ReviewPolygalacturonase-inhibiting proteins in defense against phytopathogenic fungi
Introduction
The cell wall is the first barrier that plant cells use to oppose the attack of pathogens. Most phytopathogenic microorganisms produce enzymes that are capable of degrading cell wall polymers. Cell-wall-degrading enzymes are particularly important for fungal pathogens that do not have specialized penetration structures and for necrotrophic pathogens during the late stages of the invasion process. The most extensively studied cell-wall-degrading enzymes are polygalacturonases (PGs; EC 3.2.1.15), which cleave the linkages between D-galacturonic acid residues in non-methylated homogalacturonan, a major component of pectins.
PGs are the first enzymes to be secreted by pathogens when they encounter plant cell walls 1., 2•., and their contribution to the pathogenicity of some fungi and bacteria has been assessed. Deletion of the PG pecA gene in Aspergillus flavus reduces lesion development in cotton balls, whereas expression of this gene in an A. flavus strain that lacks PG increases lesion size [3]. A PG gene is required for full virulence of Botrytis cinerea on different hosts [4], and of Alternaria citri on citrus fruit [5]. Importantly, the double knock-out of two PG genes (cppg1 and cppg2) in Claviceps purpurea renders the fungus nearly non pathogenic on rye without affecting its vegetative properties (KB Tenberge, O Tudzynski, personal communication). Endo-PG is also important for the colonization of tomato plants by the bacterium Ralstonia solanacearum [6•].
To accommodate pathogenesis in a variety of different conditions, PGs are highly variable in terms of primary structure, specific activity, pH optimum, substrate preference and mode of action. Polygalacturonase-inhibiting proteins (PGIPs) that are located in the plant cell wall counteract the action of PGs [7••], preventing cell wall degradation and therefore hampering the invasion process and the release of nutrients that is necessary for pathogen growth. As pathogenic fungi maintain PGs for pathogenicity, plants maintain PGIPs as an effective defense strategy. Furthermore, long-chain oligogalacturonides (OGs), which elicit many defense responses in plants, are produced when fungal PG activity is controlled by PGIPs 8., 9., 10•.. OGs responsible for the accumulation of H2O2 may be released in planta by endogenous PGs that are systemically induced after wounding [11]. Hence, it is tempting to speculate that PGIPs are involved in the production of OGs not only during pathogen infection but also after wounding. However, the inhibition of plant PGs by a PGIP has never been reported, and PGIPs seem to be ineffective against bacterial PGs or other pectic enzymes of either microbial or plant origin [12].
PGIP interacts with PG by engaging the same surface that apparently anchors the inhibitor to the cell wall. Binding assays with various preparations of pectins show that blockwise demethylated pectins, presumably produced by plant pectin methylesterase, are the preferential site of interaction for PGIP of Phaseolus vulgaris (bean) (O Zabotina, D Bellincampi, F Cervone, unpublished data). During pathogen attack, the pectin-anchored PGIP is expected to be released from pectin when the complex with a fungal PG is formed.
