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

The APG8/12-activating Enzyme APG7 Is Required For Proper Nutrient Recycling And Senescence In Arabidopsis Thaliana *

J. H. Doelling, J. Walker, E. M. Friedman, Allison R Thompson, R. Vierstra
Published 2002 · Medicine, Biology

Cite This
Download PDF
Analyze on Scholarcy
Share
The vacuole/lysosome serves an important recycling function during starvation and senescence in eukaryotes via a process called autophagy. Here bulk cytosolic constituents and organelles become sequestered in specialized autophagic vesicles, which then deliver their cargo to the vacuole for degradation. In yeasts, genetic screens have identified two novel post-translational modification pathways remarkably similar to ubiquitination that are required for autophagy. From searches of the Arabidopsisgenome, we have identified gene families encoding proteins related to both the APG8 and −12 polypeptide tags and orthologs for all components required for their attachment. A single APG7gene encodes the ATP-dependent activating enzyme that initiates both conjugation pathways. Phenotypic analysis of anAPG7 disruption indicates that it is not essential for normal growth and development in Arabidopsis. However, theapg7-1 mutant is hypersensitive to nutrient limiting conditions and displays premature leaf senescence. mRNAs for both APG7 and APG8 preferentially accumulate as leaves senesce, suggesting that both conjugation pathways are up-regulated during the senescence syndrome. These findings show that the APG8/12 conjugation pathways have been conserved in plants and may have important roles in autophagic recycling, especially during situations that require substantial nitrogen and carbon mobilization.
This paper references
10.1083/JCB.148.3.465
Apg9p/Cvt7p Is an Integral Membrane Protein Required for Transport Vesicle Formation in the Cvt and Autophagy Pathways
Takeshi Noda (2000)
10.1146/ANNUREV.BIOCHEM.67.1.425
The Ubiquitin System
A. Hershko (1998)
10.1006/BBRC.1995.1636
Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae.
T. Noda (1995)
10.1038/35044114
A ubiquitin-like system mediates protein lipidation
Yoshinobu Ichimura (2000)
10.1074/JBC.C000752200
The Human Homolog of Saccharomyces cerevisiae Apg7p Is a Protein-activating Enzyme for Multiple Substrates Including Human Apg12p, GATE-16, GABARAP, and MAP-LC3*
I. Tanida (2001)
10.1073/PNAS.77.1.428
Protein bodies of mung bean cotyledons as autophagic organelles.
W. van der Wilden (1980)
10.1146/ANNUREV.BIOCHEM.69.1.303
Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells.
J. Kim (2000)
10.1007/BF00042980
Regulation and expression of the multigene family coding light-harvesting chlorophyll a/b-binding proteins of photosystem II
D. E. Buetow (2004)
10.1126/SCIENCE.290.5497.1717
Autophagy as a regulated pathway of cellular degradation.
D. Klionsky (2000)
10.1023/A:1006323317890
Polypeptide tags, ubiquitous modifiers for plant protein regulation
R. Vierstra (2004)
10.1083/jcb.200105096
Cotyledon cells of Vigna mungo seedlings use at least two distinct autophagic machineries for degradation of starch granules and cellular components
K. Toyooka (2001)
10.1046/J.1365-313X.1999.00479.X
Structural and functional analysis of the six regulatory particle triple-A ATPase subunits from the Arabidopsis 26S proteasome.
H. Fu (1999)
10.1016/0962-8924(94)90069-8
Autophagy and related mechanisms of lysosome-mediated protein degradation.
W. Dunn (1994)
10.1016/S1360-1385(00)01655-1
Molecular aspects of leaf senescence.
B. Quirino (2000)
10.1105/tpc.010381
Cytokinin Growth Responses in Arabidopsis Involve the 26S Proteasome Subunit RPN12 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010381.
J. Smalle (2002)
10.1104/PP.69.1.98
Vacuolar localization of proteases and degradation of chloroplasts in mesophyll protoplasts from senescing primary wheat leaves.
V. A. Wittenbach (1982)
Uptake and apparent digestion of cytoplasmic organelles by protein bodies (protein storage vacuoles) in mung bean cotyledons.
E. Herman (1981)
10.1038/35056522
Ubiquitin and proteasomes: Molecular dissection of autophagy: two ubiquitin-like systems
Y. Ohsumi (2001)
10.1016/S1534-5807(01)00024-7
VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis.
E. Rojo (2001)
10.1038/16264
GABAA-receptor-associated protein links GABAA receptors and the cytoskeleton
H. Wang (1999)
10.1007/BF00039386
Proteolysis in plants: mechanisms and functions
R. Vierstra (2004)
10.1083/JCB.152.4.657
Dissection of Autophagosome Formation Using Apg5-Deficient Mouse Embryonic Stem Cells
N. Mizushima (2001)
10.1046/J.1365-313X.2001.01106.X
The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana.
