A novel mechanism of aluminium-induced cell death involving vacuolar processing enzyme and vacuolar collapse in tobacco cell line BY-2

Kariya, Koki; Demiral, Tijen; Sasaki, Takayuki; Tsuchiya, Yoshiyuki; Türkan, İsmail; Sano, Takeshi; Hasezawa, Seiichiro; Yamamoto, Yoko

doi:10.1016/j.jinorgbio.2013.07.001

Cited by 38 publications

(28 citation statements)

References 34 publications

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“…The rupture of the vacuole and the subsequent release of various types of enzymes indicate that plant PCD has been initiated18. Furthermore, vacuolar collapse results in the loss of plasma membrane integrity and eventually leads to cell death1920. It was suggested that the collapse of the large central vacuole is a crucial event in the PCD of plant cells, and vacuole-induced cell death is unique to plant cells21.…”

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confidence: 99%

The relationship between vacuolation and initiation of PCD in rice (Oryza sativa) aleurone cells

Zheng

Zhang

Deng

et al. 2017

Sci Rep

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Vacuole fusion is a necessary process for the establishment of a large central vacuole, which is the central location of various hydrolytic enzymes and other factors involved in death at the beginning of plant programmed cell death (PCD). In our report, the fusion of vacuoles has been presented in two ways: i) small vacuoles coalesce to form larger vacuoles through membrane fusion, and ii) larger vacuoles combine with small vacuoles when small vacuoles embed into larger vacuoles. Regardless of how fusion occurs, a large central vacuole is formed in rice (Oryza sativa) aleurone cells. Along with the development of vacuolation, the rupture of the large central vacuole leads to the loss of the intact plasma membrane and the degradation of the nucleus, resulting in cell death. Stabilizing or disrupting the structure of actin filaments (AFs) inhibits or promotes the fusion of vacuoles, which delays or induces PCD. In addition, the inhibitors of the vacuolar processing enzyme (VPE) and cathepsin B (CathB) block the occurrence of the large central vacuole and delay the progression of PCD in rice aleurone layers. Overall, our findings provide further evidence for the rupture of the large central vacuole triggering the PCD in aleruone layers.

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confidence: 99%

The relationship between vacuolation and initiation of PCD in rice (Oryza sativa) aleurone cells

Zheng

Zhang

Deng

et al. 2017

Sci Rep

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“…After a stress treatment at 4°C, autophagosome formation was visible in microspores along with PCD, and treatment with autophagy inhibitors decreased microspore cell death (Bárány et al, 2018). Vacuolar cell death through VPE in BY-2 cells treated with aluminum has been reported (Kariya et al, 2013; Kariya et al, 2018). Vacuolar cell death accompanied by autophagic activity involving the formation of lytic lysosome-like structures has also been described in BY-2 cells treated with cadmium or chemicals, and in response to sucrose starvation (Kutik et al, 2014; Iakimova et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Vacuolar processing enzyme translocates to the vacuole through the autophagy pathway to induce programmed cell death

