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

The Amount And Integrity Of MtDNA In Maize Decline With Development

D. J. Oldenburg, R. A. Kumar, A. Bendich
Published 2012 · Medicine, Biology

Cite This
Download PDF
Analyze on Scholarcy
Share
In maize and other grasses there is a developmental gradient from the meristematic cells at the base of the stalk to the differentiated cells at the leaf tip. This gradient presents an opportunity to investigate changes in mitochondrial DNA (mtDNA) that accompany growth under light and dark conditions, as done previously for plastid DNA. Maize mtDNA was analyzed by DAPI-DNA staining of individual mitochondria, gel electrophoresis/blot hybridization, and real-time qPCR. Both the amount and integrity of the mtDNA were found to decline with development. There was a 20-fold decline in mtDNA copy number per cell from the embryo to the light-grown leaf blade. The amount of DNA per mitochondrial particle was greater in dark-grown leaf blade (24 copies, on average) than in the light (2 copies), with some mitochondria lacking any detectable DNA. Three factors that influence the demise of mtDNA during development are considered: (1) the decision to either repair or degrade mtDNA molecules that are damaged by the reactive oxygen species produced as byproducts of respiration; (2) the generation of ATP by photophosphorylation in chloroplasts, reducing the need for respiratory-competent mitochondria; and (3) the shift in mitochondrial function from energy-generating respiration to photorespiration during the transition from non-green to green tissue.
This paper references
10.1104/pp.107.3.815
C4 Photosynthesis (The Effects of Leaf Development on the CO2-Concentrating Mechanism and Photorespiration in Maize)
Z. Dai (1995)
10.1002/bies.201000073
Mitochondria and the culture of the Borg
Emélie Braschi (2010)
10.1111/J.1365-313X.2005.02561.X
Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion.
M. Sheahan (2005)
10.1016/S0168-9525(00)89056-3
The maize mitochondrial genome: dynamic, yet functional.
C. Fauron (1995)
10.1016/J.JMB.2004.10.001
Changes in the structure of DNA molecules and the amount of DNA per plastid during chloroplast development in maize.
D. J. Oldenburg (2004)
10.1007/s004250050509
Expression of CKS1At in Arabidopsis thaliana indicates a role for the protein in both the mitotic and the endoreduplication cycle
A. Jacqmard (1999)
10.1104/PP.96.1.232
Chloroplast Structure and Function Is Altered in the NCS2 Maize Mitochondrial Mutant.
D. Roussell (1991)
10.1007/s002940050532
Phage T4-like intermediates of DNA replication and recombination in the mitochondria of the higher plant Chenopodium album (L.)
S. Backert (2000)
10.1146/ANNUREV.BIOCHEM.76.060305.152028
DNA replication and transcription in mammalian mitochondria.
M. Falkenberg (2007)
chloroplast and leaf development
V Ravi (2008)
10.1104/pp.112.194720
RecA-Dependent DNA Repair Results in Increased Heteroplasmy of the Arabidopsis Mitochondrial Genome1[C][W]
Marie Miller-Messmer (2012)
10.1046/J.1365-313X.2003.01748.X
The intermembrane space of plant mitochondria contains a DNase activity that may be involved in programmed cell death.
J. Balk (2003)
10.1093/gbe/evr001
Correlation between Nuclear Plastid DNA Abundance and Plastid Number Supports the Limited Transfer Window Hypothesis
D. Smith (2011)
10.1111/j.1365-313X.2011.04726.x
Arabidopsis RUGOSA2 encodes an mTERF family member required for mitochondrion, chloroplast and leaf development.
V. Quesada (2011)
10.1104/PP.96.3.985
Systemic Endopolyploidy in Arabidopsis thaliana.
D. Galbraith (1991)
10.1016/j.tplants.2010.12.006
Ancient and essential: the assembly of iron-sulfur clusters in plants.
J. Balk (2011)
Size and structure of replicating
DJ Oldenburg (1996)
10.1371/journal.pgen.1001066
Transmission of Mitochondrial DNA Diseases and Ways to Prevent Them
J. Poulton (2010)
10.1093/OXFORDJOURNALS.MOLBEV.A025977
Analysis of plastid DNA-like sequences within the nuclear genomes of higher plants.
M. Ayliffe (1998)
10.1007/978-0-387-73003-5_350
Mitochondrial DNA
M. Chèvremont (2009)
10.1038/nrg1271
Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes
J. Timmis (2004)
10.1146/annurev-arplant-042110-103857
Organization and regulation of mitochondrial respiration in plants.
A. Millar (2011)
Studies on the Behavior of Mitochondrial DNA: Synthesis of Mitochondrial DNA Occurs Actively in a Specific Region just above the Quiescent Center in the Root Meristem of Pelargonium Zonale
T. Kuroiwa (1992)
10.1007/BF00197541
Behavior of organelles and their nucleoids in the shoot apical meristem during leaf development in Arabidopsis thaliana L.