J. H. Doelling (2001)
10.1073/PNAS.93.15.8145
Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport.
P. Krysan (1996)
10.1104/PP.116.2.605
Magnesium-Chelatase from Developing Pea Leaves: Characterization of a Soluble Extract from Chloroplasts and Resolution into Three Required Protein Fractions
R. Guo (1998)
10.1046/J.1365-313X.1998.00343.X
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
S. Clough (1998)
10.1093/NAR/25.17.3389
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
S. Altschul (1997)
10.1016/0014-5793(93)80398-E
Isolation and characterization of autophagy‐defective mutants of Saccharomyces cerevisiae
M. Tsukada (1993)
10.1083/JCB.147.2.435
Formation Process of Autophagosome Is Traced with Apg8/Aut7p in Yeast
T. Kirisako (1999)
10.1091/MBC.10.5.1337
Apg7p/Cvt2p is required for the cytoplasm-to-vacuole targeting, macroautophagy, and peroxisome degradation pathways.
J. Kim (1999)
10.1105/tpc.8.9.1465
Distinct classes of cdc2-related genes are differentially expressed during the cell division cycle in plants.
P. Fobert (1996)
10.1023/A:1005934428906
A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment
L. M. Weaver (2004)
10.1093/emboj/19.7.1494
GATE‐16, a membrane transport modulator, interacts with NSF and the Golgi v‐SNARE GOS‐28
Y. Sagiv (2000)
10.1074/JBC.M200385200
Human Apg3p/Aut1p Homologue Is an Authentic E2 Enzyme for Multiple Substrates, GATE-16, GABARAP, and MAP-LC3, and Facilitates the Conjugation of hApg12p to hApg5p*
I. Tanida (2002)
10.1046/J.1365-313X.1998.00210.X
Specific accumulation of GFP in a non-acidic vacuolar compartment via a C-terminal propeptide-mediated sorting pathway.
G. P. Di Sansebastiano (1998)
10.1093/emboj/19.21.5720
LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing
Y. Kabeya (2000)
10.1105/tpc.10.5.685
Barley Aleurone Cells Contain Two Types of Vacuoles: Characterization of Lytic Organelles by Use of Fluorescent Probes
S. Swanson (1998)
10.1093/OXFORDJOURNALS.PCP.A078749
Changes in the Number and Size of Chloroplasts during Senescence of Primary Leaves of Wheat Grown under Different Conditions
K. Ono (1995)
10.1038/26506
A protein conjugation system essential for autophagy
N. Mizushima (1998)
10.1104/pp.111.4.1233
Autophagy in Tobacco Suspension-Cultured Cells in Response to Sucrose Starvation
Y. Moriyasu (1996)
10.1016/0926-6585(65)90170-6
Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol.
J. F. Wintermans (1965)
10.1074/JBC.273.51.33889
A New Protein Conjugation System in Human
N. Mizushima (1998)
10.1074/JBC.275.8.5845
The Itinerary of a Vesicle Component, Aut7p/Cvt5p, Terminates in the Yeast Vacuole via the Autophagy/Cvt Pathways*
W. Huang (2000)
Molecular organization of the 20S proteasome gene family from Arabidopsis thaliana.
H. Fu (1998)
10.1104/PP.126.1.78
Regeneration of a lytic central vacuole and of neutral peripheral vacuoles can be visualized by green fluorescent proteins targeted to either type of vacuoles.
G. P. Di Sansebastiano (2001)
10.1093/oxfordjournals.pcp.a029571
Identification of clp genes expressed in senescing Arabidopsis leaves.
K. Nakabayashi (1999)
10.1083/JCB.133.6.1251
Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates
S. Aubert (1996)
10.1083/JCB.131.3.591
Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway
T. M. Harding (1995)
10.1016/S1369-5266(00)00100-X
Protein degradation in signaling.
J. Callis (2000)
10.1091/MBC.10.5.1353
Glucose-induced autophagy of peroxisomes in Pichia pastoris requires a unique E1-like protein.
W. Yuan (1999)
10.1105/tpc.7.7.845
Regulation of Protein Degradation.
J. Callis (1995)
10.1093/OXFORDJOURNALS.PCP.A029190
Differential expression of CuZn- and Fe-superoxide dismutase genes of tobacco during development, oxidative stress, and hormonal treatments.
J. Kurepa (1997)



This paper is referenced by
10.1152/ajpheart.00713.2007
Lipid mediators of autophagy in stress-induced premature senescence of endothelial cells.
