Online citations, reference lists, and bibliographies.
← Back to Search

Ozone-Induced Cell Death In Tobacco Cultivar Bel W3 Plants. The Role Of Programmed Cell Death In Lesion Formation

S. Pasqualini, C. Piccioni, L. Reale, L. Ederli, G. Della Torre, F. Ferranti
Published 2003 · Biology, Medicine

Cite This
Download PDF
Analyze on Scholarcy
Share
Treatment of the ozone-sensitive tobacco (Nicotiana tabacum L. cv Bel W3) with an ozone pulse (150 nL L–1 for 5 h) induced visible injury, which manifested 48 to 72 h from onset of ozone fumigation. The “classical” ozone symptoms in tobacco cv Bel W3 plants occur as sharply defined, dot-like lesions on the adaxial side of the leaf and result from the death of groups of palisade cells. We investigated whether this reaction had the features of a hypersensitive response like that which results from the incompatible plant-pathogen interaction. We detected an oxidative burst, the result of H2O2 accumulation at 12 h from the starting of fumigation. Ozone treatment induced deposition of autofluorescent compounds and callose 24 h from the start of treatment. Total phenolic content was also strongly stimulated at the 10th and 72nd h from starting fumigation, concomitant with an enhancement in phenylalanine ammonia-lyase a and phenylalanine ammonia-lyase b expression, as evaluated by reverse transcriptase-polymerase chain reaction. There was also a marked, but transient, increase in the mRNA level of pathogenesis-related-1a, a typical hypersensitive response marker. Overall, these results are evidence that ozone triggers a hypersensitive response in tobacco cv Bel W3 plants. We adopted four criteria for detecting programmed cell death in ozonated tobacco cv Bel W3 leaves: (a) early release of cytochrome c from mitochondria; (b) activation of protease; (c) DNA fragmentation by terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling of DNA 3′-OH groups; and (d) ultrastructural changes characteristic of programmed cell death, including chromatin condensation and blebbing of plasma membrane. We, therefore, provide evidence that ozone-induced oxidative stress triggers a cell death program in tobacco cv Bel W3.
This paper references
10.1146/ANNUREV.ARPLANT.48.1.251
THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.
C. Lamb (1997)
10.1104/PP.123.2.487
Ozone sensitivity in hybrid poplar correlates with insensitivity to both salicylic acid and jasmonic acid. The role of programmed cell death in lesion formation.
J. R. Koch (2000)
10.1016/0031-9422(88)80254-1
The antioxidants of higher plants
R. Larson (1988)
10.1046/J.1365-3040.2002.00859.X
Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone
H. Wohlgemuth (2002)
10.1007/s004250100654
A critical role for ethylene in hydrogen peroxide release during programmed cell death in tomato suspension cells
Anke J. de Jong (2001)
10.1016/S1360-1385(00)01570-3
Programmed cell death and aerenchyma formation in roots.
M. Drew (2000)
Biochem - ical plant responses to ozone : III . Activation of the defencerelated proteins 1 , 3glucanase and chitinase in tobacco
M Schraudner (1992)
10.1201/9781420049299
Pathogenesis-related proteins in plants.
J. Rigden (1988)
10.1046/J.1365-313X.1997.11020203.X
Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury.
B. L. Orvar (1997)
Biochemical basis for the toxicity of ozone
J. Mudd (1996)
10.1104/PP.99.4.1321
Biochemical Plant Responses to Ozone : III. Activation of the Defense-Related Proteins beta-1,3-Glucanase and Chitinase in Tobacco Leaves.
M. Schraudner (1992)
10.1016/S1360-1385(97)01030-3
Salicylate, superoxide synthesis and cell suicide in plant defence
J. Draper (1997)
10.1016/0005-2728(73)90255-7
The external NADH dehydrogenases of intact plant mitochondria.