M. Fujie (2004)
10.1016/S1097-2765(04)00179-0
Mitochondrial signaling: the retrograde response.
R. Butow (2004)
10.1093/nar/gki783
Structural and functional characterizations of mung bean mitochondrial nucleoids
H. Dai (2005)
10.1093/nar/gkr1245
Role of polynucleotide kinase/phosphatase in mitochondrial DNA repair
N. Tahbaz (2012)
10.1016/j.pbi.2007.07.007
Interorganellar communication.
P. Pesaresi (2007)
10.1007/s10059-011-0036-4
Characterization of the structure and DNA complexity of mung bean mitochondrial nucleoids
Yih-Shan Lo (2011)
10.1016/j.pbi.2010.01.006
Photorespiration: current status and approaches for metabolic engineering.
V. Maurino (2010)
10.1105/tpc.010009
Nuclear Genes That Encode Mitochondrial Proteins for DNA and RNA Metabolism Are Clustered in the Arabidopsis Genome Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010009.
A. Elo (2003)
10.1006/JMBI.1997.1581
The structure of mitochondrial DNA from the liverwort, Marchantia polymorpha.
D. J. Oldenburg (1998)
10.1007/s00425-006-0329-6
Loss or retention of chloroplast DNA in maize seedlings is affected by both light and genotype
D. J. Oldenburg (2006)
10.1093/NAR/25.3.582
Unique features of the mitochondrial rolling circle-plasmid mp1 from the higher plant Chenopodium album (L.).
S. Backert (1997)
Real-time PCR evaluation of seven DNA extraction methods for the purpose of GMO analysis
Jasbeer Kaur Kesar Singh (2009)
10.1006/JMBI.2001.4783
Mitochondrial DNA from the liverwort Marchantia polymorpha: circularly permuted linear molecules, head-to-tail concatemers, and a 5' protein.
D. J. Oldenburg (2001)
10.1186/1472-6750-6-37
Critical points of DNA quantification by real-time PCR – effects of DNA extraction method and sample matrix on quantification of genetically modified organisms
K. Cankar (2006)
10.1111/j.1469-8137.2012.04166.x
Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide.
M. Cvetkovska (2012)
10.1159/000312724
Recent and Frequent Insertions of Chloroplast DNA into Maize Nuclear Chromosomes
L. Roark (2010)
10.1093/jxb/erq441
Independent effects of leaf growth and light on the development of the plastid and its DNA content in Zea species.
Qi Feng Zheng (2011)
10.1038/embor.2011.168
The incredible shrinking organelle
M. Gray (2011)
10.1093/NAR/14.24.9755
Tricircular mitochondrial genomes of Brassica and Raphanus: reversal of repeat configurations by inversion.
J. Palmer (1986)
Total genomic DNA extraction, quality check and quantitation Proceedings of the training programme on classical and modern plant breeding techniques—a hands on training
Kk Vinod (2004)
10.4161/psb.6.6.15224
How and why does mitochondrial respiratory chain respond to light?
K. Yoshida (2011)
10.1007/BF00336777
Reaching for the ring: the study of mitochondrial genome structure
A. Bendich (2004)
10.1199/tab.0110
Chloroplast Biogenesis: Control of Plastid Development, Protein Import, Division and Inheritance
W. Sakamoto (2008)
10.1534/genetics.107.079624
Mitochondrial DNA Transfer to the Nucleus Generates Extensive Insertion Site Variation in Maize
Ashley N. Lough (2008)
10.1104/pp.104.044602
Sequence and Comparative Analysis of the Maize NB Mitochondrial Genome1[w]
S. Clifton (2004)
10.1007/BF01287811
Morphometric analysis of cucurbit mitochondria: The relationship between chondriome volume and DNA content
A. Bendich (2005)
10.1016/J.TIG.2003.10.012
Mitochondrial genomes: anything goes.
G. Burger (2003)
10.1093/JXB/ERL148
Horizontal gene transfer in plants.
A. O. Richardson (2007)
Dosage compensation in Drosophila.
J. Lucchesi (1983)
10.1371/journal.pgen.1000834
Molecular Poltergeists: Mitochondrial DNA Copies (numts) in Sequenced Nuclear Genomes
Einat Hazkani-Covo (2010)
Total genomic DNA extraction, quality check and quantitation
KK Vinod (2004)
10.1074/JBC.M307525200
Molecular Definition of the Ascorbate-Glutathione Cycle in Arabidopsis Mitochondria Reveals Dual Targeting of Antioxidant Defenses in Plants*
O. Chew (2003)
10.1006/JMBI.1996.0048
Structural analysis of mitochondrial DNA molecules from fungi and plants using moving pictures and pulsed-field gel electrophoresis.