Teper‐Bamnolker

Danieli

Peled-Zehavi

et al. 2019

Preprint

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One sentence summary: Carbon starvation induced programmed cell death 26 by trafficking vacuolar processing enzyme through the autophagy pathway to 27 the vacuole. 28 29The author responsible for distribution of materials integral to the findings 30 presented in this article in accordance with the policy described in the 31 Instructions for Authors (www.plantcell.org) is: Dani Eshel (dani@agri.gov.il). 32 33 34 2 35 Abstract 36 37 The caspase-like vacuolar processing enzyme (VPE) is a key factor in 38 programmed cell death (PCD) associated with plant stress responses. Growth 39 medium lacking a carbon source and dark conditions caused punctate labeling 40 of 35S::VPE1-GFP (StVPE1-GFP) in potato leaves. Carbon starvation of BY-2 41 cells induced higher VPE activity and PCD symptoms. Growing VPE-RNAi BY-42 2 cells without sucrose reduced VPE activity and prevented PCD symptoms. 43 During extended exposure to carbon starvation, VPE expression and activity 44 levels peaked, with a gradual increase in BY-2 cell death. Histological analysis 45 of StVPE1-GFP in BY-2 cells showed that carbon starvation induces its 46 translocation from the endoplasmic reticulum to the central vacuole, through 47 tonoplast engulfment. Exposure of BY-2 culture to the autophagy inhibitor 48 concanamycin A caused autophagic bodies accumulation in the cell vacuole. 49 Such accumulation did not occur in the presence of 3-methyladenine, an 50 inhibitor of early-stage autophagy. BY-2 cells constitutively expressing 51 StATG8IL-RFP, an autophagosome marker, showed colocalization with the 52 StVPE1-GFP protein in the cytoplasm and vacuole. RNAi silencing of the core 53 autophagy component ATG4 in BY-2 cells reduced VPE activity and cell death. 54 These results are the first to suggest that VPE translocates to the cell vacuole 55 through the autophagy pathway, leading to PCD. 56 endopeptidase activity, unlike caspases that cleave their substrates at aspartic 91 acid residues (Silva et al., 2005; Van Durme and Nowack, 2016). The VPE 92 proteins belong to a family of cysteine proteinases that are well conserved 93 among a variety of organisms, including many plant and animal species (Cai 94 and Gallois, 2015; Hatsugai et al., 2015; Sueldo and van der Hoorn, 2017). 95 VPEs were originally found to be responsible for the maturation of seed 96 storage proteins and various other vacuolar proteins in plants (Hara-Nishimura 97 et al., 1991; Hara-Nishimura et al., 1993; Hatsugai et al., 2004). VPE, which is 98 released into the vacuole during PCD, triggers the degradation of other 99 proteins (Hara-Nishimura et al., 2005; Kuroyanagi et al., 2005; Van Durme and 100 Nowack, 2016). VPEs, which exhibit caspase-1-like activity, play important 101 roles in plant PCD, be it developmental or in response to biotic or abiotic stress 102 (reviewed by Hatsugai et al., 2015; Vorster et al., 2019). Specifically, VPE has 103 been characterized as a major factor in the HR. By silencing the gene 104 encoding VPE, Hatsugai et al. (2004) showed that vacuolar collapse, caused ...

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“…These proteins and enzymes are directly or indirectly involved in the regulation of plant defense. For example, vacuolar processing enzyme (VPE), (c49130_g1) which was up-regulated in AM vs AC and AF vs AC, may be a cysteine protease responsible for caspase -1 activity and promote programmed cell death (PCD) by disrupting the vacuole in pathogenesis like in tobacco 24 . It may positively regulate HR cell death mediated by NB-LRR recognition of the invading pathogen like metacaspase-1 in a variety of plants 25 .…”

Section: Discussionmentioning

confidence: 99%

Response of peanut Arachis hypogaea roots to the presence of beneficial and pathogenic fungi by transcriptome analysis

Hao

Wang

Nong

et al. 2017

Sci Rep

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Entomopathogenic fungus Metarhizium anisopliae obtain survival benefit meanwhile promote the nutrient absorption of root as an endophyte. However, little is known concerning molecular mechanisms in the process. We performed the transcriptome sequencing of A. hypogaea roots inoculated M. anisopliae and pathogenic Fusarium axysporum, respectively. There were 81323 unigenes from 132023 transcripts. Total 203 differentially expressed genes (DEGs) respond to the two fungi, including specific 76 and 34 DEGs distributed respectively in M. anisopliae and F. axysporum treatment. KEGG pathway enrichment for DEGs showed the two top2 were signal transductions of plant-pathogen interaction and plant hormone. By qRT-PCR, the mRNA level of 26 genes involved in plant-fungus interaction confirmed the reliability of the RNA-Seq data. The expression pattern of the key DEGs on jasmonic acid (JA) or salicylic acid (SA) signaling pathway presented regulating consistency with JA or SA concentration detected by HPLC-MS. Those significantly stronger down-regulated DEGs by M. anisopliae thanby F. axysporum linking to hypersensitive response and negative regulation of defense, and those specific up-regulated genes in M. anisopliae treatment may predict that the less immunity is conducive to symbiosis F. axysporum may trigger JA-mediated defense regulated by ERF branch of JA signaling pathway, whereas M. anisopliae does not.

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A novel mechanism of aluminium-induced cell death involving vacuolar processing enzyme and vacuolar collapse in tobacco cell line BY-2

Cited by 38 publications

References 34 publications

The relationship between vacuolation and initiation of PCD in rice (Oryza sativa) aleurone cells

The relationship between vacuolation and initiation of PCD in rice (Oryza sativa) aleurone cells

Vacuolar processing enzyme translocates to the vacuole through the autophagy pathway to induce programmed cell death

Response of peanut Arachis hypogaea roots to the presence of beneficial and pathogenic fungi by transcriptome analysis

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