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

Light-Dependent Death Of Maize Lls1 Cells Is Mediated By Mature Chloroplasts1

J. Gray, D. Janick-Buckner, B. Buckner, P. S. Close, G. Johal
Published 2002 · Medicine, Biology

Cite This
Download PDF
Analyze on Scholarcy
Share
We reported previously the isolation of a novel cell death-suppressing gene from maize (Zea mays) encoded by the Lls1 (Lethal leaf spot-1) gene. Although the exact metabolic function of LLS1 remains elusive, here we provide insight into mechanisms that underlie the initiation and propagation of cell death associated withlls1 lesions. Our data indicate that lls1lesions are triggered in response to a cell-damaging event caused by any biotic or abiotic agent or intrinsic metabolic imbalance—as long as the leaf tissue is developmentally competent to developlls1 lesions. Continued expansion of these lesions, however, depends on the availability of light, with fluence rate being more important than spectral quality. Double-mutant analysis oflls1 with two maize mutants oil-yellowand iojap, both compromised photosynthetically and unable to accumulate normal levels of chlorophyll, indicated that it was the light harvested by the plant that energized lls1lesion development. Chloroplasts appear to be the key mediators oflls1 cell death; their swelling and distortion occurs before any other changes normally associated with dying cells. In agreement with these results are indications that LLS1 is a chloroplast-localized protein whose transcript was detected only in green tissues. The propagative nature of light-dependentlls1 lesions predicts that cell death associated with these lesions is caused by a mobile agent such as reactive oxidative species. LLS1 may act to prevent reactive oxidative species formation or serve to remove a cell death mediator so as to maintain chloroplast integrity and cell survival.
This paper references
10.1094/MPMI.1998.11.11.1110
The maize lethal leaf spot 1 mutant has elevated resistance to fungal infection at the leaf epidermis
C. Simmons (1998)
10.1038/sj.cdd.4400309
The hypersensitive response and the induction of cell death in plants
J. Morel (1997)
10.1105/tpc.12.3.405
Deficiency in Fatty Acid Synthase Leads to Premature Cell Death and Dramatic Alterations in Plant Morphology
Z. Mou (2000)
10.1007/BF00273926
Organization, promoter analysis and transcriptional regulation of the Staphylococcus xylosus xylose utilization operon
Christine W. Sizemore (2004)
10.1016/S0092-8674(00)81912-1
The Barley Mlo Gene: A Novel Control Element of Plant Pathogen Resistance
R. Büschges (1997)
10.1016/0885-5765(88)90040-9
Evidence that molecular components of papillae may be involved in ml-o resistance to barley powdery mildew
J. Aist (1988)
10.1046/J.1365-313X.2001.01058.X
A deficiency of coproporphyrinogen III oxidase causes lesion formation in Arabidopsis.
A. Ishikawa (2001)
10.1073/PNAS.94.7.3454
Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning.
B. Rathinasabapathi (1997)
10.1016/S0885-5765(88)80033-X
Hypersensitive cell death, autofluorescence, and insoluble silicon accumulation in barley leaf epidermal cells under attack by Erysiphe graminis f. sp. hordei***
H. Koga (1988)
10.1073/PNAS.98.2.771
The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms.
J. M. Mach (2001)
10.1034/J.1399-3054.2000.108003231.X
Cell death in maize.
B. Buckner (2000)
10.3109/10520296409061248
Identification of Cauose by its Diachrome and Fluorochrome Reactions
W. Eschrich (1964)
10.1016/S0006-2952(98)00227-5
Reactive oxygen intermediates as mediators of programmed cell death in plants and animals.
T. Jabs (1999)
Accession numbers used for the CAO (chlorophyll a oxygenase, chlorophyll b synthase) clade are as follows: Arabidopsis CAO (Arabidopsis), AAD54323; rice CAO
Cmo
Gene descriptions
MG Neuffer (1997)
10.1023/A:1006198431596
Apoptosis in developing anthers and the role of ABA in this process during androgenesis in Hordeum vulgare L.
M. Wang (1999)
10.1002/J.1537-2197.1983.TB06434.X
PLASTID DEVELOPMENT IN IOJAP‐ AND CHLOROPLAST MUTATOR‐AFFECTED MAIZE PLANTS
D. Thompson (1983)
10.1023/A:1026592509060
Hypersensitive response-related death
M. Heath (2004)
10.1074/JBC.274.49.34993
Topology, Subcellular Localization, and Sequence Diversity of the Mlo Family in Plants*
A. Devoto (1999)
Development of a core RFLP map in maize using an immortalized F2 population.