R. Douce (1973)
10.1105/tpc.8.3.393
Cleavage of Nuclear DNA into Oligonucleosomal Fragments during Cell Death Induced by Fungal Infection or by Abiotic Treatments.
D. Ryerson (1996)
10.1146/ANNUREV.PHYTO.36.1.393
Programmed cell death in plant disease: the purpose and promise of cellular suicide.
D. Gilchrist (1998)
10.1042/BST0240456
Plant defence systems and ozone.
M. Schraudner (1996)
10.1016/S1360-1385(97)85222-3
Sugar import and metabolism during seed development
H. Weber (1997)
10.1016/0076-6879(90)82018-W
Isolation of subcellular organelles.
B. Storrie (1990)
10.1016/S0981-9428(00)01192-X
Activities of nucleases in senescing daylily petals.
Tadas Panavas (2000)
10.1201/9781420049299
Pathogenesis-related proteins in plants
U. Pfitzner (1999)
10.1016/S1369-5266(00)00216-8
Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues.
E. Beers (2001)
The involvement of cysteine protease inhibitor genes in the regulation of programmed cell death in plants
M Solomon (1999)
Programmed cell death and aeren - chyma formation in roots
MC Drew (2000)
10.1016/S0091-679X(08)61922-6
Identification of dying cells--in situ staining.
S. Ben-Sasson (1995)
10.1038/34112
A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD
M. Enari (1998)
10.1023/A:1026588408152
Programmed cell death during endosperm development
T. E. Young (2004)
10.1016/S0031-9422(00)97805-1
Polyamines as radical scavengers and protectants against ozone damage
W. Bors (1989)
10.1016/0269-7491(91)90076-9
Origin of Bel-W3, Bel-C and Bel-B tobacco varieties and their use as indicators of ozone.
H. E. Heggestad (1991)
10.1104/PP.124.2.609
Ethylene induces epidermal cell death at the site of adventitious root emergence in rice.
H. Mergemann (2000)
Programmed cell death in plants : a pathogentriggered response activated coordinately with multiple defense reactions
JT Greenberg (1994)
10.1073/PNAS.93.10.5099
Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance.
Y. K. Sharma (1996)
10.1016/0092-8674(94)90217-8
Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions
J. Greenberg (1994)
10.1016/S0005-2728(00)00231-0
Polycations induce the release of soluble intermembrane mitochondrial proteins.
M. Mather (2001)
10.1007/BF00046452
Ozone-induced changes of mRNA levels of β-1,3-glucanase, chitinase and ‘pathogenesis-related’ protein 1b in tobacco plants
D. Ernst (2004)
10.1007/BF00201815
Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco
N. Yalpani (2004)
10.1105/tpc.11.3.431
The Involvement of Cysteine Proteases and Protease Inhibitor Genes in the Regulation of Programmed Cell Death in Plants
M. Solomon (1999)
10.1046/J.1469-8137.2002.00539.X
Ozone‐response mechanisms in tobacco: implications of polyamine metabolism
M. V. Buuren (2002)
Programmed
JT Greenberg (1994)
10.1104/PP.126.3.993
Ozone quenching properties of isoprene and its antioxidant role in leaves.
F. Loreto (2001)
10.1046/j.1365-313x.1998.00294.x
Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3.
M. Schraudner (1998)
10.1093/OXFORDJOURNALS.PCP.A029131
ATP Synthesis Driven by α-Keto Acid-stimulated Alternative Oxidase in Pea Leaf Mitochondria
A. Vianello (1997)
10.1034/J.1399-3054.2002.1150205.X
Salicylic acid modulates ozone-induced hypersensitive cell death in tobacco plants.
S. Pasqualini (2002)
10.1104/pp.104.1.67
Biochemical Plant Responses to Ozone (IV. Cross-Induction of Defensive Pathways in Parsley (Petroselinum crispum L.) Plants)
H. Eckey-Kaltenbach (1994)
10.1046/J.1365-313X.1993.04020327.X
Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging.
