Vacuolar processing enzyme activates programmed cell death in the apical meristem inducing loss of apical dominance

Teper‐Bamnolker, Paula; Buskila, Yossi; Belausov, Eduard; Wolf, Dalia; Doron‐Faigenboim, Adi; Ben‐Dor, Shifra; Hoorn, Renier A. L. van der; Lers, Amnon; Eshel, Dani

doi:10.1111/pce.13044

Cited by 26 publications

(23 citation statements)

References 52 publications

(109 reference statements)

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“…Following the stress, induction of StVPE1 in the stem meristem induces loss of apical dominance and stem branching. The mature StVPE1 protein exhibits specific activity for caspase-1, with optimal activity at acidic pH, consistent with its established vacuolar localization (Teper-Bamnolker et al, 2017). Downregulation of St VPE1 by RNA interference (RNAi) or overexpression of green fluorescent protein-labeled StVPE1 ( StVPE1-GFP ) results in reduced or enhanced stem branching, respectively (Teper-Bamnolker et al, 2017).…”

Section: Introductionsupporting

confidence: 54%

“…VPE is considered a PCD executor in plant systems in response to several biotic and abiotic stresses (reviewed by Hatsugai et al, 2015; Vorster et al, 2019). Phylogenetic analysis has shown that StVPE1, classified as a vegetative-type VPE, has high sequence similarity and conserved regions with tobacco NtVPE-1a , NtVPE-1b , NtVPE-2 and NtVPE-3 (Teper-Bamnolker et al, 2017; Supplementary data 1A). To study its role in PCD induction, VPE-RNAi-expressing BY-2 lines were produced, and their PCD response was compared to that in wild-type (WT) cells.…”

Section: Resultsmentioning

confidence: 99%

“…The VPE-dependent PCD pathway has been shown to be involved not only in immune responses, but also in responses to a variety of stress inducers (reviewed by Hatsugai et al, 2015). We have previously shown the involvement of StVPE1⁊ in PCD induced by cold incubation or chemical stress under dark conditions (Teper-Bamnolker et al, 2012; Teper-Bamnolker et al, 2017). Here, carbon starvation of BY-2 cells for short periods, 24 h and 48 h, was shown to induce VPE expression and activity, respectively, accompanied by gradual PCD of the cell population (Figures 2 and 3).…”

Section: Discussionmentioning

confidence: 99%

“…Potato ( Solanum tuberosum L.) cv. Désirée and transgenic potato plants expressing StVPE1-GFP (Teper-Bamnolker et al, 2017) were grown on Nitsch’s medium (Nitsch and Nitsch, 1969) supplemented with 2% (w/v) sucrose and 50 mg mL -1 kanamycin. Plants were grown under a 16 h light/8 h dark cycle (long day) at 25°C in a growth chamber.…”

Section: Methodsmentioning

confidence: 99%

“…Potato ( Solanum tuberosum ) VPE1 (StVPE1) has been shown to be involved in the PCD response of the stem apical meristem to abiotic stress (Teper-Bamnolker et al, 2012; Teper-Bamnolker et al, 2017). Following the stress, induction of StVPE1 in the stem meristem induces loss of apical dominance and stem branching.…”

Section: Introductionmentioning

confidence: 99%

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

Teper‐Bamnolker

Danieli

Peled-Zehavi

et al. 2019

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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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Section: Introductionsupporting

confidence: 54%