Disrupting Autophagy Restores Peroxisome Function to an
Arabidopsis lon2 Mutant and Reveals a Role for the LON2
Protease in Peroxisomal Matrix Protein Degradation
Lisa M. Farmer,1Mauro A. Rinaldi, Pierce G. Young, Charles H. Danan, Sarah E. Burkhart, and Bonnie Bartel2
Department of Biochemistry and Cell Biology, Rice University, Houston, Texas 77005
Peroxisomes house critical metabolic reactions that are essential for seedling development. As seedlings mature, metabolic
requirements change, and peroxisomal contents are remodeled. The resident peroxisomal protease LON2 is positioned to
degrade obsolete or damaged peroxisomal proteins, but data supporting such a role in plants have remained elusive.
Arabidopsis thaliana lon2 mutants display defects in peroxisomal metabolism and matrix protein import but appear to
degrade matrix proteins normally. To elucidate LON2 functions, we executed a forward-genetic screen for lon2 suppressors,
which revealed multiple mutations in key autophagy genes. Disabling core autophagy-related gene (ATG) products prevents
autophagy, a process through which cytosolic constituents, including organelles, can be targeted for vacuolar degradation.
We found that atg2, atg3, and atg7 mutations suppressed lon2 defects in auxin metabolism and matrix protein processing and
rescued the abnormally large size and small number of lon2 peroxisomes. Moreover, analysis of lon2 atg mutants uncovered
an apparent role for LON2 in matrix protein turnover. Our data suggest that LON2 facilitates matrix protein degradation during
peroxisome content remodeling, provide evidence for the existence of pexophagy in plants, and indicate that peroxisome
destruction via autophagy is enhanced when LON2 is absent.
Peroxisomes are single membrane–bound organelles that com-
partmentalize certain oxidative reactions in eukaryotes, including
fatty acid b-oxidation and hydrogen peroxide metabolism (re-
viewed in Hu et al., 2012). Peroxisomal proteins are imported
into the organelle from the cytosol; defects in human peroxisomal
biogenesis underlie the Zellweger syndrome spectrum disorders,
which often are fatal (reviewed in Wanders and Waterham, 2005).
Plant peroxisomes also are essential (reviewed in Hu et al.,
2012); viable plant mutants lacking peroxisomes have not been
Peroxisome formation and maintenance requires membrane
recruitment, matrix protein import, organelle division, and dis-
tribution in daughter cells. Peroxisome biogenesis in yeast
requires more than 30 peroxin (PEX) genes; about half of these
are conserved in plants and mammals (reviewed in Hu et al.,
2012; Nagotu et al., 2012). PEX5 and PEX7 are receptors that
translocate matrix proteins into peroxisomes by binding cargo
with peroxisome-targeting signals (PTSs) and docking with the
PEX13 and PEX14 membrane peroxins (Nagotu et al., 2012).
PEX5 recognizes proteins containing a PTS1 (McCollum et al.,
1993; Van der Leij et al., 1993), a variant of a C-terminal Ser-Lys-
Leu (SKL-COOH) motif. PEX7 recognizes proteins bearing a
PTS2 (Marzioch et al., 1994), a nine–amino acid sequence em-
bedded in an ;30–amino acid N-terminal presequence. This
presequence is removed upon peroxisome import in mammals
and plants (Swinkels et al., 1991; Helm et al., 2007). After cargo
translocation into the organelle, PEX5 and PEX7 are returned to
the cytosol for reuse (Collins et al., 2000; Dammai and Subramani,
2001; Nair et al., 2004). PEX5 recycling requires the ubiquitin-
conjugating enzyme PEX4, which is tethered to the peroxisome
membrane by PEX22 (Collins et al., 2000; Zolman et al., 2005) and
assisted by a complex of membrane peroxins with ubiquitin-
protein ligase activity (Platta et al., 2009; Kaur et al., 2013).