Section snippets
The structural and functional variability of PGIPs
Plants have evolved PGIPs with different recognition capabilities to counteract the many PGs secreted by pathogenic fungi. Not only do PGIPs from different plants differ in their inhibitory activity, but PGIPs from a single plant inhibit PGs from different fungi or different PGs from the same fungus, often with different strength [7••]. Moreover, biochemical analyses reveal that total PGIP activity in some plants, including bean [13], Arabidopsis, soybean and wheat (D Pontiggia, G De Lorenzo,
PGIPs as effectors of defense
Recent evidence demonstrates that PGIPs limit fungal invasion. Tomato plants overexpressing a pear pgip gene displayed reduced lesion area after B. cinerea inoculation [28••]. A decreased susceptibility to this fungus has also been observed in Arabidopsis plants overexpressing Atpgip1 and Atpgip2 separately (S Ferrari, F Cervone et al., unpublished data), and in tobacco expressing Pvpgip2 (C Manfredini, G De Lorenzo et al., unpublished data). Interestingly, in all of these cases, the infection
The structural basis of the interactive properties of PGIPs
All known PGIPs are glycoproteins of molecular mass around 40 kDa, and comprise 10 modules characterized by the consensus sequence for extracytoplasmic leucine-rich repeats (LRRs), GxIPxxLGxLxxLxxLxLxxNxLT/S 35., 36.. Within each LRR the sequence xxLxLxx is predicted to form a β-strand/β-turn structure, in which the x residues are solvent-exposed and involved in the interaction with ligands 18., 37., 38.. In all living organisms, LRR domains are specialized for interaction with protein ligands
Conclusions
Plants have evolved PGIPs with specific modes of expression and specific recognition capabilities for the many PGs secreted by phytopathogenic fungi. The role of PGIPs as important players in the defense response is now clear: they are induced early during infection, retard PG function, prevent cell wall degradation, and limit fungal growth and colonization. Furthermore, because of their ability to generate elicitor-active OGs, PGIPs are included among the microbe-detecting molecules that are
Acknowledgements
We thank the Giovanni Armenise-Harvard Foundation for supporting our research.
References and recommended reading
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References (54)
- et al.
Polygalacturonases are required for rapid colonization and full virulence of Ralstonia solanacearum on tomato plants
Physiol Mol Plant Pathol
(2000) - et al.
Pectins: structure, biosynthesis, and oligogalacturonide-related signaling
Phytochem
(2001) - et al.
Can Phaseolus PGIP inhibit pectic enzymes from microbes and plants?
Phytochem
(1990) - et al.
Signal transmission in the plant immune response
Trends Plant Sci
(2001) - et al.
Identification of target amino acids that effect interactions of fungal polygalacturonases and their plant inhibitors
Physiol Mol Plant Pathol
(2000) - et al.
Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato
Cell
(1997) - et al.
Differential accumulation of polygalacturonase-inhibiting protein (PGIP) mRNA in two near-isogenic lines of Phaseolus vulgaris L. upon infection with Colletotrichum lindemuthianum
Physiol Mol Plant Pathol
(1996) - et al.
The leucine-rich repeat as a protein recognition motif
Curr Opin Struct Biol
(2001) The biology of the small leucine-rich proteoglycans — functional network of interactive proteins
J Biol Chem
(1999)- et al.
Decorin is a biological ligand for the epidermal growth factor receptor
J Biol Chem
(1999)
Structure, function and evolution of plant disease resistance genes
Curr Opin Plant Biol
Putting knowledge of plant disease resistance genes to work
Curr Opin Plant Biol
1.68-Å crystal structure of endopolygalacturonase II from Aspergillus niger and identification of active site residues by site-directed mutagenesis
J Biol Chem
Fungal invasion enzymes and their inhibition
Pathogenicity genes of phytopathogenic fungi
Mol Plant Pathol
Molecular genetic evidence for the involvement of a specific polygalacturonase, P2c, in the invasion and spread of Aspergillus flavus in cotton bolls
Appl Environ Microbiol
The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea
Mol Plant Microbe Interact
Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata
Mol Plant Microbe Interact
The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi
Annu Rev Phytopathol
Host–pathogen interactions. XXXIII. A plant protein converts a fungal pathogenesis factor into an elicitor of plant defense responses
Plant Physiol
Perception of fungal elicitors and signal transduction
A wound- and systemin-inducible polygalacturonase in tomato leaves
Proc Natl Acad Sci USA
Polygalacturonase-inhibiting proteins (PGIPs) with different specificities are expressed in Phaseolus vulgaris
Mol Plant Microbe Interact
Cytological localization of the pgip genes in the embryo suspensor cells of Phaseolus vulgaris L
Theor Appl Genet
Molecular characterization of a polygalacturonase inhibitor from Pyrus communis L. cv. Bartlett
Plant Physiol
Structure and expression of an inhibitor of fungal polygalacturonases from tomato
Plant Mol Biol
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana
Nature
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