Autophagy is activated and involved in cell death with participation of cathepsins during stress-induced microspore embryogenesis in barley

Bárány, Ivett; Berenguer, Eduardo; Solís, María-Teresa; Pérez-Pérez, Yolanda; Santamaría, M. Estrella; Crespo, José L.; Risueño, María Carmen; Dı́az, Isabel; Testillano, Pilar S.

doi:10.1093/jxb/erx455

Cited by 62 publications

(53 citation statements)

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“…In a recent report, together with ROS production, we have demonstrated activation of autophagy after the inductive stress of microspore embryogenesis in barley. 20 Interestingly, key autophagy genes, particularly HvATG5 and HvATG6, were upregulated in microspore cultures after the stress treatment to induce embryogenesis. 20 Our results showed that barley stress-treated microspores showed an increase in the presence of autophagosomes and autophagic bodies, which exhibited specific immunofluorescence labeling with antibodies against ATG5 20 and ATG8 29,30 (provided by M.F.…”

Section: Stress-induced Microspore Cell Death Is Accompanied By Ros Pmentioning

confidence: 97%

“…Previous reports that analyzed the possible role of certain cell death-related proteases in the stress response of the microspores have revealed that cathepsin L/F-, B-and H-like activities were induced after stress; concomitantly, cathepsin-like genes HvPap-1 and HvPap-6 were up-regulated. 20 The use of specific antibodies against HvPap-1 and HvPap-6 cysteine-proteases in western and immunofluorescence assays has shown not only that cathepsin gene expression and enzymatic activity increased but also that the proteins increased in microspores after the stress. 20 Our results using anti-HvPap-1 20 antibodies (provided by I. Díaz, CBGP-UAM, Montegancedo, Spain) in immunofluorescence assays analyzed by confocal microscopy, showed that cathepsins increased in stress-treated microspores and localized in small cytoplasmic rounded areas ( Figure 3G, H activity was also analyzed in microspore cultures and results showed similar kinetics to that of C1 cysteine proteases, with a marked increase in proteolytic activity after the stress treatment to induce embryogenesis.…”

Section: Stress-induced Microspore Cell Death Is Accompanied By Ros Pmentioning

confidence: 99%

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Modulation of autophagy and protease activities by small bioactive compounds to reduce cell death and improve stress-induced microspore embryogenesis initiation in rapeseed and barley

Pérez-Pérez¹,

Bárány²,

Berenguer³

et al. 2018

Plant Signaling & Behavior

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Microspore embryogenesis is a powerful biotechnological tool that is very useful in crop breeding for the rapid production of haploid and double-haploid embryos and plants. In this in vitro system, the haploid microspore is reprogrammed by the application of specific stress treatments. A high level of cell death after the stress is a major factor that greatly reduces embryogenesis yield at its initial stages. Autophagy is a degradation pathway that is present in all eukaryotes and plays key roles in a range of processes, including stress responses. Many proteases participate in autophagy and cell death; among them, cathepsins are the most abundant enzymes with a role in plant senescence and programmed cell death (PCD). Moreover, although plant genomes do not contain homologues of caspases, caspase 3-like activity (main executioner protease of animal cell death) has been detected in many plant PCD processes. Recent studies by our group in barley microspore cultures reported that the stress treatment required for inducing microspore embryogenesis (cold treatment), also produced reactive oxygen species (ROS) and cell death, concomitantly with the induction of autophagy, as well as cathepsin-like and caspase 3-like proteolytic activities. In the present study, we report new data on microspore embryogenesis of rapeseed that indicate, as in barley, activation of cell death and autophagy processes after the inductive stress. The results revealed that treatments modulating autophagy and proteases produced the same effect in the two plant systems, regardless of the stress applied, cold in barley or heat in rapeseed. Pharmacological treatments with small bioactive compounds that inhibit ROS, autophagy and specific cell death-proteases led to reduced cell death and an increased embryogenesis initiation rate in both, barley and rapeseed. Taken together, these findings open up new intervention pathways by modulating autophagy and proteases, which are very promising in terms of increasing the efficiency of in vitro microspore embryogenesis systems for biotechnological applications in crop breeding.

