The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense

Matteo, Adele Di; Federici, L.; Mattei, Benedetta; Salvi, G.; Johnson, Kenneth A.; Savino, C.; Lorenzo, Giulia De; Tsernoglou, Demetrius; Cervone, Felice

doi:10.1073/pnas.1733690100

Cited by 205 publications

(288 citation statements)

References 41 publications

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“…These observations are consistent with the observed competitive mode of inhibition. Notably, a similar mode of inhibition has been proposed for PGIP, a protein inhibitor of fungal polygalacturonases Di Matteo et al, 2003), suggesting that 8 Thr193 Ser105 1 Trp223 Asp116 3 Lys224 Asp116 5 Gln299 Asn98 8 The number of atom-atom contacts at a distance of below 4.1 Å have been identified using the program Contact (CCP4). this may represent a general strategy evolved by plants for controlling pectic enzymes.…”

Section: The Inhibitor Folds In An Up-and-down Four-helical Bundlementioning

confidence: 73%

Structural Basis for the Interaction between Pectin Methylesterase and a Specific Inhibitor Protein

Matteo¹,

Giovane

Raiola³

et al. 2005

Plant Cell

203

224

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Pectin, one of the main components of the plant cell wall, is secreted in a highly methyl-esterified form and subsequently deesterified in muro by pectin methylesterases (PMEs). In many developmental processes, PMEs are regulated by either differential expression or posttranslational control by protein inhibitors (PMEIs). PMEIs are typically active against plant PMEs and ineffective against microbial enzymes. Here, we describe the three-dimensional structure of the complex between the most abundant PME isoform from tomato fruit (Lycopersicon esculentum) and PMEI from kiwi (Actinidia deliciosa) at 1.9-Å resolution. The enzyme folds into a right-handed parallel b-helical structure typical of pectic enzymes. The inhibitor is almost all helical, with four long a-helices aligned in an antiparallel manner in a classical up-and-down fourhelical bundle. The two proteins form a stoichiometric 1:1 complex in which the inhibitor covers the shallow cleft of the enzyme where the putative active site is located. The four-helix bundle of the inhibitor packs roughly perpendicular to the main axis of the parallel b-helix of PME, and three helices of the bundle interact with the enzyme. The interaction interface displays a polar character, typical of nonobligate complexes formed by soluble proteins. The structure of the complex gives an insight into the specificity of the inhibitor toward plant PMEs and the mechanism of regulation of these enzymes.

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Section: The Inhibitor Folds In An Up-and-down Four-helical Bundlementioning

confidence: 73%

Structural Basis for the Interaction between Pectin Methylesterase and a Specific Inhibitor Protein

Matteo¹,

Giovane

Raiola³

et al. 2005

Plant Cell

203

224

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“…6A). The N terminus of the PGIP structure contains two pairs of conserved Cys, which form disulfide bridges capping its solenoid structure (Di Matteo et al, 2003). This apparent homology suggests a potential role for the corresponding Cys in the second group of RLPs.…”

Section: Identification Of Likely Functional Residues In Cf-rlpsmentioning

confidence: 99%

“…These can be differentiated from RLPs and RLKs by their lack of a TM domain or kinase domain. Although no structure of an RLP or RLK has yet been reported, the structure of a bean (Phaseolus vulgaris) PGIP has recently been solved (Protein Data Bank ID 1OGQA), and provides a good basis for modeling RLPs and RLKs (Di Matteo et al, 2003).…”

mentioning

confidence: 99%

Phylogenomic Analysis of the Receptor-Like Proteins of Rice and Arabidopsis

et al. 2005

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The tomato (Lycopersicon esculentum) Cf-9 resistance gene encodes the first characterized member of the plant receptor-like protein (RLP) family. Other RLPs such as CLAVATA2 and TOO MANY MOUTHS are known to regulate development. The domain structure of RLPs consists of extracellular leucine-rich repeats, a transmembrane helix, and a short cytoplasmic region. Here, we identify 90 RLPs in rice (Oryza sativa) and compare them with functionally characterized RLPs from different plant species and with 56 Arabidopsis (Arabidopsis thaliana) RLPs, including the downy mildew resistance protein RPP27. Many RLPs cluster into four distinct superclades, three of which include RLPs known to be involved in plant defense. Sequence comparisons reveal diagnostic amino acid residues that may specify different molecular functions in different RLP subtypes. This analysis of rice RLPs thus identified at least 73 candidate resistance genes and four genes potentially involved in development. Due to the synteny between rice and other Gramineae, this analysis should provide valuable tools for experimental studies in rice and other cereals.

