An extracellular aspartic protease functions in Arabidopsis disease resistance signaling

Xia, Yiji; Suzuki, Hideyuki; Borevitz, Justin O.; Blount, Jack W.; Guo, Zhai; Patel, Kanu; Dixon, Richard A.; Lamb, Christopher J.

doi:10.1038/sj.emboj.7600086

Cited by 323 publications

(312 citation statements)

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“…Hyperactivation of the aspartyl protease CONSTITUTIVE DISEASE RESISTANCE1 in Arabidopsis causes spontaneous (lesion mimic) cell death (Xia et al, 2004). In contrast, the aspartyl protease encoded by the PROMOTION OF CELL SURVIVAL1 gene in Arabidopsis functions to promote cell survival during embryogenesis and gametogenesis, and its ectopic overexpression blocks normal PCD processes associated with anther dehiscence (Ge et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

Aspartyl Protease-Mediated Cleavage of BAG6 Is Necessary for Autophagy and Fungal Resistance in Plants

et al. 2016

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The Bcl-2-associated athanogene (BAG) family is an evolutionarily conserved group of cochaperones that modulate numerous cellular processes. Previously we found that Arabidopsis thaliana BAG6 is required for basal immunity against the fungal phytopathogen Botrytis cinerea. However, the mechanisms by which BAG6 controls immunity are obscure. Here, we address this important question by determining the molecular mechanisms responsible for BAG6-mediated basal resistance. We show that Arabidopsis BAG6 is cleaved in vivo in a caspase-1-like-dependent manner and via a combination of pulldowns, mass spectrometry, yeast two-hybrid assays, and chemical genomics, we demonstrate that BAG6 interacts with a C2 GRAM domain protein (BAGP1) and an aspartyl protease (APCB1), both of which are required for BAG6 processing. Furthermore, fluorescence and transmission electron microscopy established that BAG6 cleavage triggers autophagy in the host that coincides with disease resistance. Targeted inactivation of BAGP1 or APCB1 results in the blocking of BAG6 processing and loss of resistance. Mutation of the cleavage site blocks cleavage and inhibits autophagy in plants; disease resistance is also compromised. Taken together, these results identify a mechanism that couples an aspartyl protease with a molecular cochaperone to trigger autophagy and plant defense, providing a key link between fungal recognition and the induction of cell death and resistance.

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Section: Discussionmentioning

confidence: 99%

Aspartyl Protease-Mediated Cleavage of BAG6 Is Necessary for Autophagy and Fungal Resistance in Plants

et al. 2016

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“…Given the clear contribution of enzymes in defense and virulence, it seems probable that the attacked organisms produce inhibitors. Examples of these secreted enzymes from both plants and fungi are lipases [50 ,51], chitinases [52], and proteases [53,54]. Besides diversification at interaction surfaces, substrate adaptation and inhibitor inactivation may be additional layers of manipulation in the molecular battlefield of extracellular plant-pathogen interactions.…”

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confidence: 99%

Enzyme–inhibitor interactions at the plant–pathogen interface

Misas-Villamil

Hoorn

2008

Current Opinion in Plant Biology

117

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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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“…This approach has been used to investigate resistance mechanisms with the expectation that elevated expression of defense signaling molecules may lead to a quantitative impact on resistance even where there is significant cross talk and functional redundancy. Thus, several new components have been shown to regulate plant-pathogen interactions (Grant et al, 2003;Xia et al, 2004;Zhang et al, 2007). Aiming to uncover genes involved in SA-mediated signaling mechanisms, we carried out activation tagging in SA-deficient Arabidopsis plants that constitutively express the bacterial salicylate hydroxylase (NahG; Gaffney et al, 1993).…”

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confidence: 99%

Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions

et al. 2009

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We isolated an activation-tagged Arabidopsis (Arabidopsis thaliana) line, constitutive disease susceptibility2-1D (cds2-1D), that showed enhanced bacterial growth when challenged with various Pseudomonas syringae strains. Systemic acquired resistance and systemic PATHOGENESIS-RELATED GENE1 induction were also compromised in cds2-1D. The T-DNA insertion adjacent to NINE-CIS-EPOXYCAROTENOID DIOXYGENASE5 (NCED5), one of six genes encoding the abscisic acid (ABA) biosynthetic enzyme NCED, caused a massive increase in transcript level and enhanced ABA levels .2-fold. Overexpression of NCED genes recreated the enhanced disease susceptibility phenotype. NCED2, NCED3, and NCED5 were induced, and ABA accumulated strongly following compatible P. syringae infection. The ABA biosynthetic mutant aba3-1 showed reduced susceptibility to virulent P. syringae, and ABA, whether through exogenous application or endogenous accumulation in response to mild water stress, resulted in increased bacterial growth following challenge with virulent P. syringae, indicating that ABA suppresses resistance to P. syringae. Likewise ABA accumulation also compromised resistance to the biotrophic oomycete Hyaloperonospora arabidopsis, whereas resistance to the fungus Alternaria brassicicola was enhanced in cds2-1D plants and compromised in aba3-1 plants, indicating that ABA promotes resistance to this necrotroph. Comparison of the accumulation of salicylic acid and jasmonic acid in the wild type, cds2-1D, and aba3-1 plants challenged with P. syringae showed that ABA promotes jasmonic acid accumulation and exhibits a complex antagonistic relationship with salicylic acid. Our findings provide genetic evidence that the abiotic stress signal ABA also has profound roles in modulating diverse plantpathogen interactions mediated at least in part by cross talk with the jasmonic acid and salicylic acid biotic stress signal pathways.

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An extracellular aspartic protease functions in Arabidopsis disease resistance signaling

Cited by 323 publications

References 49 publications

Aspartyl Protease-Mediated Cleavage of BAG6 Is Necessary for Autophagy and Fungal Resistance in Plants

Aspartyl Protease-Mediated Cleavage of BAG6 Is Necessary for Autophagy and Fungal Resistance in Plants

Enzyme–inhibitor interactions at the plant–pathogen interface

Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions

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