Tandemly Duplicated Arabidopsis Genes That Encode Polygalacturonase-Inhibiting Proteins Are Regulated Coordinately by Different Signal Transduction Pathways in Response to Fungal Infection

Ferrari, Simone; Vairo, Donatella; Ausubel, Frederick M.; Cervone, Felice; Lorenzo, Giulia De

doi:10.1105/tpc.005165

Cited by 243 publications

(293 citation statements)

References 73 publications

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“…Most genes showed the typical response of up-regulation during starvation and down-regulation upon resupply. Strikingly strong regulation was observed for genes encoding polygalacturonase inhibiting proteins (PGIP1, PGIP2; Ferrari et al, 2003), aspartic proteinases, protease-inhibitors, and several FAD-related oxidoreductases. A second pattern consisted of a strong up-regulation in roots and/or in shoots after K 1 resupply with weak or nondetectable change during long-term starvation.…”

Section: Defense Mechanisms and Production Of Secondary Metabolitesmentioning

confidence: 97%

The Potassium-Dependent Transcriptome of Arabidopsis Reveals a Prominent Role of Jasmonic Acid in Nutrient Signaling

2004

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Full genome microarrays were used to assess transcriptional responses of Arabidopsis seedlings to changing external supply of the essential macronutrient potassium (K+). Rank product statistics and iterative group analysis were employed to identify differentially regulated genes and statistically significant coregulated sets of functionally related genes. The most prominent response was found for genes linked to the phytohormone jasmonic acid (JA). Transcript levels for the JA biosynthetic enzymes lipoxygenase, allene oxide synthase, and allene oxide cyclase were strongly increased during K+ starvation and quickly decreased after K+ resupply. A large number of well-known JA responsive genes showed the same expression profile, including genes involved in storage of amino acids (VSP), glucosinolate production (CYP79), polyamine biosynthesis (ADC2), and defense (PDF1.2). Our findings highlight a novel role of JA in nutrient signaling and stress management through a variety of physiological processes such as nutrient storage, recycling, and reallocation. Other highly significant K+-responsive genes discovered in our study encoded cell wall proteins (e.g. extensins and arabinogalactans) and ion transporters (e.g. the high-affinity K+ transporter HAK5 and the nitrate transporter NRT2.1) as well as proteins with a putative role in Ca2+ signaling (e.g. calmodulins). On the basis of our results, we propose candidate genes involved in K+ perception and signaling as well as a network of molecular processes underlying plant adaptation to K+ deficiency.

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Section: Defense Mechanisms and Production Of Secondary Metabolitesmentioning

confidence: 97%

The Potassium-Dependent Transcriptome of Arabidopsis Reveals a Prominent Role of Jasmonic Acid in Nutrient Signaling

2004

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“…Ethylene has been proposed to be more effective against necrotrophic pathogens, such as B. cinerea than against biotrophic pathogens. Ethylene-insensitive mutants ein2, ein3, and etr1 show enhanced susceptibility to B. cinerea Ferarri et al 2003). Plants that overexpress transcription factors involved in the ethylene and JA pathways exhibit an increased resistance to several necrotrophs (Berrocal-Lobo et al 2002;Berrocal-Lobo and Molina 2004;Pré et al 2008).…”

Section: Discussionmentioning

confidence: 99%

A Combinatorial Interplay Among the 1-Aminocyclopropane-1-Carboxylate Isoforms Regulates Ethylene Biosynthesis inArabidopsis thaliana

et al. 2009

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Ethylene (C 2 H 4 ) is a unique plant-signaling molecule that regulates numerous developmental processes. The key enzyme in the two-step biosynthetic pathway of ethylene is 1-aminocyclopropane-1-carboxylate synthase (ACS), which catalyzes the conversion of S-adenosylmethionine (AdoMet) to ACC, the precursor of ethylene. To understand the function of this important enzyme, we analyzed the entire family of nine ACS isoforms (ACS1, ACS2, ACS4-9, and ACS11) encoded in the Arabidopsis genome. Our analysis reveals that members of this protein family share an essential function, because individual ACS genes are not essential for Arabidopsis viability, whereas elimination of the entire gene family results in embryonic lethality. Phenotypic characterization of single and multiple mutants unmasks unique but overlapping functions of the various ACS members in plant developmental events, including multiple growth characteristics, flowering time, response to gravity, disease resistance, and ethylene production. Ethylene acts as a repressor of flowering by regulating the transcription of the FLOWERING LOCUS C. Each single and high order mutant has a characteristic molecular phenotype with unique and overlapping gene expression patterns. The expression of several genes involved in light perception and signaling is altered in the high order mutants. These results, together with the in planta ACS interaction map, suggest that ethylene-mediated processes are orchestrated by a combinatorial interplay among ACS isoforms that determines the relative ratio of homo-and heterodimers (active or inactive) in a spatial and temporal manner. These subunit isoforms comprise a combinatorial code that is a central regulator of ethylene production during plant development. The lethality of the null ACS mutant contrasts with the viability of null mutations in key components of the ethylene signaling apparatus, strongly supporting the view that ACC, the precursor of ethylene, is a primary regulator of plant growth and development.

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“…PGs are important virulence factors for various fungi and bacteria, and a partial contribution of PGIPs to plant defense has been shown genetically using overexpression and gene silencing [22,23]. For example, B. cinerea BcPG1 is effectively inhibited by bean PvPGIP2 and PvPGIP2, and overexpression of these PGIPs in tobacco and Arabidopsis increases resistance to Botrytis infections [24].…”

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

confidence: 99%

“…Apart from directly suppressing PG activity, PGIPs are also thought to contribute to pathogen perception by preventing the degradation of oligogalacturonan elicitors that are released during infection [25]. PGIPs are widely distributed in the plant kingdom and are encoded by small gene families that are regulated by different pathways, probably minimizing pathogen interference in PGIP expression [22,26].…”

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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Tandemly Duplicated Arabidopsis Genes That Encode Polygalacturonase-Inhibiting Proteins Are Regulated Coordinately by Different Signal Transduction Pathways in Response to Fungal Infection

Cited by 243 publications

References 73 publications

The Potassium-Dependent Transcriptome of Arabidopsis Reveals a Prominent Role of Jasmonic Acid in Nutrient Signaling

The Potassium-Dependent Transcriptome of Arabidopsis Reveals a Prominent Role of Jasmonic Acid in Nutrient Signaling

A Combinatorial Interplay Among the 1-Aminocyclopropane-1-Carboxylate Isoforms Regulates Ethylene Biosynthesis inArabidopsis thaliana

Enzyme–inhibitor interactions at the plant–pathogen interface

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