Licensed to kill: the lifestyle of a necrotrophic plant pathogen

doi:10.1016/j.tplants.2006.03.005

Trends in Plant Science

Volume 11, Issue 5, May 2006, Pages 247-253

https://doi.org/10.1016/j.tplants.2006.03.005 Get rights and content

Necrotrophic plant pathogens have received an increasing amount of attention over the past decade. Initially considered to invade their hosts in a rather unsophisticated manner, necrotrophs are now known to use subtle mechanisms to subdue host plants. The gray mould pathogen Botrytis cinerea is one of the most comprehensively studied necrotrophic fungal plant pathogens. The genome sequences of two strains have been determined. Targeted mutagenesis studies are unraveling the roles played in the infection process by a variety of B. cinerea genes that are required for penetration, host cell killing, plant tissue decomposition or signaling. Our increasing understanding of the tools used by a necrotrophic fungal pathogen to invade plants will be instrumental to designing rational strategies for disease control.

Section snippets

Necrotrophic plant pathogens

Biotrophic plant pathogenic microbes such as downy or powdery mildews and rusts are generally accepted to have an intricate biological interaction with their host plant [1], presumably as a result of co-evolution [2]. Many plant pathologists have long considered that necrotrophic plant pathogenic fungi do not have much of a ‘real’ interaction with their host. Necrotrophs kill host cells by means of toxic molecules and lytic enzymes and they subsequently decompose the plant tissue and consume it

Brief history of white and gray mould

The genus Botrytis was established as early as 1729. Fungi from the family of Sclerotiniaceae are among the earliest studied plant pathogens. In 1886, Anton De Bary [4] described the ability of S. sclerotiorum, a close relative of B. cinerea, to kill and macerate plant cells. He could microscopically distinguish both processes and could mimic these by administering cell-free extracts of fungal cultures to plant tissues. Similar studies were performed on B. cinerea in the first half of the 20th

Penetrating the host tissue

Pathogens landing on a leaf must penetrate the host surface, which is composed of cutin covered with wax. There is cytological [11] and molecular-genetic [12] evidence for B. cinerea developing appressoria (infection structures that differentiate on the surface and form a penetration peg that breaches the cuticle) (Figure 2b) [11]. Appressoria of the rice blast fungus Magnaporthe grisea penetrate by exerting an extreme physical pressure on the host tissue, resulting from high osmotic turgor in

Host cell death requires the active participation of the pathogen and the host

B. cinerea possesses multiple tools that facilitate host cell death.

Decomposition and consumption of plant biomass

The ultimate goal of a necrotrophic plant pathogen is not to kill its host plant per se but to decompose plant biomass and convert it into fungal mass. A common feature shared by all plant species that are colonized by B. cinerea (i.e. dicots and corolliferous monocots) is their relatively high content of pectin in the cell wall. Plant species with low pectin contents are considered poor hosts for B. cinerea. It was therefore postulated that the host preference of B. cinerea reflects its

Infection requires intricate sensing and signaling

The infection of a host plant is a highly regulated process in which the pathogen must decide whether or not to germinate, when and where to develop an infection structure (appressorium) or produce enzymes and metabolites. There must be continuous sensing of the physical and chemical environment to make the correct decisions (Figure 2a). Sensing and signaling therefore play an important role in all stages of infection [51]. For example, M. grisea can germinate on hydrophilic as well as on

Perspectives

Botrytis cinerea uses multiple strategies to subdue its host plant(s). So far, the ‘silver bullet’, which is crucial for an infection to succeed on all host tissues without affecting fungal growth in vitro, has not been identified and might not exist. Certain virulence factors can be important for one isolate on one particular host species, but they might be dispensable on another host species, or they might be dispensable for a different isolate 24, 47, 48. I prefer not to use the term

Acknowledgements

I am grateful to Bettina and Paul Tudzynski, Matthias Hahn, Günther Doehlemann, Peter van Baarlen and Jos Raaijmakers for critical reading of the manuscript.

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Trends in Plant Science

Licensed to kill: the lifestyle of a necrotrophic plant pathogen

Section snippets

Necrotrophic plant pathogens

Brief history of white and gray mould

Penetrating the host tissue

Host cell death requires the active participation of the pathogen and the host

Decomposition and consumption of plant biomass

Infection requires intricate sensing and signaling

Perspectives

Acknowledgements

Trends Plant Sci.

FEMS Microbiol. Lett.

Phytochemistry

Phytochemistry

Curr. Biol.

Physiol. Mol. Plant Pathol.

Fungal Genet. Biol.

Physiol. Mol. Plant Pathol.

Fungal Genet. Biol.

Physiol. Mol. Plant Pathol.

Physiol. Mol. Plant Pathol.

Fungal Genet. Biol.

FEMS Microbiol. Ecol.

Evolution of plant resistance at the molecular level: ecological context of species interactions

Heredity

Host-selective toxins and avirulence determinants: what's in a name?

Annu. Rev. Phytopathol.

Ueber einige Sclerotinien und Sclerotienkrankheiten

Botanische Zeitschrift

Toxins and cell-wall dissolving enzymes in relation to plant disease

Annu. Rev. Phytopathol.

Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen

Mol. Plant Pathol.

Agrobacterium-mediated transformation of Botrytis cinerea, simple purification of monokaryotic transformants and rapid conidia-based identification of the transfer-DNA host genomic DNA flanking sequences

Curr. Genet.

Approaches to molecular genetics and genomics of Botrytis

Expressed sequence tags from the phytopathogenic fungus Botrytis cinerea

Eur. J. Plant Pathol.

Morphology and cellular organization in Botrytis interactions with plants

The tetraspanin BcPls1 is required for appressorium-mediated penetration of Botrytis cinerea into host plant leaves

Mol. Microbiol.

Glycerol generates turgor in rice blast

Nature

PLS1, a gene encoding a tetraspanin-like protein, is required for penetration of rice leaf by the fungal pathogen Magnaporthe grisea

Proc. Natl. Acad. Sci. U. S. A.

Cutinase A of Botrytis cinerea is expressed, but not essential, during penetration of gerbera and tomato

Mol. Plant Microbe Interact.

Molecular and functional characterization of a secreted lipase from Botrytis cinerea

Mol. Plant Pathol.

The genome sequence of the rice blast fungus Magnaporthe grisea

Nature

In situ localization of AOS in host–pathogen interactions

Microsc. Microanal.

The ultrastructure of interactions between Botrytis species and broad bean leaves

Physiol. Plant Pathol.

Necrotising activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris

Plant J.

The putative role of botrydial and related metabolites in the infection mechanism of Botrytis cinerea

J. Chem. Ecol.

Functional analysis of the cytochrome P450 monooxygenase gene Bcbot1 of Botrytis cinerea indicates that botrydial is a strain-specific virulence factor

Mol. Plant Microbe Interact.

Virulence-toxin production relationship in isolates of the plant pathogenic fungus Botrytis cinerea

J. Phytopathol.

Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum

Annu. Rev. Phytopathol.

Functional analysis of an extracellular catalase of Botrytis cinerea

Mol. Plant Pathol.

Botrytis cinerea induces the formation of free radicals in fruits of Capsicum annuum at positions remote from the site of infection

Protoplasma