J. Greenberg (1993)
10.1111/J.1365-3040.1994.TB00173.X
Plant defence systems induced by ozone
J. Kangasjärvi (1994)
10.1016/0092-8674(94)90218-6
Arabidopsis mutants simulating disease resistance response
R. Dietrich (1994)
10.1016/0092-8674(94)90544-4
H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response
Alex Levine (1994)
10.1016/0003-2697(76)90527-3
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
M. M. Bradford (1976)
10.1104/pp.009712
Ethylene Synthesis Regulated by Biphasic Induction of 1-Aminocyclopropane-1-Carboxylic Acid Synthase and 1-Aminocyclopropane-1-Carboxylic Acid Oxidase Genes Is Required for Hydrogen Peroxide Accumulation and Cell Death in Ozone-Exposed Tomato1
W. Moeder (2002)
10.1016/S0981-9428(01)01250-5
In situ histochemical monitoring of ozone- and TMV-induced reactive oxygen species in tobacco leaves
S. Rossetti (2001)
10.1023/A:1026592509060
Hypersensitive response-related death
M. Heath (2004)
A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of proteindye binding
MM Bradford (1976)
10.1046/J.1365-313X.1996.9050715.X
Pollination induces mRNA poly(A) tail-shortening and cell deterioration in flower transmitting tissue.
H. Wang (1996)
10.1007/BF01279568
Programmed cell death of plant tracheary elements differentiating in vitro
A. Groover (2005)
10.1023/A:1026548726807
Ozone: a tool for probing programmed cell death in plants
M. V. Rao (2004)
10.1016/S0962-8924(00)01803-1
Mitochondria as the central control point of apoptosis.
S. Desagher (2000)
10.1105/tpc.9.7.1157
Programmed Cell Death in Plants.
R. Pennell (1997)
10.1046/J.0960-7412.2001.01247.X
Salt causes ion disequilibrium-induced programmed cell death in yeast and plants.
Gyung-Hye Huh (2002)
Pathogen-induced programmed cell death in tobacco.
R. Mittler (1997)
10.1016/0014-5793(90)80974-N
Hydrogen peroxide production during experimental protein glycation
Z. Y. Jiang (1990)
10.1104/pp.110.1.125
Ultraviolet-B- and Ozone-Induced Biochemical Changes in Antioxidant Enzymes of Arabidopsis thaliana
M. Rao (1996)
10.1016/S0891-5849(97)00108-1
The effects of ozone on antioxidant responses in plants.
Y. K. Sharma (1997)
10.1093/OXFORDJOURNALS.PCP.A029455
Evidence for Programmed Cell Death during Leaf Senescence in Plants
C. Yen (1998)
Hypersensitive responserelated death
MC Heath (2000)
Biochem - ical plant responses to ozone : III . Activation of the defence - related proteins  - 1 , 3 - glucanase and chitinase in tobacco
M Schraudner (1992)
Mitochondria as the control point of apoptosis
S Desagher (2000)
death in plants : a pathogen - triggered response activated coordinately with multiple defense reactions
A Groover (1997)
10.1046/J.1365-3040.2001.00692.X
Metabolic regulation and gene expression of root phosphoenolpyruvate carboxylase by different nitrogen sources
S. Pasqualini (2001)
10.1046/J.1365-313X.1997.12020267.X
A programmed cell death pathway activated in carrot cells cultured at low cell density
P. McCabe (1997)
10.1073/PNAS.90.3.980
Do all programmed cell deaths occur via apoptosis?
L. M. Schwartz (1993)
10.1128/JB.107.3.815-823.1971
Protease activities during the course of sporulation on Bacillus subtilis.
L. Prestidge (1971)
10.1016/S1360-1385(96)90005-9
Logjam at the Styx: Programmed cell death in plants
A. M. Jones (1996)
10.1016/S0176-1617(97)80016-8
Osmotically-stressed poplar cell cultures: anthocyanin accumulation, deaminase activity, and solute composition
Ashok Tholakalabavi (1997)
10.1016/S0305-1978(00)00080-6
Effect of a chronic and moderate ozone pollution on the phenolic pattern of bean leaves (Phaseolus vulgaris L. cv Nerina): relations with visible injury and biomass production.
