Identification of target amino acids that affect interactions of fungal polygalacturonases and their plant inhibitors

Stotz, Henrik U.; Bishop, John G.; Bergmann, Carl; Koch, Marcus A.; Albersheim, Peter; Darvill, Alan G.; Labavitch, John M.

doi:10.1006/pmpp.2000.0258

Cited by 127 publications

(96 citation statements)

References 32 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…However, frequency of nonsynonymous substitutions significantly higher than those in the other portion of the ORF indicated a higher variability of the xxLxLxx region, consistent with the hypervariability observed in many R genes (Meyers et al, 1998;Hulbert et al, 2001;Lehmann, 2002) and the role of this region in ligand recognition (Warren et al, 1998;Leckie et al, 1999). Maximum likelihood models of codon evolution in protein-coding DNA sequences (Nielsen and Yang, 1998) have been applied to pgip genes from several dicots to propose that positive selection acting at a handful of sites is responsible for the evolution of these genes (Stotz et al, 2000). Unfortunately, this model cannot be applied at this stage to analyze the intraspecific evolution of the bean pgip family, due to the low number of members and the low degree of variability of paralogs and homologs so far characterized.…”

Section: Discussionmentioning

confidence: 57%

“…Instead, replacements at 224 determine gain/loss of recognition of FmPG both between paralogous genes (PvPPGIP1 versus PvPPGIP2; Leckie et al, 1999) and between corresponding genes of different genotypes (PvBPGIP2 versus PvPPGIP2). Surprisingly, neither position is among those that are proposed to evolve adaptively in PGIPs, according to models of codon evolution (Stotz et al, 2000). Duplication and diversification of Pvpgip genes result not only in a diversification of their biochemical function, but also in a diversification of their regulation.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Characterization of the Complex Locus of Bean Encoding Polygalacturonase-Inhibiting Proteins Reveals Subfunctionalization for Defense against Fungi and Insects

et al. 2004

View full text Add to dashboard Cite

Polygalacturonase-inhibiting proteins (PGIPs) are extracellular plant inhibitors of fungal endopolygalacturonases (PGs) that\ud belong to the superfamily of Leu-rich repeat proteins. We have characterized the full complement of pgip genes in the bean\ud (Phaseolus vulgaris) genotype BAT93. This comprises four clustered members that span a 50-kb region and, based on their\ud similarity, form two pairs (Pvpgip1/Pvpgip2 and Pvpgip3/Pvpgip4). Characterization of the encoded products revealed both\ud partial redundancy and subfunctionalization against fungal-derived PGs. Notably, the pair PvPGIP3/PvPGIP4 also inhibited\ud PGs of two mirid bugs (Lygus rugulipennis and Adelphocoris lineolatus). Characterization of Pvpgip genes of Pinto bean showed\ud variations limited to single synonymous substitutions or small deletions. A three-amino acid deletion encompassing a residue\ud previously identified as crucial for recognition of PG of Fusarium moniliforme was responsible for the inability of BAT93\ud PvPGIP2 to inhibit this enzyme. Consistent with the large variations observed in the promoter sequences, reverse\ud transcription-PCR expression analysis revealed that the different family members differentially respond to elicitors, wounding,\ud and salicylic acid. We conclude that both biochemical and regulatory redundancy and subfunctionalization of pgip genes are\ud important for the adaptation of plants to pathogenic fungi and phytophagous insects

show abstract

Section: Discussionmentioning

confidence: 57%

Section: Discussionmentioning

confidence: 99%

Characterization of the Complex Locus of Bean Encoding Polygalacturonase-Inhibiting Proteins Reveals Subfunctionalization for Defense against Fungi and Insects

et al. 2004

View full text Add to dashboard Cite

show abstract

“…With a single lysine-to-glutamine mutation at position 224, PvPGIP1 acquired the ability to interact with FmPG1 [31]. Importantly, this position is among the seven sites under diversifying selection that were found around the negatively charged pocket implicated in PG binding (blue and red in Figure 2e) [32,33 ]. Sequencing PGs from different Fusarium spp.…”

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

120

View full text Add to dashboard Cite

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...

show abstract

“…Adaptive replacements occur disproportionately in the active site cleft of the enzyme, suggesting that chitinolytic activity in plants responds to inhibitor evolution in fungal pathogens. Likewise, adaptive molecular evolution occurs in plant polygalacturonase inhibitor proteins (Stotz et al, 2000), which bind fungal polygalacturonases. Finally, nucleotide polymorphism at the wip1 wound-inducible serine protease inhibitor locus in the Zea genus was shown not to differ from neutral expectations (Tiffin and Gaut, 2001).…”

Section: Patterns Of Genetic Variation At Resistance Locimentioning

confidence: 99%

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

Meaux

Mitchell-Olds

2003

Heredity

View full text Add to dashboard Cite

Molecular data regarding the diversity of plant loci involved in resistance to herbivores or pathogens are becoming increasingly available. These genes demonstrate variable patterns of diversity, suggesting that they differ in their evolutionary history. In parallel, the study of natural variation for resistance, generally conducted at the phenotypic level, has shown that resistance does not evolve solely under selection pressures exerted by enemies. Metapopulation dynamics and other ecological characteristics of interacting species also appear to have a large impact on resistance evolution. Until now, studies of resistance at the molecular level have been conducted separately from ecological studies in extant populations. Future progress requires an evolutionary approach integrating both molecular and ecological aspects of resistance evolution. Such an approach will contribute greatly to our understanding of the evolution of molecular diversity at loci involved in biotic stress.

show abstract

Identification of target amino acids that affect interactions of fungal polygalacturonases and their plant inhibitors

Cited by 127 publications

References 32 publications

Characterization of the Complex Locus of Bean Encoding Polygalacturonase-Inhibiting Proteins Reveals Subfunctionalization for Defense against Fungi and Insects

Characterization of the Complex Locus of Bean Encoding Polygalacturonase-Inhibiting Proteins Reveals Subfunctionalization for Defense against Fungi and Insects

Enzyme–inhibitor interactions at the plant–pathogen interface

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

Contact Info

Product

Resources

About