Molecular Plant Pathology

Matthew Dickinson, James Beynon, Matthew Dickinson, James Beynon

• Éditeur: CRC Press
• Année: 2020
• ISBN:
  9781000725056
• Édition: 1
• Sujet: Biological Sciences
• Sous-sujet: Botany

For the past century, it has been known that plants possess genetically inherited resistance mechanisms to combat phytopathogenic fungi, bacteria and viruses, and that the relationship between pathogens and host plants is highly specialized and complex. As techniques of molecular biology have developed over the past 25 years, our understanding of the molecular basis of these relationships has advanced significantly.
Molecular Plant Pathology, the fourth volume in the Annual Plant Reviews series, discusses the ways by which molecular plant pathology can be exploited to control disease and thereby maximize crop yield. It covers the three main areas of plant pathology: how pathogens cause disease; (the molecular signaling that takes place between plant and pathogen); how plants resist disease (what is known about resistance genes, apoptosis, and systemic-acquired resistance); and how molecular plant pathology can be exploited to control disease.
Since disease control is directly related to increased crop production, the topics covered in this book are of major economic significance. This economic importance coupled with the clear, concise coverage of the materials, render Molecular Plant Pathology an extremely useful reference for academic and industrial researchers in plant pathology and other related areas of study.Features

1 Fungal pathogenicity—establishing infection

Pascale V. Balhadère and Nicholas J. Talbot

1.1 Introduction

The first obstacle encountered by any plant pathogen is the outer surface of a plant, whether in the form of a tough leaf cuticle, a fibrous stem, or the root surface submerged within soil. In each case, pathogenic fungi have evolved mechanisms to breach these surfaces, by using natural openings, such as stornata, or direct rupture of the surface layers. This chapter describes the early events in plant infection and the specific morphogenetic pathways that have evolved in fungi for this purpose. It concentrates mainly on the developmental biology of the rice blast fungus, Magnaporthe grisea, an appressorium-forming cereal pathogen. In recent years, rapid progress has occurred in identifying genes from this fungus that are involved in the plant infection process and in determining their function. A view of the specific signal transduction pathways and gene expression patterns required for plant colonisation is, therefore, emerging and can act as a framework for understanding the biology of fungal pathogens. Based on this information, experiments can be designed to determine the conservation of pathogenic processes among diverse species. This chapter follows the chronology of plant infection by M. grisea and describes the key genetic components so far identified and their known, or predicted, functions. Comparisons to other fungal pathogens are made throughout the text.

1.2 The rice blast fungus, Magnaporthe grisea

The ascomycete, Magnaporthe grisea (Hebert) Barr (anamorph Pyricularia oryzae Saca), causes one of the major diseases of cultivated rice, called rice blast disease (Ou, 1985). The biology of M. grisea shares many features with the life cycles of other major fungal pathogens, including, most significantly:

• The differentiation of infection-specialised cells called appressoria (Figure 1.1) (Mendgen et al., 1996; Howard, 1997).
• The synthesis and mobilisation of materials, such as mucilage, hydrophobic, melanin, storage carbohydrates and glycerol, during this process (Money, 1995; Yoder and Turgeon, 1996; Kershaw and Talbot, 1998).
• The mechanics of cuticle penetration (Howard, 1997).
• Specialised signal transduction pathways that regulate the morphogenetic changes associated with pathogenesis (Dean, 1997; Hamer and Holden, 1997; Kronstad et al., 1998).
• The existence of a gene-for-gene relationship between M. grisea and its hosts, involving genetically dominant fungal avirulence genes and plant resistance genes (Laugé and De Wit, 1998).

Figure 1.1 Low temperature scanning electron micrograph showing appressorium differentiation by Magnaporthe grisea on the surface of a rice leaf. A conidium (c) has landed and attached near a stoma (St). It has germinated through elongation of a short germ tube, whose tip has further differentiated into a dome-shaped appressorium (a). This melanized inflated cell is responsible for turgor-driven penetration of the leaf cuticle. (Internal scale bar = 10μm).

The biology of rice blast has been studied using a combination of genetic and physiological approaches. The pre-penetration stages in the development of M. grisea can, for example, be reproducibly induced and adjusted in vitro on artificial surfaces, such as hydrophobic plastic membranes (Bourett and Howard, 1990) or onion epidermis (Chida and Sisler, 1987). The fungus is amenable to classical genetic analysis through sexual crosses (Valent et al., 1986), by isolation of rare fertile rice pathogenic isolates of the fungus and by introgression of fertility into stable laboratory strains of M. grisea (Valent et al., 1991). The development of a reliable DNA-mediated transformation system (Parsons et al., 1987; Leung et al., 1990) has also proved invaluable in allowing targeted gene replacement, gene disruption and heterologous expression of genes in M. grisea (Sweigard et al., 1992; Mitchell and Dean, 1995; Kershaw et al., 1998). The M. grisea genome has been extensively mapped, both genetically and physically (Sweigard et al., 1993; Hayashi and Naito, 1994; Smith and Leong, 1994; Kang et al., 1995; Diaz-Perez et al., 1996; Dioh et al., 1996; Zhu et al., 1997), and a publicly-funded international genome sequencing project has recently been initiated at several locations worldwide, coordinated from Clemson University Genome Center (Clemson, SC, USA) and in the private sector by the DuPont Company (Wilmington, DE, USA), amongst others.

Collectively, the application of these procedures has allowed a wealth of experimental data to be collected on the M. grisea-vice pathosystem, and a model can thus be made linking cytological, biochemical, physiological and molecular aspects of infection-related events. An understanding of how infection generally proceeds in M. grisea is thus beginning to emerge and should provide further insight into the general mechanisms of fungal pathogenicity, whilst also highlighting some of the inherent peculiarities of the M. grisea-rice interaction.

