The Fatal Effect Of Tungsten On Pisum Sativum L. Root Cells: Indications For Endoplasmic Reticulum Stress-induced Programmed Cell Death
I. Adamakis, E. Panteris, E. Eleftheriou
Published 2011 · Medicine, Biology
Download PDFAnalyze on Scholarcy
Programmed cell death (PCD) is a widespread response of plants against abiotic stress, such as heavy metal toxicity. Tungsten (W) is increasingly considered toxic for plants since it irreversibly affects their growth. Therefore, we investigated whether W could induce some kind of PCD in plants, like other heavy metals do. The morphology of cell and nucleus, the integrity of the cytoskeleton, Evans Blue absorbance and the expression of PCD-related genes were used as indicators of PCD in W-treated roots of Pisum sativum (pea). TEM and fluorescence microscopy revealed mitotic cycle arrest, protoplast shrinkage, disruption of the cytoskeleton and chromatin condensation and peripheral distribution in the nucleus of W-affected cells. Moreover, Evans Blue absorbance in roots increased in relation to the duration of W treatment. These effects were suppressed by inhibitors of the 26S proteasome, caspases and endoplasmic reticulum stress. In addition, silencing of DAD-1 and induction of HSR203J, BiP-D, bZIP28 and bZIP60 genes were also recorded in W-treated pea roots by semi-quantitative RT-PCR. The above observations show that W induces a kind of PCD in pea roots, further substantiating its toxicity for plants. Data imply that endoplasmic reticulum stress-unfolded protein response may be involved in W-induced PCD.
This paper references
Effects of sodium tungstate on the ultrastructure and growth of pea (Pisum sativum) and cotton (Gossypium hirsutum) seedlings
I. Adamakis (2008)
Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings
Jie Xiong (2009)
Arsenate toxicity on the apices of Pisum sativum L. seedling roots: Effects on mitotic activity, chromatin integrity and microtubules
Stefania Dho (2010)
What happened to plant caspases?
L. Bonneau (2008)
A novel membrane fusion-mediated plant immunity against bacterial pathogens.
N. Hatsugai (2009)
A homolog of the defender against apoptotic death gene (DAD1) in senescing gladiolus petals is down-regulated prior to the onset of programmed cell death.
Tetsuya Yamada (2004)
Effects of Sodium
The Caspase-like Sites of Proteasomes, Their Substrate Specificity, New Inhibitors and Substrates, and Allosteric Interactions with the Trypsin-like Sites*
A. Kisselev (2003)
Tudor staphylococcal nuclease
JF Sundström (2009)
Programmed cell death remodels lace plant leaf shape during development
AHLAN Gunawardena (2004)
Arabidopsis bZIP60 Is a Proteolysis-Activated Transcription Factor Involved in the Endoplasmic Reticulum Stress Response[W]
Y. Iwata (2008)
The Phosphorylation State and Expression of Soybean BiP Isoforms Are Differentially Regulated following Abiotic Stresses*
J. C. Cascardo (2000)
Cellular response to endoplasmic reticulum stress: a matter of life or death
M. Boyce (2006)
Genetic Studies of a Cluster of Acute Lymphoblastic Leukemia Cases in Churchill County, Nevada
K. Steinberg (2007)
Aluminum-induced cell death of barley-root border cells is correlated with peroxidase- and oxalate oxidase-mediated hydrogen peroxide production
L. Tamás (2005)
Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome
J. Sundström (2009)
Environmentally induced programmed cell death in leaf protoplasts of Aponogeton madagascariensis
Christina E. N. Lord (2011)
Cell Death in Plant Disease
D. Pontier (2004)
Cell death in plant disease : mechanisms and molecular markers
Glycosylation of phytepsin and expression of dad1, dad2 and ost1 during onset of cell death in germinating barley scutella
P. Lindholm (2000)
Initiation of programmed cell death in self-incompatibility: role for cytoskeleton modifications and several caspase-like activities.
Maurice Bosch (2008)
Programmed Cell Death Remodels Lace Plant Leaf Shape during Development Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016188.
A. Gunawardena (2004)
Cell Identity Mediates the Response of Arabidopsis Roots to Abiotic Stress
J. Dinneny (2008)
Plant cell death processes
L. Noodén (2004)
Identification of an Arabidopsis transmembrane bZIP transcription factor involved in the endoplasmic reticulum stress response.
H. Tajima (2008)
The phosphorylation state and expression
EP Fontes (2000)
An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis.
Y. Duan (2010)
The plant homologue of the defender against apoptotic death gene is down‐regulated during senescence of flower petals 1
D. Orzáez (1997)
Microtubules Are a Target for Self-Incompatibility Signaling in Papaver Pollen1
N. S. Poulter (2008)
An Endoplasmic Reticulum Stress Response in Arabidopsis Is Mediated by Proteolytic Processing and Nuclear Relocation of a Membrane-Associated Transcription Factor, bZIP28[W][OA]
J. Liu (2007)
Cortical actin filament organization in developing and functioning stomatal complexes of Zea mays and Triticum turgidum.