A. Bendich (1996)
10.1007/s00709-011-0325-y
Effects of chloroplast dysfunction on mitochondria: white sectors in variegated leaves have higher mitochondrial DNA levels and lower dark respiration rates than green sectors
Haruka Toshoji (2011)
10.1007/s002940050067
Electron microscopic investigation of mitochondrial DNA from Chenopodium album (L.).
S. Backert (1996)
10.1007/978-94-009-0951-9_6
Extraction of DNA from plant tissues
S. O. Rogers (1989)
The structure of mitochondrial
DJ Oldenburg (1998)
10.1016/j.mito.2011.05.004
The implications of mitochondrial DNA copy number regulation during embryogenesis.
Phillippa J. Carling (2011)
10.1104/PP.89.3.1011
Plastid transcription activity and DNA copy number increase early in barley chloroplast development.
B. Baumgartner (1989)
In vivo measurement of plant respiration
M. Ribas-Carbó (2010)
10.1038/nature01743
Widespread horizontal transfer of mitochondrial genes in flowering plants
U. Bergthorsson (2003)
10.1093/nar/gkp100
Oxidative stress induces degradation of mitochondrial DNA
I. Shokolenko (2009)
10.1105/tpc.8.3.447
Size and Structure of Replicating Mitochondrial DNA in Cultured Tobacco Cells.
D. J. Oldenburg (1996)
Quantitative fluorescence
S Miyamura (1986)
10.1093/jxb/erp361
Heteroplasmy and stoichiometric complexity of plant mitochondrial genomes--though this be madness, yet there's method in't.
M. Woloszynska (2010)
10.1016/S1360-1385(97)01148-5
The mystery of the rings: structure and replication of mitochondrial genomes from higher plants
S. Backert (1997)
10.1104/pp.108.126953
The Mitochondrial Cycle of Arabidopsis Shoot Apical Meristem and Leaf Primordium Meristematic Cells Is Defined by a Perinuclear Tentaculate/Cage-Like Mitochondrion1[W][OA]
J. M. Seguí-Simarro (2008)
10.1016/J.BBAMCR.2006.01.003
Plant mitochondrial dynamics.
David C Logan (2006)
10.1038/nrg2348
Coordination of gene expression between organellar and nuclear genomes
Jesse D. Woodson (2008)
10.1016/j.tplants.2012.01.008
Molecular evolution of genes recruited into C₄ photosynthesis.
Ben P. Williams (2012)
10.1146/annurev.arplant.043008.092119
DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis.
T. Kleine (2009)
10.1007/s10265-009-0268-y
Mitochondrial fusion and inheritance of the mitochondrial genome
H. Takano (2009)
10.1373/clinchem.2008.112797
The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.
S. Bustin (2009)
10.1016/J.PBI.2004.03.007
Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport.
A. Fernie (2004)
10.1007/s00294-003-0408-1
Maize BMS cultured cell lines survive with massive plastid gene loss
A. B. Cahoon (2003)
10.1007/BF01293188
Quantitative fluorescence microscopy on dynamic changes of plastid nucleoids during wheat development
S. Miyamura (2005)
Tricircular mitochondrial genomes
JD Palmer (1986)
10.1105/tpc.105.037770
Arabidopsis Nitric Oxide Synthase1 Is Targeted to Mitochondria and Protects against Oxidative Damage and Dark-Induced Senescence
F. Guo (2005)
Ancient and essential: the assembly of ironsulfur clusters in plants The intermembrane space of plant mitochondria contains a DNase activity that may be involved in programmed cell death
J Balk (2003)
10.1093/JEXBOT/52.356.513
Compartmentation of metabolism within mitochondria and plastids.
C. Bowsher (2001)
10.1104/pp.108.128439
High Glycolate Oxidase Activity Is Required for Survival of Maize in Normal Air1[OA]
I. Zelitch (2008)
10.1007/s00606-007-0608-0
An update on chloroplast genomes
V. Ravi (2007)
10.1006/ANBO.1993.1097
Flow Cytometric Determination of Nuclear Replication Stage in Seed Tissues
R. Bino (1993)
10.1002/BIES.950060608
Why do chloroplasts and mitochondria contain so many copies of their genome?
A. Bendich (1987)
10.1093/NAR/12.24.9249
The physical map and organisation of the mitochondrial genome from the fertile cytoplasm of maize.
D. Lonsdale (1984)
Planta
(2013)
10.1104/pp.105.060327
Mutational Decay and Age of Chloroplast and Mitochondrial Genomes Transferred Recently to Angiosperm Nuclear Chromosomes1[w]
C. Huang (2005)
10.1073/PNAS.0401077101
Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution.