1.3 The onset of infection: infection court preparation and appressorium differentiation

M. grisea is a heterothallic pyrenomycete that can infect a wide range of grass species. The host spectrum of any particular strain of M. grisea is narrow, however, suggesting an ancient phylogenetic divergence between rice-pathogenic and non-pathogenic forms, as revealed by the conservation (or propagation) of MGR586 repeated sequences solely in rice pathogenic isolates of the fungus (Hamer et al., 1989a). In the field, asexual reproduction of M. grisea predominates and the fungus reproduces by means of asexual conidia produced from disease lesions. Three-celled pyriform conidia are formed in a sympo-dial fashion at the tip of slender conidiophores that emerge into the air from lesions, either through stornata or by direct rupture of the cuticle (Howard and Valent, 1996). Despite the existence of sexual reproduction and reports of sexual recombination in the field (Zeigler, 1998), sexual reproductive structures seem to play little, if any, role in the infection cycle, the subsequent evolution of the disease, or the genetic variability observed among pathogen populations (Valent, 1997).

Rice blast disease is primarily propagated through conidia, which are dispersed onto healthy leaves from neighbouring sporulating sites by wind and water-splash, thus initiating multiple rounds of infection (Ou, 1985). Contact with water rapidly triggers the release and hydration of a glyco-conjugated mucilage stored in the periplasm at the spore apex. This serves as an adhesive to anchor the conidium to the highly hydrophobic rice leaf, in a water environment favourable for subsequent infection events, whilst resisting the flow of water (Hamer et al., 1988). In the course of infection, mucilage is further syn-thesised to attach newly formed structures (germ tubes and appressoria) to the substratum. Spore tip mucilage (STM)-mediated attachment occurs regardless of whether the host is resistant or susceptible to M. grisea. Consistent with this, appressorium formation is induced on non-host synthetic substrates to the same extent as on host leaves, and can thus be considered a non-selective process (Gilbert et al., 1996). STM-mediated attachment appears to represent a prerequisite for completion of the appressorium differentiation process and subsequent infection (Jelitto et al., 1994; Xiao et al., 1994a; Gilbert tal, 1996).

There is now a growing body of evidence implicating particular physical and chemical characteristics of the rice leaf in the induction of appressorium development. These include: hydrophobicity (Lee and Dean, 1994); surface hardness (Xiao et al., 1994b); cutin monomers and wax polar lipids (Uchiyama and Okuyama, 1990; Gilbert et al., 1996). Taken singly, these properties are by no means specific to rice and are found in other plant species. However, collectively, these diverse cues may act to relay the presence of a conducive environment and later to interact with fungal-derived molecules present at the fungus/plant interface. These molecules include the class I hydrophobin, MPGlp (Talbot et al., 1993; Beckerman and Ebbole, 1996; Talbot et al., 1996), and several, as yet unidentified, mucilage glycoproteins with α-D mannose and α-D glucose residues (Xiao et al., 1994a). The composition of the mucilage that surrounds the developing germ tube and appressorium appears to be somewhat peculiar to M. grisea, containing an abundance of neutral lipids and glycolipids (Ebata et al., 1998). The significance of mannose-substituted glycoproteins is emphasised by the fact that mannose-binding rice lectin can interfere with development of the appressorium (Teraoka et al., 1999).

One important component in the development of appressoria is a cell wall protein encoded by the MPG1 gene. MPG1 was first isolated as a pathogenicity determinant, specifically expressed during appressorium morphogenesis and in planta (Talbot et al., 1993). MPG1 was shown to encode a fungal hydrophobin, a class of proteins implicated in a number of fungal developmental processes, including, most notably, the formation of aerial hyphae (Talbot, 1999; Wösten et al., 1999). Hydrophobins are morphogenetic proteins that are secreted by fungi and undergo polymerisation in response to air-water or hydrophobic surface interfaces (Wessels, 1997). Once polymerised, hydrophobins form amphipathic membranous structures with hydrophobic rodlets decorating one side. These rodlet layers coat the surfaces of spores and aerial hyphae of fungi, providing a hydrophobic surface that may be required for growth into the air and protection from subsequent desiccation (Wessels, 1997; Talbot, 1999). Hydrophobins may also play a role in spore dispersal and their abundance, variety and conservation among fungal species indicates that they perform a number of other functions in development (Kershaw and Talbot, 1998; Talbot, 1999).

The MPGl hydrophobin was shown to self-assemble at the rice leaf surface, providing an amphipathic layer upon which subsequent appressorium development occurs (Talbot et al., 1996). This polymer appears to serve as a morphogenetic sensor of an inductive surface for appressorium formation, because Δmpgl mutants are reduced in their ability to form appressoria (Talbot et al., 1993, 1996; Beckerman and Ebbole, 1996). The significance of the hydrophobin self-assembly process to appressorium development has been highlighted by the fact that diverse hydrophobins can substitute for MPGlp if expressed under control of the MPG1 promoter in M. grisea. This shows that hydrophobin production is important ...

Table des matières

• Cover
• Half Title
• Series Page
• Title Page
• Copyright Page
• Preface
• Contributors
• Table of Contents
• 1 Fungal pathogenicity—establishing infection
• 2 Bacterial pathogenicity
• 3 Viral pathogenicity
• 4 Genetic analysis and evolution of plant disease resistance genes
• 5 Resistance genes and resistance protein function
• 6 Signalling in plant disease resistance
• 7 Programmed cell death in plants in response to pathogen attack
• 8 Systemic acquired resistance
• 9 Transgenic approaches to disease resistant plants as exemplified by viruses
• 10 Emerging technologies and their application in the study of host-pathogen interactions
• Index