In young seedlings, peroxisomes house fatty acid b-oxidation
and the glyoxylate cycle (reviewed in Eastmond and Graham,
2001), which allow utilization of storage lipids for energy and
fixed carbon before photosynthesis is established. Peroxisome-
defective Arabidopsis thaliana mutants therefore often require
external fixed carbon for normal development (Hayashi et al.,
1998; Zolman et al., 2000). Peroxisomes also metabolize the
protoauxin indole-3-butyric acid (IBA) (reviewed in Strader and
Bartel, 2011) into the active auxin indole-3-acetic acid (IAA),
which plays multiple critical roles in development (reviewed in
Woodward and Bartel, 2005b). Mutants with dysfunctional per-
oxisomes often display impaired IBA-to-IAA conversion (Strader
et al., 2010) and dampened IBA responsiveness (Zolman et al.,
2000). IBA resistance provides an indirect measure of peroxi-
some function that facilitates the isolation and characterization
of peroxisome-defective mutants (Zolman et al., 2000, 2005;
Zolman and Bartel, 2004; Woodward and Bartel, 2005a; Ramón
and Bartel, 2010; Ratzel et al., 2011).
As seedlings establish photosynthesis several days after ger-
mination, peroxisomes are remodeled, photorespiration enzymes
1Current address: Department of Pediatrics, USDA/Agricultural Re-
search Service Children’s Nutrition Research Center, Baylor College of
Medicine, Houston, TX 77030.
2Address correspondence to email@example.com.
The author responsible for distribution of materials integral to the findings
presented in this article in accordance with the policy described in the
Instructions for Authors (www.plantcell.org) is: Bonnie Bartel (bartel@
CSome figures in this article are displayed in color online but in black and
white in the print edition.
WOnline version contains Web-only data.
The Plant Cell, Vol. 25: 4085–4100, October 2013, www.plantcell.org ã 2013 American Society of Plant Biologists. All rights reserved.
like hydroxypyruvate reductase (HPR) are synthesized, and ob-
solete glyoxylate cycle enzymes, such as isocitrate lyase (ICL)
and malate synthase (MLS), are degraded. Immunolabeling
experiments in greening cucurbit cotyledons directly demon-
strate the presence of both photorespiration enzymes and
glyoxylate cycle enzymes in the same peroxisomes (Titus and
Becker, 1985; Nishimura et al., 1986; Sautter, 1986). Moreover,
MLS is stable following in vitro import into early pumpkin
(Cucurbita sp Amakuri Nankin) seedling peroxisomes but de-
graded after import into transitional peroxisomes (Mori and
Nishimura, 1989). These data provide support for the one-
population hypothesis, in which individual peroxisomal proteins
are degraded and new enzymes are imported into existing
peroxisomes during seedling maturation, rather than a two-
population hypothesis in which entire peroxisomes are degraded
and resynthesized with new content during developmental tran-
sitions (reviewed in Nishimura et al., 1996).
Although glyoxylate cycle enzymes and photorespiration
enzymes have not been directly colocalized in Arabidopsis
peroxisomes, these enzymes are present together in cotyledons
during the ;2-d window during seedling development when ICL
and MLS are degraded and HPR begins accumulating (Lingard
et al., 2009). Peroxisome entry is a prerequisite for efficient ICL
and MLS degradation; pex mutants with matrix protein import
defects stabilize ICL and MLS (Lingard et al., 2009; Burkhart
et al., 2013). Moreover, PEX4 and PEX22 promote ICL and MLS
turnover, hinting at a role for ubiquitination in matrix protein
degradation (Zolman et al., 2005; Lingard et al., 2009). However,
because PEX4 and PEX22 also are implicated in PEX5 recycling
and thus indirectly promote matrix protein import, this finding
does not provide a definitive mechanism for matrix protein
Several peroxisomal proteases have been examined for pos-
sible matrix protein degradation roles (Lingard and Bartel, 2009).
LON proteases were first characterized in bacteria (reviewed
in Tsilibaris et al., 2006) and contain an N-terminal substrate
binding domain, a central ATPase domain containing Walker A
and B ATP-binding motifs, and a C-terminal proteolytic domain
containing a Ser-Lys catalytic dyad (Tsilibaris et al., 2006). LON
proteases are predicted to form ring-shaped oligomers and
often degrade misfolded proteins (Tsilibaris et al., 2006).
