cycle of the rice blast fungus is shown in Fig. 1. Infections occur when fungal spores land and attach themselves to leaves using a special adhesive released from the tip of each spore 4 . The germinating spore develops an appressorium-a specialized infection cell-which generates enormous turgor pressure (up to 8 MPa) that ruptures the leaf cuticle, allowing invasion of the underlying leaf tissue 5,6 . Subsequent colonization of the leaf produces disease lesions from which the fungus sporulates and spreads to new plants. When rice blast infects young rice seedlings, whole plants often die, whereas spread of the disease to the stems, nodes or panicle of older plants results in nearly total loss of the rice grain 2 . Different host-limited forms of M. grisea also infect a broad range of grass species including wheat, barley and millet. Recent reports have shown that the fungus has the capacity to infect plant roots 7 .Here we present our preliminary analysis of the draft genome sequence of M. grisea, which has emerged as a model system for understanding plant-microbe interactions because of both its economic significance and genetic tractability 1,2 . Acquisition of the M. grisea genome sequenceThe genome of a rice pathogenic strain of M. grisea, 70-15, was sequenced through a whole-genome shotgun approach. In all, greater than sevenfold sequence coverage was produced, and a summary of the principal genome sequence data is provided in Table 1 and Supplementary Table S1. The draft genome sequence consists of 2,273 sequence contigs longer than 2 kilobases (kb), ordered and orientated within 159 scaffolds. The total length of all sequence contigs is 38.8 mega...

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A Mechanism for Surface Attachment in Spores of a Plant Pathogenic Fungus

Cited by 449 publications

References 14 publications

PDE1 Encodes a P-Type ATPase Involved in Appressorium-Mediated Plant Infection by the Rice Blast Fungus Magnaporthe grisea

PDE1 Encodes a P-Type ATPase Involved in Appressorium-Mediated Plant Infection by the Rice Blast Fungus Magnaporthe grisea

The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea.

The genome sequence of the rice blast fungus Magnaporthe grisea

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