J. Gardiner (1993)
10.1094/MPMI.1999.12.11.1022
LSD1 regulates salicylic acid induction of copper zinc superoxide dismutase in Arabidopsis thaliana.
D. Kliebenstein (1999)
the CMO (choline monooxygenase) clade are as follows: Arabidopsis CMO precursor, T08550; spinach
10.1101/GAD.218202
Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense.
P. Brodersen (2002)
10.1007/978-1-4684-4544-2_29
Disease Lesion Mimic Mutations
V. Walbot (1983)
10.1104/PP.125.1.94
Programmed cell death in development and defense.
A. Jones (2001)
10.1094/MPMI.1998.11.7.643
Induced resistance responses in maize.
S. W. Morris (1998)
10.1105/tpc.12.10.1811
Simulation of Fungal-Mediated Cell Death by Fumonisin B1 and Selection of Fumonisin B1–Resistant (fbr) Arabidopsis Mutants
J. Stone (2000)
A lethal leaf spot of maize
AJ Ullstrup (1967)
10.1105/tpc.8.8.1367
Disease Lesion Mimicry Caused by Mutations in the Rust Resistance Gene rp1.
G. Hu (1996)
10.1105/TPC.8.10.1773
Resistance gene-dependent plant defense responses.
K. Hammond-Kosack (1996)
10.1046/J.1365-313X.1993.04020327.X
Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging.
J. Greenberg (1993)
10.1105/tpc.9.7.1157
Programmed Cell Death in Plants.
R. Pennell (1997)
10.1023/A:1009616228304
Role of reactive oxygen species (ROS) in apoptosis induction
H. Simon (2004)
10.1073/PNAS.95.21.12719
Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a.
A. Tanaka (1998)
10.1104/PP.116.1.107
Cellular responses to tetrapyrrole-induced oxidative stress in transgenic plants with reduced uroporphyrinogen decarboxylase or coproporphyrinogen oxidase activity
Hans-Peter Mock (1997)
10.1073/PNAS.96.24.14165
Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection.
R. Mittler (1999)
of mesophyll and bundle sheath chloroplast thylakoids of maize ( Zea mays L . )
ML Polacco (1987)
10.1146/ANNUREV.ARPLANT.48.1.525
PROGRAMMED CELL DEATH IN PLANT-PATHOGEN INTERACTIONS.
J. Greenberg (1997)
10.1094/MPMI.2000.13.8.869
Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight.
Z. Yin (2000)
10.1016/S0981-9428(99)80031-X
Activated oxygen and free oxygen radicals in pathology: New insights and analogies between animals and plants
S. Hippeli (1999)
10.1016/S0022-2836(05)80360-2
Basic local alignment search tool.
S. Altschul (1990)
Identification of callose by its diachrome and flourochrome reactions
W Eschrich (1964)
10.1300/J101v13n25_11
Flow
Cathleen A. Towey (2000)
10.1105/tpc.10.7.1095
A Porphyrin Pathway Impairment Is Responsible for the Phenotype of a Dominant Disease Lesion Mimic Mutant of Maize
G. Hu (1998)
10.1002/(SICI)1097-0320(19960201)23:2<97::AID-CYTO2>3.0.CO;2-I
Flow cytometry of mesophyll and bundle sheath chloroplast thylakoids of maize (Zea mays L.).
E. Pfündel (1996)
10.1002/j.1460-2075.1992.tb05497.x
Molecular cloning and characterization of iojap (ij), a pattern striping gene of maize.
C. Han (1992)
10.1105/TPC.9.2.209
Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola.
C. Bestwick (1997)
10.1093/emboj/16.24.7342
The chloroplastic protein import machinery contains a Rieske‐type iron–sulfur cluster and a mononuclear iron‐binding protein
A. Caliebe (1997)
10.1093/OXFORDJOURNALS.JHERED.A110341
Genetic, developmental, and environmental influences on Oy-700 expression in maize
M. Polacco (1987)
10.1007/s004410000193
The morphology of apoptosis
G. Häcker (2000)
10.1126/science.274.5294.1853
The Metal-Insulator Transition in Correlated Disordered Systems
E. Abrahams (1996)
10.1105/tpc.11.9.1695
The Gain-of-Function Arabidopsis acd6 Mutant Reveals Novel Regulation and Function of the Salicylic Acid Signaling Pathway in Controlling Cell Death, Defenses, and Cell Growth
D. N. Rate (1999)
10.1007/BF00260649
Recombination at the Rp1 locus of maize
S. Hulbert (2004)
10.1016/S0098-8472(98)00040-9
Development of ultrastructural damage to chloroplasts in a plastoquinone-deficient mutant of maize
R. R. Wise (1998)
Apoptosis, oncosis, and necrosis. An overview of cell death.
