A Plant Vacuolar Protease, VPE, Mediates Virus-Induced Hypersensitive Cell Death

Hatsugai, Noriyuki; Kuroyanagi, Miwa; Yamada, Kenji; Meshi, Tetsuo; Tsuda, Shinya; Kondo, Maki; Nishimura, Mikio; Hara‐Nishimura, Ikuko

doi:10.1126/science.1099859

Cited by 569 publications

(670 citation statements)

References 26 publications

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“…Caspase-1-like activities have been reported in several plant-microbe interactions. For example, vacuolar processing enzyme (VPE), a cysteine protease localized to the vacuole, is required for TMV-mediated HR-PCD and resistance (Hatsugai et al, 2004). Inoculation of tobacco with an incompatible strain of Pseudomonas syringae or B. cinerea triggered caspase-1-like activity that was suppressed in the VPE mutant background.…”

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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“…Other cell death routes are likely to be induced via NDR1 because AvrRpm1 triggered cell death was only suppressed to levels observed for ndr1, and we could not suppress NDR1-dependent cell death. These pathways could include vacuolar proteases or metacaspases (Hatsugai et al, 2004;He et al, 2008), but how these enzymes relate to autophagy is currently unknown.…”

Section: Multiple Routes To Cell Death In Plant Pathogen Interactionsmentioning

confidence: 99%

Autophagic Components Contribute to Hypersensitive Cell Death in Arabidopsis

Hofius¹

2009

Journal of End-to-End-testing

156

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SUMMARYAutophagy has been implicated as a prosurvival mechanism to restrict programmed cell death (PCD) associated with the pathogen-triggered hypersensitive response (HR) during plant innate immunity. This model is based on the observation that HR lesions spread in plants with reduced autophagy gene expression. Here, we examined receptor-mediated HR PCD responses in autophagy-deficient Arabidopsis knockout mutants (atg), and show that infectioninduced lesions are contained in atg mutants. We also provide evidence that HR cell death initiated via Toll/Interleukin-1 (TIR)-type immune receptors through the defense regulator EDS1 is suppressed in atg mutants. Furthermore, we demonstrate that PCD triggered by coiled-coil (CC)-type immune receptors via NDR1 is either autophagy-independent or engages autophagic components with cathepsins and other unidentified cell death mediators. Thus, autophagic cell death contributes to HR PCD and can function in parallel with other prodeath pathways.

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“…10,11 A paper in Science reported that VPE localizes in the vacuolar membrane and mediates virus-induced hypersensitive cell death by regulating the collapse of this membrane. 12 VPEs, including seed-type VPE and vegetative-type VPE, were originally discovered as cysteine proteinases responsible for the maturation of vacuolar proteins. 13,14 Elicitors can activate plant innate immunity.…”

Section: Role Of Vpe In Pcdmentioning

confidence: 99%

“…9 Therefore, the molecular identification of protein kinases with caspase activity will help us elucidate elicitor signal transduction. As VPE was identified to have YVADase activity and to be involved in various cell death responses, 12,19 we postulated that elicitor signals are transduced via VPEs in plants. …”

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confidence: 99%

The role of vacuolar processing enzymes in plant immunity

Zhang

Zheng

2010

Plant Signaling & Behavior

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In the course of their development, plants have had to face a wide range of potential pathogens, including viral, bacterial, fungal and oomycete pathogens. Plants, unlike animals, which have specialized defender cells and an adaptive immune system, have an innate immunity of each cell and produce systemic signals emanating from the infection site. The plant innate immunity (PTI) is induced by pathogen-associated molecular patterns (PAMPs) 1 and elicitors. 2,3 However, some pathogens deliver virulence proteins that target host protein to overcome the plant immunity response. Most plants have evolved the corresponding resistance (R) protein to recognize effector activity, which will trigger plant resistance through effector-triggered immunity (ETI). 4 Natural selection drives evolution of new pathogen effector proteins and plant R proteins. This tug-of-war between plants and pathogens is represented as a zig-zag-zig model. [5][6][7] Both PTI and ETI cause stomatal closure and hypersensitive response (HR), a programmed host cell death (PCD) to limit pathogen development. 5,8 Proteases play important roles in plant innate immunity. in this mini-review, we describe the current view on the role of a plant protease, vacuolar processing enzyme (vPe), and the first identified plant caspase-1-like protein, in plant immunity. in the past several years, vPes were determined to play important roles in various types of cell death in plants. early studies demonstrated the identification of vPe as a vacuolar hydrolytic protein responsible for maturation of vacuolar proteins. Later, Nicotiana benthamiana vPe was reported to mediate virusinduced hypersensitive response by regulating membrane collapse. The ortholog of vPe in Arabidopsis is also suggested to be involved in both mycotoxin-induced cell death and developmental cell death. However, the role of vPe in elicitorsignaling is still unclear. Our recent studies demonstrated the involvement of vPe in elicitor signal transduction to induce stomatal closure and defense responses, including defense gene expression and hypersensitive cell death. Key words: hypersensitive cell death, elicitor, stomatal closure, pathogen-associated molecular patterns, plant innate immunity, programmed cell death activity. At least eight caspase activities have now been measured in plant extracts, which were found using caspase substrates, and various caspase inhibitors can block many forms of plant programmed cell death. 9 In the past several years, vacuolar-processing enzyme (VPE) has been determined to play important roles in plant immunity responses. In this review paper, I describe the current view on the role of VPE in plant immunity, based on our own research and recent developments in this field. The role of vacuolar processing enzymes in plant immunity Role of VPE in PCDPlant vacuoles play fundamental roles in controlling turgor pressure, molecular degradation and storage, as well as timely execution of PCD in, e.g., plant disease resistance, tissue senescence and seed development. 10,11 A ...

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A Plant Vacuolar Protease, VPE, Mediates Virus-Induced Hypersensitive Cell Death

Cited by 569 publications

References 26 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

Autophagic Components Contribute to Hypersensitive Cell Death in Arabidopsis

The role of vacuolar processing enzymes in plant immunity

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