Eukaryotic LON isoforms are found in mitochondria, chloro-
plasts, and peroxisomes (Kikuchi et al., 2004; Ostersetzer
et al., 2007; Lingard and Bartel, 2009). The peroxisomal Lon
from the methylotrophic yeast Hansenula polymorpha promotes
degradation of misfolded peroxisomally targeted dihydrofolate
reductase (Aksam et al., 2007), and in Penicillium chrysogenum,
peroxisomal Lon degrades oxidatively damaged catalase-
peroxidase (Bartoszewska et al., 2012). By contrast, mammalian
cells expressing a dominant-negative form of rat liver peroxi-
somal Lon mislocalize catalase to the cytosol (Omi et al.,
2008), indicating that peroxisomal LON function somehow
promotes matrix protein import. Arabidopsis encodes four LON
isoforms; LON2 is the only isoform bearing a canonical PTS1
and localized in peroxisomes (Ostersetzer et al., 2007; Eubel
et al., 2008; Reumann et al., 2009). All examined Arabidopsis
lon2 alleles are resistant to IBA-induced lateral root formation
but respond normally to auxins not requiring b-oxidation (Lingard
and Bartel, 2009; Burkhart et al., 2013), suggesting reduced
IBA-to-IAA conversion. Additionally, lon2 mutants display age-
dependent defects in PTS2 processing that are accompanied
by defects in peroxisomal matrix protein import (Lingard and
Bartel, 2009; Burkhart et al., 2013), indicating that LON2 is
necessary for sustained import of matrix proteins. This age-
dependent defect in matrix protein import contrasts with import
defects in pex14 mutants, which appear less severe as seedlings
age (Hayashi et al., 2000; Monroe-Augustus et al., 2011). In spite
of these defects in peroxisome physiology, disrupting Arabidopsis
LON2 does not appear to result in matrix protein stabilization
(Lingard and Bartel, 2009; Burkhart et al., 2013).
A second peroxisomal protease that has been tested for a role
in Arabidopsis matrix protein degradation is DEG15. DEG15
processes PTS2 proteins into their mature forms by removing
the PTS2-containing N-terminal region (Helm et al., 2007;
Schuhmann et al., 2008), but DEG15 is not required for ICL or
MLS degradation (Lingard and Bartel, 2009). Similarly, the per-
oxisomal M16 metalloprotease PXM16 is not required for deg-
radation of glyoxylate cycle enzymes; pxm16 and lon2 pxm16
mutants efficiently degrade ICL and MLS (Lingard and Bartel,
Beyond possible protease involvement in degrading individual
peroxisomal matrix proteins, yeast and mammals can degrade
peroxisomes using a specialized form of autophagy termed
pexophagy. Interestingly, Aspergillus nidulans ICL appears to be
degraded via pexophagy when cells are moved from fatty acid
to Glc carbon sources (Amor et al., 2000). Autophagy functions
in bulk degradation and recycling of cytosolic constituents, of-
ten in response to nutrient limitation or other stresses (reviewed
in Bassham, 2007; Xie and Klionsky, 2007; Reumann et al.,
2010; Li and Vierstra, 2012). Preautophagosomal structures are
formed by a subset of the AUTOPHAGY-RELATED (ATG) pro-
teins and assist an isolation membrane in engulfing cytoplasmic
constituents in autophagosomes. Autophagosomes can envelop
diverse substrates, including ribosomes, organelles, and protein
aggregates (reviewed in Xie and Klionsky, 2007; Li and Vierstra,
2012). Mature autophagosomes are delivered to the lytic vacuole
by fusion of the outer autophagosome membrane with the vac-
uolar membrane. Once in the vacuole, the inner membrane is
dissolved, and autophagosome contents are degraded by vacu-
olar hydrolases. Although the core autophagy machinery is con-
served in plants (reviewed in Bassham, 2007; Reumann et al.,
2010; Li and Vierstra, 2012), it is unclear whether peroxisome
turnover by pexophagy occurs in plants.