M. Kanoun (2001)
10.1105/tpc.12.10.1849
Ozone-Sensitive Arabidopsis rcd1 Mutant Reveals Opposite Roles for Ethylene and Jasmonate Signaling Pathways in Regulating Superoxide-Dependent Cell Death
K. Overmyer (2000)
10.1105/tpc.8.3.375
Apoptosis: A Functional Paradigm for Programmed Plant Cell Death Induced by a Host-Selective Phytotoxin and Invoked during Development.
H. Wang (1996)
10.1046/J.1365-313X.1999.00544.X
Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement.
M. Gao (1999)
10.1007/978-1-4757-9217-1_16
ENDONUCLEASES ASSOCIATED WITH APOPTOSIS
A. Eastman (1994)
10.1042/BJ3160487
Degradation of aggrecan precursors within a specialized subcompartment of the chicken chondrocyte endoplasmic reticulum.
M. Alonso (1996)
10.1083/JCB.119.3.493
Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation
Y. Gavrieli (1992)
10.1104/PP.118.4.1243
Ozone sensitivity in hybrid poplar is correlated with a lack of defense-gene activation
Riehl Koch J (1998)
10.1023/A:1026561029533
Salicylic acid in the machinery of hypersensitive cell death and disease resistance
M. E. Alvarez (2004)
Colorimetry of Total Phenolics with Phosphomolybdic-Phosphotungstic Acid Reagents
V. L. Singleton (1965)
10.1104/PP.95.3.882
Biochemical plant responses to ozone : I. Differential induction of polyamine and ethylene biosynthesis in tobacco.
C. Langebartels (1991)
10.1023/A:1026536324081
Programmed cell death in plant reproduction
Hen-Ming Wu (2004)
10.1016/S1360-1385(97)01162-X
Ozone: An abiotic elicitor of plant defence reactions
H. Sandermann (1998)
10.1080/11263500112331350810
Apoptosis-like DNA fragmentation in leaves and floral organs precedes their developmental senescence
A. Mazzucato (2001)
10.1046/J.1365-313X.1999.00447.X
Characterization of an Arabidopsis thaliana receptor-like protein kinase gene activated by oxidative stress and pathogen attack.
P. Czernic (1999)
10.2307/2266119
Plant Response to Air Pollution.
M. Yunus (1997)



This paper is referenced by
10.1016/J.ENVEXPBOT.2008.09.005
Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity
G. Tanou (2009)
Stress responses of duckweed (Lemna minor L.) and water velvet (Azolla filiculoides Lam.) to anionic surfactant sodium-dodecyl-sulphate (SDS)
. Fornia (2012)
10.5511/plantbiotechnology.19.0531b
Copper treatment of peach leaves causes lesion formation similar to the biotic stress response.
Fumiyuki Goto (2019)
10.1016/j.plaphy.2008.09.008
NO release by nitric oxide donors in vitro and in planta.
L. Ederli (2009)
10.1038/nchembio.158
A unified mechanism of action for volatile isoprenoids in plant abiotic stress.
C. Vickers (2009)
Characterization of AtCNGC11/12-induced Cell Death and the Role of AtCNGC11 and AtCNGC12 in Ca2+ Dependent Signalling Pathways
William Urquhart (2011)
10.3390/plants8040085
Elevated Ozone Concentration Reduces Photosynthetic Carbon Gain but Does Not Alter Leaf Structural Traits, Nutrient Composition or Biomass in Switchgrass
Shuai Li (2019)
10.1007/s00425-005-0016-z
Thaxtomin A induces programmed cell death in Arabidopsis thaliana suspension-cultured cells
I. Duval (2005)
10.1007/978-94-007-6428-6_11
Signaling Role of Salicylic Acid in Abiotic Stress Responses in Plants
Tomonori Kawano (2013)
INDIVIDUAL AND COMBINED EFFECTS OF SO AND O ON ROOT KNOT NEMATODE MULTIPLICATION
Deepti Yadav (2014)
10.1111/plb.12347
Biochemical and physiological processes associated with the differential ozone response in ozone-tolerant and sensitive soybean genotypes.