E. Panteris (2007)
Activation of caspase-like proteases and induction of apoptosis by isopentenyladenosine in tobacco BY-2 cells
P. Mlejnek (2002)
Programmed cell death of the megagametophyte during post-germinative growth of white spruce (Picea glauca) seeds is regulated by reactive oxygen species and the ubiquitin-mediated proteolytic system.
X. He (2010)
Tungsten affects the cortical microtubules of Pisum sativum root cells: experiments on tungsten-molybdenum antagonism.
I-D S Adamakis (2010)
Ultraviolet-C Overexposure Induces Programmed Cell Death in Arabidopsis, Which Is Mediated by Caspase-like Activities and Which Can Be Suppressed by Caspase Inhibitors, p35 and Defender against Apoptotic Death*
A. Danon (2004)
Cytoskeletal alterations in interphase cells of the green alga Spirogyra decimina in response to heavy metals exposure: II. The effect of aluminium, nickel and copper.
P. Přibyl (2008)
dad-1, A putative programmed cell death suppressor gene in rice.
Y. Tanaka (1997)
Devil inside: does plant programmed cell death involve the endomembrane system?
Jean-Luc Cacas (2010)
Expression of defender against apoptotic death (DAD-1) in Iris and Dianthus petals
D. V. D. Kop (2003)
Cellular response to endoplasmic reticulum
M Boyce (2006)
Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana
D. Lu (2008)
Analysis of ER stress in developing rice endosperm accumulating beta-amyloid peptide.
Youko Oono (2010)
Expression of an evolutionarily distinct novel BiP gene during the unfolded protein response in Arabidopsis thaliana.
S. Noh (2003)
Possible involvement of MAP kinase pathways in acquired metal-tolerance induced by heat in plants
P Chen (2008)
Sodium tungstate ( Na 2 WO 4 ) exposure increases apoptosis in human peripheral blood lymphocytes
JW Pan (2001)
A transient proteasome activation is needed for acetic acid-induced programmed cell death to occur in Saccharomyces cerevisiae.
D. Valenti (2008)
ER stress and the unfolded protein response.
M. Schröder (2005)
The cortical microtubules are a universal target of tungsten toxicity among land plant taxa.
I. Adamakis (2010)
AN EXPERIMENT IN MEDICAL PEDAGOGY.
E. R. Le Count
Unfolded protein response followed by induction of cell death in cultured tobacco cells treated with tunicamycin
Y. Iwata (2004)
Endoplasmic reticulum stress-induced programmed cell death in soybean cells
Anna Zuppini (2004)
Die and let live - programmed cell death in plants.
E. Lam (1999)
Death by proteases in plants: Whodunit
V. Rotari (2005)
An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants.
Y. Iwata (2005)
Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis
Y. Liao (2008)
Sodium tungstate (Na2WO4) exposure increases apoptosis in human peripheral blood lymphocytes
A. Osterburg (2010)
during the unfolded protein response in Arabidopsis thaliana
Y Oono (2010)
BAX Inhibitor-1 Modulates Endoplasmic Reticulum Stress-mediated Programmed Cell Death in Arabidopsis*
N. Watanabe (2008)
Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death.
D. Pontier (1998)
Programmed cell death in plants: distinguishing between different modes.
Theresa J. Reape (2008)
Erratum to: Environmentally induced programmed cell death in leaf protoplasts of Aponogeton madagascariensis
Christina E. N. Lord (2010)
Metacaspase-dependent programmed cell death is essential for plant embryogenesis
M. F. Suárez (2004)
Colchicine-induced Paracrystals in Root Cells of Wheat (Triticum aestivum L.)
Th. Karagiannidou (1995)
Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana
Shinya Kamauchi (2005)
Environmental fate of tungsten from military use.
J. Clausen (2009)
Functional specification of Arabidopsis isopropylmalate isomerases in glucosinolate and leucine biosynthesis.
Y. He (2010)
Cytoskeletal alterations in interphase cells of the green alga Spirogyra decimina in response to heavy metals exposure: I. The effect of cadmium
P. Přibyl (2005)
A review of tungsten: from environmental obscurity to scrutiny.
A. Koutsospyros (2006)
Temporal and spatial activation of caspase-like enzymes induced by self-incompatibility in Papaver pollen
Maurice Bosch (2007)
Aluminum-induced cell death in root-tip cells of barley.
J. Pan (2001)
Temporal and spatial activation
M Bosch (2007)
The endoplasmic reticulum stress signaling pathways in plants
R. Urade (2009)
Constitutive caspase-like machinery executes programmed cell death in plant cells
M. Elbaz (2002)
Apoptosis and the proteasome.
L. Grimm (1999)
Phenylbutyric Acid Rescues Endoplasmic Reticulum Stress-Induced Suppression of APP Proteolysis and Prevents Apoptosis in Neuronal Cells
J. Wiley (2010)
Cadmium toxicity in cultured tomato cells—Role of ethylene, proteases and oxidative stress in cell death signaling
E. Iakimova (2008)
Cellular response to unfolded proteins in the endoplasmic reticulum of plants
R. Urade (2007)
AR Osterburg (2010)
Cell cycle phase-specific death response of tobacco BY-2 cell line to cadmium treatment.