S. Patschan (2008)
10.4161/auto.7.10.16617
Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors
Katarzyna Zientara-Rytter (2011)
Identification of genetic regulators of longevity in dark-held detached Arabidopsis inflorescences : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Plant Biology, Massey University, Palmerston North, New Zealand.
R. Jibran (2014)
10.1104/pp.104.900125
ER-Derived Compartments Are Formed by Highly Regulated Processes and Have Special Functions in Plants
G. Galili (2004)
10.1105/tpc.18.00736
A Subsidiary Cell-Localized Glucose Transporter Promotes Stomatal Conductance and Photosynthesis
H. Wang (2019)
10.1007/s12229-011-9063-2
Flower Senescence-Strategies and Some Associated Events
Waseem Shahri (2011)
10.1371/journal.pone.0182591
SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana
Junmarie Soto-Burgos (2017)
10.1016/j.tplants.2018.02.010
Mitophagy: A Mechanism for Plant Growth and Survival.
Martyna Broda (2018)
10.1080/15548627.2015.1034407
Elucidating the composition and conservation of the autophagy pathway in photosynthetic eukaryotes
Adva Shemi (2015)
10.1093/aob/mcu041
SNARE VTI13 plays a unique role in endosomal trafficking pathways associated with the vacuole and is essential for cell wall organization and root hair growth in arabidopsis
Emily R. Larson (2014)
10.1111/j.1469-8137.2012.04084.x
Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis.
Anne Guiboileau (2012)
10.1371/journal.pone.0069847
Gene Expression Profiles Deciphering Leaf Senescence Variation between Early- and Late-Senescence Cotton Lines
Xiangqiang Kong (2013)
10.1016/j.febslet.2010.01.007
Autophagy in plants and phytopathogens
K. Yoshimoto (2010)
10.1111/J.1365-313X.2006.02979.X
Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings.
D. Osuna (2007)
10.1007/978-90-481-2863-1_16
Lipid Trafficking in Plant Photosynthetic Cells
J. Jouhet (2009)
10.1007/s00709-010-0190-0
From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features
S. Reumann (2010)
10.1016/j.jplph.2010.05.015
Differential gene expression in kernels and silks of maize lines with contrasting levels of ear rot resistance after Fusarium verticillioides infection.
A. Lanubile (2010)
10.1105/tpc.111.090993
The ATG1/ATG13 Protein Kinase Complex Is Both a Regulator and a Target of Autophagic Recycling in Arabidopsis[C][W]
Anongpat Suttangkakul (2011)
10.1111/j.1744-7909.2012.01178.x
What to eat: evidence for selective autophagy in plants.
Brice E. Floyd (2012)
10.1007/s11240-016-1070-x
Ectopic expression of an autophagy-associated MdATG7b gene from apple alters growth and tolerance to nutrient stress in Arabidopsis thaliana
P. Wang (2016)
10.1111/jipb.12941
Autophagy in plants: Physiological roles and post-translational regulation.
H. Qi (2020)
10.3390/plants4030573
Sulfite Oxidase Activity Is Essential for Normal Sulfur, Nitrogen and Carbon Metabolism in Tomato Leaves
G. Brychkova (2015)
10.1080/15548627.2015.1100356
Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition)
D. Klionsky (2016)
10.1016/J.SCIENTA.2013.10.038
Isolation and characterization of MdATG18a, a WD40-repeat AuTophaGy-related gene responsive to leaf senescence and abiotic stress in Malus
P. Wang (2014)
Regulators of autophagy in Leishmania major
K. L. Woods (2009)
10.1111/pce.12049
Evidence for contribution of autophagy to rubisco degradation during leaf senescence in Arabidopsis thaliana.
Y. Ono (2013)
Interaction of Arabidopsis AMSH proteins with ESCRT-III and their role in intracellular membrane trafficking
Anthi Katsiarimpa (2014)
10.4161/auto.5.4.8310
Autophagy regulates progression of programmed cell death during petal senescence in Japanese morning glory
Kenichi Shibuya (2009)
10.4161/auto.5629
Autophagy protein 6 (ATG6) is required for pollen germination in Arabidopsis thaliana
N. Harrison-Lowe (2008)
10.1016/S0070-2153(05)67002-0
The molecular and genetic control of leaf senescence and longevity in Arabidopsis.
P. O. Lim (2005)
Functions of CML24: A potential calcium sensor of Arabidopsis
Yu-Chang Tsai (2010)
Genetic and biochemical analyses of the Arabidopsis atToc90 protein
P. Lymperopoulos (2012)
See more
Semantic Scholar Logo Some data provided by SemanticScholar