G. Majno (1995)
10.1136/bmj.318.7189.995
Induction
G. Chamberlain (1999)
10.1016/S0092-8674(00)80179-8
A Novel Suppressor of Cell Death in Plants Encoded by the Lls1 Gene of Maize
J. Gray (1997)
10.1046/J.1365-313X.1997.11040729.X
Programmed cell death in the root cortex of soybean root necrosis mutants.
R. Kosslak (1997)
10.1016/0092-8674(94)90218-6
Arabidopsis mutants simulating disease resistance response
R. Dietrich (1994)
Recombination between paralogues at the Rp1 rust resistance locus in maize.
Q. Sun (2001)
10.1093/JEXBOT/51.342.123
Bundle sheath proteins are more sensitive to oxidative damage than those of the mesophyll in maize leaves exposed to paraquat or low temperatures.
A. Kingston-Smith (2000)
A tale of two mimics; transposon mutagenesis and characterization of two disease lesion mimic mutations of maize
G. Johal (1994)
Medicago truncatula LLS1 homolog, contig of overlapping expressed sequence tags AW257191
Be248884
Pathogen-induced programmed cell death in tobacco.
R. Mittler (1997)
10.1038/sj.cdd.4400782
The ‘harmless’ release of cytochrome c
O. V. Ahsen (2000)
10.1105/tpc.11.7.1365
Molecular Characterization of the Maize Rp1-D Rust Resistance Haplotype and Its Mutants
N. Collins (1999)
10.1110/PS.8.5.978
ChloroP, a neural network‐based method for predicting chloroplast transit peptides and their cleavage sites
O. Emanuelsson (1999)
10.1126/SCIENCE.1068037
A Draft Sequence of the Rice Genome (Oryza sativa L. ssp. indica)
Jun Yu (2002)
10.1126/SCIENCE.1359642
Reductase activity encoded by the HM1 disease resistance gene in maize.
G. Johal (1992)
10.1007/s004250050504
Changes in the location of polyphenol oxidase in potato (Solanum tuberosum L.) tuber during cell death in response to impact injury: comparison with wound tissue
J. C. Partington (1999)
10.1002/BIES.950170805
Disease lesion mimics of maize: A model for cell death in plants
G. Johal (1995)
A draft sequence of the rice genome (Oryza sativa L. ssp. japonica).
S. Goff (2002)
10.1515/znc-1999-9-1002
Response Of Chloroplast Structure To Photodynamic Herbicides And High Oxygen
A. Mostowska (1999)
10.1046/J.1365-313X.1999.00420.X
Inhibition of protoporphyrinogen oxidase expression in Arabidopsis causes a lesion-mimic phenotype that induces systemic acquired resistance.
A. Molina (1999)
The maize NCS2 abnormal growth mutant has a chimeric nad4-nad7 mitochondrial gene and is associated with reduced complex I function.
J. Marienfeld (1994)
10.1126/science.273.5283.1853
Initiation of Runaway Cell Death in an Arabidopsis Mutant by Extracellular Superoxide
T. Jabs (1996)
10.1105/tpc.8.10.1793
Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions.
J. Dangl (1996)
10.1023/A:1026552827716
Regulators of cell death in disease resistance
K. Shirasu (2004)
10.1038/35037710
The biochemistry of apoptosis
M. Hengartner (2000)
Recombination at the Rp 1 locus of maize
SH Hulbert (1991)



This paper is referenced by
10.1016/j.plaphy.2010.08.016
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.
S. Gill (2010)
10.1016/S2095-3119(13)60393-7
Identification and Genetic Analysis of a Novel Rice Spotted-Leaf Mutant with Broad-Spectrum Resistance to Xanthomonas oryzae pv. oryzae
Hai-Chao Shen (2014)
10.2478/V10176-012-0042-X
Life with Oxidative Stress
Dorota Gurda (2012)
10.1186/1471-2229-4-5
Synthesis of chlorophyll b: Localization of chlorophyllide a oxygenase and discovery of a stable radical in the catalytic subunit
L. Eggink (2003)
10.1093/jxb/erp320
Chloroplast and reactive oxygen species involvement in apoptotic-like programmed cell death in Arabidopsis suspension cultures
S. M. Doyle (2010)
10.1093/jxb/err402
Photosynthesis, photorespiration, and light signalling in defence responses.
Saijaliisa Kangasjärvi (2012)
10.1016/j.jplph.2015.01.004
Differences in gene expression between natural and artificially induced leaf senescence in barley.