Andrea Kuthanová (2008)
Proteasome function is required for activation of programmed cell death in heat shocked tobacco Bright‐Yellow 2 cells
R. A. Vacca (2007)
Activation of the Programmed Cell Death Pathway by Inhibition of Proteasome Function in Plants*
M. Kim (2003)
Study of Defense-related Gene Expression in Grapevine Leaves and Berries Infected with Botrytis cinerea
A. Bézier (2004)
Bio-availability of tungsten in the vicinity of an abandoned mine in the English Lake District and some potential health implications.
B. Wilson (2006)
This paper is referenced by
Seed birth to death: dual functions of reactive oxygen species in seed physiology.
S. J. Jeevan Kumar (2015)
Structural Evidence of Programmed Cell Death Induction by Tungsten in Root Tip Cells of Pisum sativum
I. Adamakis (2019)
Effects of bisphenol A on the microtubule arrays in root meristematic cells of Pisum sativum L.
I. Adamakis (2013)
Early generation of nitric oxide contributes to copper tolerance through reducing oxidative stress and cell death in hulless barley roots
Yanfeng Hu (2016)
Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research?
J. Xiong (2012)
Chromium-Induced Ultrastructural Changes and Oxidative Stress in Roots of Arabidopsis thaliana.
E. Eleftheriou (2015)
Chromium-Induced Ultrastructural Changes and Oxidative Stress in Roots of Arabidopsis thaliana
Eleftherios P. Eleftheriou (2015)
ROS-mediated abiotic stress-induced programmed cell death in plants
V. Petrov (2015)
The mystery of underground death: cell death in roots during ontogeny and in response to environmental factors.
Agnieszka Bagniewska-Zadworna (2016)
Bisphenol A disrupts microtubules and induces multipolar spindles in dividing root tip cells of the gymnosperm Abies cephalonica.
I. Adamakis (2016)
Transcriptome-Wide Mapping of Pea Seed Ageing Reveals a Pivotal Role for Genes Related to Oxidative Stress and Programmed Cell Death
H. Chen (2013)
Copper treatment of peach leaves causes lesion formation similar to the biotic stress response.
Fumiyuki Goto (2019)
Aberration of mitosis by hexavalent chromium in some Fabaceae members is mediated by species-specific microtubule disruption
Eleftherios P. Eleftheriou (2015)
Hop/Sti1 – A Two-Faced Cochaperone Involved in Pattern Recognition Receptor Maturation and Viral Infection
Christian E. Lamm (2017)
Influence of Increasing Tungsten Concentrations and Soil Characteristics on Plant Uptake: Greenhouse Experiments with Zea mays
Gianniantonio Petruzzelli (2019)
Responses of Plant Proteins to Heavy Metal Stress—A Review
M. K. Hasan (2017)
Comparison of antioxidant enzyme activities and DNA damage in chickpea (Cicer arietinum L.) genotypes exposed to vanadium
M. Imtiaz (2016)
Tungsten disrupts root growth in Arabidopsis thaliana by PIN targeting.
Ioannis-Dimosthenis S. Adamakis (2014)
Hexavalent chromium-induced differential disruption of cortical microtubules in some Fabaceae species is correlated with acetylation of α-tubulin
Eleftherios P. Eleftheriou (2015)
Endoplasmic Reticulum Stress Response in Arabidopsis Roots
Yueh Cho (2017)
Concentration-dependent effects of tungstate on germination, growth, lignification-related enzymes, antioxidants, and reactive oxygen species in broccoli (Brassica oleracea var. italica L.)
Mona F. A. Dawood (2019)
Tungsten Toxicity in Plants
I. Adamakis (2012)
Reactive Oxygen Species Signaling and Seed Germination
Prabhakaran Soundararajan (2017)
Silver nanoparticle toxicity effect on the seagrass Halophila stipulacea.
Zoi Mylona (2019)
The role of ion disequilibrium in induction of root cell death and autophagy by environmental stresses.
Vadim Demidchik (2018)
Involvement of plant cytoskeleton in cellular mechanisms of metal toxicity
I. Horiunova (2016)
Ethylene modulates root cortical senescence in barley
Hannah M. Schneider (2018)
Effect of tungstate on pea root growth and protein tyrosine phosphorylation
N. I. Gazizova (2013)
The nitrate reductase inhibitor, tungsten, disrupts actin microfilaments in Zea mays L.
Ioannis-Dimosthenis S. Adamakis (2013)
Elemental composition of Marrubium astracanicum Jacq. growing in tungsten-contaminated sites
Gürcan Güleryüz (2016)
The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants.
Omar Arias Gaguancela (2016)
Effect of tungsten on growth, biochemical constituents, molybdenum and tungsten contents in wheat
A Naresh Kumar (2018)See more