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Section: Stress-induced Microspore Cell Death Is Accompanied By Ros Pmentioning

confidence: 97%

Section: Stress-induced Microspore Cell Death Is Accompanied By Ros Pmentioning

confidence: 99%

Modulation of autophagy and protease activities by small bioactive compounds to reduce cell death and improve stress-induced microspore embryogenesis initiation in rapeseed and barley

Pérez-Pérez¹,

Bárány²,

Berenguer³

et al. 2018

Plant Signaling & Behavior

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“…In addition, it has been recently suggested that the autophagy pathway might promote PCD during microspore embryogenesis in barley. 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).…”

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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“…Moreover, autophagic cell death, which is regarded as one of the major PCD types, has been well studied in animals, including in C. elegans and D. melanogaster (Martin et al , ; Samara et al , ; Mariño et al , ). In plants, PCD and autophagy are usually found simultaneously in various cellular responses, like pathogen‐induced hypersensitive response (Xu et al , ), leaf senescence (Ono et al , ), xylem fiber development (Courtois‐Moreau et al , ) and microspore embryogenesis (Bárány et al , ). Additionally, emerging evidence suggests that autophagy is involved in the regulation of PCD during plant sexual reproduction (Minina et al , ; Xu et al , ).…”

Section: The Roles Of Autophagy In Key Processes Of Plant Reproductionmentioning

confidence: 99%

“…Nevertheless, autophagy and PCD are often considered as two disconnected events in plant reproduction. Recently, potential crosstalk between autophagy and PCD in plant sexual reproduction has often been speculated and discussed, although the detailed working mechanisms have not been well explored (Minina et al , ; Bárány et al , ).…”

Section: Introductionmentioning

confidence: 99%

Boosting autophagy in sexual reproduction: a plant perspective

Mei

et al. 2020

New Phytologist

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Summary The key process of sexual reproduction is the successful fusion of the sperm and egg cell. Distinct from dynamic and flagellated animal sperm cells, higher flowering plant sperm cells are immotile. Therefore, plants have evolved a novel reproductive system to achieve fertilization and generate progenies. Plant sexual reproduction consists of multiple steps, mainly including gametophyte development, pollen–pistil recognition, pollen germination, double fertilization and postfertilization. During reproduction, active production, consumption and recycling of cellular components and energy are critically required to achieve fertilization. However, the underlying machinery of cellular degradation and turnover remains largely unexplored. Autophagy, the major catabolic pathway in eukaryotic cells, participates in regulating multiple aspects of plant activities, including abiotic and biotic stress resistance, pathogen response, senescence, nutrient remobilization and plant development. Nevertheless, a key unanswered question is how autophagy regulates plant fertilization and reproduction. Here, we focus on comparing and contrasting autophagy in several key reproductive processes of plant and animal systems to feature important distinctions and highlight future research directions of autophagy in angiosperm reproduction. We further discuss the potential crosstalk between autophagy and programmed cell death, which are often considered as two disconnected events in plant sexual reproduction.

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Autophagy is activated and involved in cell death with participation of cathepsins during stress-induced microspore embryogenesis in barley

Abstract: Autophagy is activated and plays a role in stress-induced cell death during microspore embryogenesis, along with cathepsin-like C1A protease activities. Autophagy inhibition reduces cell death, improving embryogenesis induction efficiency.

Cited by 62 publications

References 65 publications

Modulation of autophagy and protease activities by small bioactive compounds to reduce cell death and improve stress-induced microspore embryogenesis initiation in rapeseed and barley

Modulation of autophagy and protease activities by small bioactive compounds to reduce cell death and improve stress-induced microspore embryogenesis initiation in rapeseed and barley

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

Boosting autophagy in sexual reproduction: a plant perspective

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