Armin Springer (2015)
10.1371/journal.pone.0201359
Propagation of cell death in dropdead1, a sorghum ortholog of the maize lls1 mutant
Anoop Sindhu (2018)
10.1007/978-94-007-5724-0_16
The Pathway of Chlorophyll Degradation: Catabolites, Enzymes and Pathway Regulation
S. Hörtensteiner (2013)
10.1080/17429145.2018.1432772
Drought stress revealed physiological, biochemical and gene-expressional variations in ‘Yoshihime’ peach (Prunus Persica L) cultivar
M. S. Haider (2018)
10.1073/pnas.2036571100
Chlorophyll breakdown: Pheophorbide a oxygenase is a Rieske-type iron–sulfur protein, encoded by the accelerated cell death 1 gene
Adriana Pružinská (2003)
10.1146/ANNUREV.ARPLANT.57.032905.105212
Chlorophyll degradation during senescence.
S. Hörtensteiner (2006)
10.1111/J.1365-313X.2006.02752.X
Specific cleavage of ribosomal RNA and mRNA during victorin-induced apoptotic cell death in oat.
T. X. Hoat (2006)
10.1002/9780470988855.CH2
Chlorophyll Catabolism and Leaf Coloration
S. Hörtensteiner (2007)
10.1007/s00425-018-2946-2
Characterization of the pheophorbide a oxygenase/phyllobilin pathway of chlorophyll breakdown in grasses
A. Das (2018)
10.1093/mp/ssp029
Camouflage patterning in maize leaves results from a defect in porphobilinogen deaminase.
Mingshu Huang (2009)
10.1534/GENETICS.104.036327
Identification and Characterization of Regions of the Rice Genome Associated With Broad-Spectrum, Quantitative Disease Resistance
R. Wisser (2005)
EVALUATION OF NOVEL INPUT OUTPUT TRAITS IN SORGHUM THROUGH BIOTECHNOLOGY
Tejinder Kumar Mall (2010)
10.1007/s00122-016-2758-3
A novel nitrogen-dependent gene associates with the lesion mimic trait in wheat
Lei Li (2016)
10.1007/s11103-004-2331-3
Recent advances in chlorophyll biosynthesis and breakdown in higher plants
U. Eckhardt (2004)
10.1111/J.1365-313X.2006.02894.X
Reduced activity of plastid protoporphyrinogen oxidase causes attenuated photodynamic damage during high-light compared to low-light exposure.
I. Lermontova (2006)
10.1111/J.1365-313X.2007.03051.X
Early chloroplastic alterations analysed by optical coherence tomography during a harpin-induced hypersensitive response.
M. Boccara (2007)
10.1016/j.plaphy.2015.02.001
Enhanced excision repair and lack of PSII activity contribute to higher UV survival of Chlamydomonas reinhardtii cells in dark.
Vishalsingh R Chaudhari (2015)
10.1023/B:PLAN.0000028766.61559.4c
A small family of LLS1-related non-heme oxygenases in plants with an origin amongst oxygenic photosynthesizers
J. Gray (2004)
10.1105/tpc.106.044891
The Senescence-Induced Staygreen Protein Regulates Chlorophyll Degradation[W]
S. Park (2007)
10.1104/pp.107.097865
RNAi Silencing of Genes for Elicitation or Biosynthesis of 5-Deoxyisoflavonoids Suppresses Race-Specific Resistance and Hypersensitive Cell Death in Phytophthora sojae Infected Tissues1[OA]
T. L. Graham (2007)
10.3389/fgene.2015.00226
The molecular cloning and clarification of a photorespiratory mutant, oscdm1, using enhancer trapping
Jinxia Wu (2015)
10.1094/MPMI-18-0375
OsLSD1, a rice zinc finger protein, regulates programmed cell death and callus differentiation.
L. Wang (2005)
10.1104/pp.15.01870
The Genetics of Leaf Flecking in Maize and Its Relationship to Plant Defense and Disease Resistance1[OPEN]
B. Olukolu (2016)
10.1023/B:PLAN.0000028789.51807.6a
The Wound-Inducible Lls1 Gene from Maize is an Orthologue of the Arabidopsis Acd1 Gene, and the LLS1 Protein is Present in Non-Photosynthetic Tissues
Manli Yang (2004)
10.1080/09670260600960850
Acclimation to darkness in the marine chlorophyte Koliella antarctica cultured under low salinity: hypotheses on its origin in the polar environment
L. Ferroni (2007)
10.1071/FP07153
AtMCP1b, a chloroplast-localised metacaspase, is induced in vascular tissue after wounding or pathogen infection.
Luis Castillo-Olamendi (2008)
See more
Semantic Scholar Logo Some data provided by SemanticScholar