S. Arimura (2004)
10.1128/MCB.01357-08
Dynamic Compartmentalization of Base Excision Repair Proteins in Response to Nuclear and Mitochondrial Oxidative Stress
Lyra M Griffiths (2008)
10.1007/BF00326439
Investigation of plant organellar DNAs by pulsed-field gel electrophoresis
S. Backert (2004)
10.1186/1471-2229-9-3
A multiple-method approach reveals a declining amount of chloroplast DNA during development in Arabidopsis
B. Rowan (2008)
10.1016/j.mito.2009.03.003
DNA extraction procedures meaningfully influence qPCR-based mtDNA copy number determination.
W. Guo (2009)
10.1007/BF02668342
Complete nucleotide sequence of the mitochondrial DNA from a liverwort,Marchantia polymorpha
K. Oda (2007)
10.1146/annurev.arplant.59.032607.092915
Plastid evolution.
S. Gould (2008)
10.1111/j.1365-313X.2010.04389.x
Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells.
Tobias Preuten (2010)
10.1034/J.1399-3054.2003.00055.X
Measurements of photosynthesis and respiration in plants.
S. Hunt (2003)
10.1007/BF00194444
Studies on the behavior of organelles and their nucleoids in the root apical meristem of Arabidopsis thaliana (L.) Col.
M. Fujie (2004)
10.1093/NAR/14.14.5651
Tripartite mitochondrial genome of spinach: physical structure, mitochondrial gene mapping, and locations of transposed chloroplast DNA sequences.
D. Stern (1986)
10.1007/s00294-011-0342-6
Distinguishing authentic mitochondrial and plastid DNAs from similar DNA sequences in the nucleus using the polymerase chain reaction
R. A. Kumar (2011)



This paper is referenced by
10.1007/s00425-020-03349-7
Cytosine methylation of rice mitochondrial DNA from grain and leaf tissues
Kanagesswari Muniandy (2020)
10.3389/fpls.2020.00596
Reactive Oxygen Species, Antioxidant Agents, and DNA Damage in Developing Maize Mitochondria and Plastids
Diwaker Tripathi (2020)
10.1002/9781118647110.CH14
Ploidy Variation of the Nuclear, Chloroplast, and Mitochondrial Genomes in Somatic Cells
Xiujun Li (2017)
10.1093/jxb/eru359
Changes in DNA damage, molecular integrity, and copy number for plastid DNA and mitochondrial DNA during maize development
R. A. Kumar (2014)
10.1371/journal.pgen.1008373
The alternative reality of plant mitochondrial DNA: One ring does not rule them all
Alexander Kozik (2019)
10.1186/s12864-018-5254-0
Homologous recombination changes the context of Cytochrome b transcription in the mitochondrial genome of Silene vulgaris KRA
Helena Štorchová (2018)
10.1007/s00294-015-0482-1
Organellar genome copy number variation and integrity during moderate maturation of roots and leaves of maize seedlings
Jin Ma (2015)
10.1038/ncomms3247
A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis.
T. Hirayama (2013)
10.1002/bies.201400052
Unique features of DNA replication in mitochondria: A functional and evolutionary perspective
I. Holt (2014)
10.1201/B19543-7
Molecular biology of mitochondria: Genome, transcriptome, and proteome
Muhammad Hameed (2016)
Changes in molecular integrity of chloroplast DNA and mitochondrial DNA in maize
R. A. Kumar (2014)
10.1586/erv.12.150
Hepatitis B core–based virus–like particles to present heterologous epitopes
K. Roose (2013)
10.3390/plants8100358
Plant Organelle Genome Replication
Stewart A. Morley (2019)
10.1101/422808
Homologous recombination changes the context of Cytochrome b transcription in the mitochondrial genome of Silene vulgaris KRA
H. Štorchová (2018)
10.1093/jxb/erv298
Implications of mutation of organelle genomes for organelle function and evolution.
J. Raven (2015)
10.1007/s10577-013-9349-9
DNA abandonment and the mechanisms of uniparental inheritance of mitochondria and chloroplasts
A. Bendich (2013)
10.2741/4531
Plant mitochondrial DNA.
Stewart A. Morley (2017)
10.1038/s41598-019-45244-6
Replication fork rescue in mammalian mitochondria
R. Torregrosa-Muñumer (2019)
10.1016/j.mito.2014.03.008
Minireview: DNA replication in plant mitochondria.
J. Cupp (2014)
10.1007/s00425-015-2253-0
Molecular integrity of chloroplast DNA and mitochondrial DNA in mesophyll and bundle sheath cells of maize
Rachana A. Kumar (2015)
10.3389/fpls.2015.00883
DNA maintenance in plastids and mitochondria of plants
D. J. Oldenburg (2015)
10.1016/j.it.2017.07.012
DNA Sensing across the Tree of Life.
S. Gallucci (2017)
Semantic Scholar Logo Some data provided by SemanticScholar