Cattleya Chutteang (2016)
10.1089/ars.2012.5016
Apoplastic and chloroplastic redox signaling networks in plant stress responses.
Maija Sierla (2013)
10.1007/978-3-642-36470-9_2
Salicylic Acid-Induced Local and Long-Distance Signaling Models in Plants
Tomonori Kawano (2013)
10.1007/s11103-007-9239-7
The chimeric cyclic nucleotide-gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner
W. Urquhart (2007)
10.1007/978-981-10-1201-3_7
Air Pollutants and Photosynthetic Efficiency of Plants
Bhupinder Dhir (2016)
10.1094/PHP-2013-0509-09-RS
A Quick and Simple Method to Evaluate Anisogramma anomala Ascospore Viability
S. Heckert (2013)
10.1111/J.1399-3054.2006.00775.X
The role of the mitochondrion in plant responses to biotic stress
S. Amirsadeghi (2007)
10.1016/j.envpol.2011.08.043
The efficiency of tobacco Bel-W3 and native species for ozone biomonitoring in subtropical climate, as revealed by histo-cytochemical techniques.
E. S. Alves (2011)
10.1093/treephys/tpp009
RNAi-mediated suppression of isoprene biosynthesis in hybrid poplar impacts ozone tolerance.
Katja Behnke (2009)
10.1111/J.1469-8137.2005.01409.X
Isoprene decreases the concentration of nitric oxide in leaves exposed to elevated ozone.
V. Velikova (2005)
10.1016/J.JPLPH.2007.10.003
Pre-exposure of calli to ozone promotes tolerance of regenerated Lycopersicon esculentum cv. PKM1 plantlets against acute ozone stress.
D. Nagendraprasad (2008)
10.14578/JKFS.2013.102.4.601
The Effects of Ozone on Photosynthesis, Antioxidative Enzyme Activity and Leaf Anatomical Response in the Indoor Plants and Japanese Red Pine
Ju Young Lee (2013)
10.1080/14786419.2015.1118631
Ecophysiological and phytochemical response to ozone of wine grape cultivars of Vitis vinifera L.
A. Valletta (2016)
10.3390/metabo9030046
Ozone and Wounding Stresses Differently Alter the Temporal Variation in Formylated Phloroglucinols in Eucalyptus globulus Leaves
Bin Liu (2019)
10.1002/9780470986592.CH10
The Mitochondrion and Plant Programmed Cell Death
Mark Diamond (2007)
10.1016/B978-0-12-385851-1.00004-4
The Botanical Dance of Death: Programmed Cell Death in Plants
J. Kacprzyk (2011)
10.3389/fpls.2015.00234
Vacuolar processing enzyme in plant programmed cell death
N. Hatsugai (2015)
10.1002/9781119552154.ch21
Isoprenoids in Plant Protection Against Abiotic Stress
Syed Uzma Jalil (2020)
Ascospore viability and dispersal from pruned branches infected with Anisogramma anomala
S. Heckert (2011)
10.1039/B315561G
Protein oxidation in plant mitochondria as a stress indicator.
I. M. Møller (2004)
10.11298/TAIKI1995.40.2_41
Role of Phytohormones in Ozone-exposed Plants
D. Ogawa (2005)
10.1093/TREEPHYS/25.3.277
Activation of stress-responsive mitogen-activated protein kinase pathways in hybrid poplar (Populus trichocarpa x Populus deltoides).
L. Hamel (2005)
See more
Semantic Scholar Logo Some data provided by SemanticScholar