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“…PGIPs predominantly consist of leucine-rich repeats (LRRs), which fold with a concave inner surface presenting a cluster of negatively charged residues that are probably involved in interactions with PGs [27]. Extracellular LRRs are also found in receptor-like kinases and it is possible that PGIPs evolved from these LRR proteins by truncation and subsequent specialization.…”

Section: Wheat Inhibitor Xip-i Targets Fungal Gh11 and Gh10 Xylanasesmentioning

confidence: 99%

Enzyme–inhibitor interactions at the plant–pathogen interface

Misas-Villamil

Hoorn

2008

Current Opinion in Plant Biology

115

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The plant apoplast during plant-pathogen interactions is an ancient battleground that holds an intriguing range of attacking enzymes and counteracting inhibitors. Examples are pathogen xylanases and polygalacturonases that are inhibited by plant proteins like TAXI, XIP, and PGIP; and plant glucanases and proteases, which are targeted by pathogen proteins such as GIP1, EPI1, EPIC2B, and AVR2. These seven well-characterized inhibitors have different modes of action and many probably evolved from inactive enzymes themselves. Detailed studies of the structures, sequence variation, and mutated proteins uncovered molecular struggles between these enzymes and their inhibitors, resulting in positive selection for variant residues at the contact surface, where single residues determine the outcome of the interaction. Introduction Extracellular plant-pathogen interactions probably existed long before the evolution of pathogen effector translocation systems and plant resistance (R) genes. The molecular basis of these interactions is mostly undiscovered but some have been investigated in detail and reveal intriguing mechanisms. Here we will highlight major recent findings of extracellular enzyme-inhibitor interactions at the plant-pathogen interface.Although extracellular plant-pathogen interactions are complex, they can be simplified by assuming that they evolved in several stages (Figure 1). First, micro-organisms became pathogens by attacking plants using cell-wall-degrading enzymes and other hydrolases ( Figure 1A). In response to this attack, plants secrete inhibitors that suppress these hydrolases ( Figure 1B). Initially, these inhibitors were probably constitutively produced, but upon evolution of pathogen recognition systems the production and secretion of these proteins became inducible, becoming part of the arsenal of pathogenesis-related (PR) proteins. Besides suppression of pathogen attack, counter attack mechanisms also evolved in plants through the induced secretion of hydrolytic enzymes ( Figure 1C). Examples are the well-studied PR proteins including endo-b-1,3-glucanases (PR-2), chitinases (PR-3), and proteases (PR-7) [1 ]. Pathogens, in turn, responded to this counter attack by producing inhibitors that suppress these enzymes ( Figure 1D). The fifth and latest step was a sophisticated refinement of the pathogen recognition system by the evolution of R genes that recognize the manipulation of plant targets by pathogens, inducing a severe defense response that includes cell death ( Figure 1E). Aspects of this simplified model are consistent with the 'zigzag' model for the plant immune system, which explains the suppression of basal defense responses by pathogen effector proteins, followed by the evolution of efficient effector recognition by R proteins [2].Antagonistic interactions between organisms at the molecular level result in enzymes that evade inhibition, and inhibitors that adapt to these new enzymes. These 'molecular struggles' result in positive selection for variation of residues at the interactio...

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The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense

Cited by 205 publications

References 41 publications

Structural Basis for the Interaction between Pectin Methylesterase and a Specific Inhibitor Protein

Structural Basis for the Interaction between Pectin Methylesterase and a Specific Inhibitor Protein

Phylogenomic Analysis of the Receptor-Like Proteins of Rice and Arabidopsis

Enzyme–inhibitor interactions at the plant–pathogen interface

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