We undertook a forward-genetic screen for lon2 suppressors
to elucidate the molecular functions and targets of LON2 in
Arabidopsis. We isolated multiple alleles of several pivotal ATG
genes that suppressed the suite of lon2 physiological and mo-
lecular defects. At the same time, disrupting autophagy revealed
an additional molecular defect in lon2; lon2 atg double mutants
failed to degrade obsolete glyoxylate cycle enzymes in a timely
fashion during seedling development. Our results imply that
LON2 normally functions in the removal of obsolete matrix
proteins during development. Moreover, the absence of LON2
accelerates pexophagy, which degrades peroxisomes that
otherwise would carry out important metabolic functions in de-
4086The Plant Cell
Isolating Suppressors of lon2 Defects
Because of the unusual assortment of defects in peroxisome
physiology that result when Arabidopsis LON2 is mutated, we
sought to identify LON2 regulators or substrates among LON2
genetic interactors. We screened for mutations that suppressed
the IBA resistance and PTS2-processing defects of lon2-2,
which contains a T-DNA insertion in the last exon of LON2 that
would remove the PTS1 from the protein and prevent its import
into the peroxisome (Lingard and Bartel, 2009). We mutagenized
lon2-2 seeds carrying a cauliflower mosaic virus 35S promoter–
driven version of green fluorescent protein (GFP) bearing an
N-terminal PTS2 peptide (35S:PTS2-GFP) (Woodward and
Bartel, 2005a) and screened ;80,000 M2 seedlings for sup-
pressors in a two-part screen. First, we identified M2 seedlings
that produced approximately wild-type numbers of lateral roots
in the presence of IBA, thereby rescuing the lon2-2 resistance to
IBA-induced lateral root formation. Approximately 800 putative
mutants were transferred to soil and allowed to self-fertilize, and
surviving M3 progeny were rescreened for IBA sensitivity. Next,
the 61 suppressors displaying the most robust IBA sensitivity
were examined by immunoblotting for suppression of the lon2
PTS2-processing defect, revealing nine strong suppressors of
both lon2 phenotypes from eight different M1 pools: 1-1, 4-114,
5-49, 8-8, 11-10, 13-3, 14-22, 14-36, and 16-24. Whereas 8-d-
old lon2 seedlings rarely made a lateral root after growth on 10 mM
IBA, IBA-induced lateral root numbers were comparable to
those of the wild type in these suppressors (Figure 1A), sug-
gesting rescued IBA-to-IAA conversion. Additionally, the sup-
pressors fully restored the ability of lon2-2 to process the PTS2
protein peroxisomal malate dehydrogenase (PMDH) from its
precursor into its mature form (Figure 1B), suggesting that these
suppressors also rescued the lon2-2 peroxisomal matrix protein
Mutations in the Autophagy Gene ATG7 Suppress
We used recombination mapping to localize the causal lesions in
four suppressors (1-1, 4-114, 5-49, and 16-24) to the bottom of
chromosome 5 between At5g42590 and At5g54950, near the
LON2 locus (At5g47040) (Figure 2A). This linkage complicated
our ability to identify the causal lesions by traditional mapping
methods. Therefore, we used whole-genome sequencing of
backcrossed suppressor lines to identify mutations in three
suppressors (4-114, 5-49, and 16-24). Among the homozygous
mutations present in these suppressors (Figures 3A to 3C; see
Supplemental Data Set 1 online), each carried an independent
mutation in ATG7 (At5g45900; Figure 2B). In addition, we
identified atg7 lesions in the 1-1 and 8-8 suppressors (Figure 2B)
following PCR amplification and sequencing of ATG7 genomic
DNA from these mutants (see Supplemental Table 1 online). All
five atg7 alleles identified in our lon2 suppressors are expected
to impair ATG7 function; three were nonsense alleles, which we
renamed atg7-4 (suppressor 5-49; Gln-12 to stop), atg7-5
(suppressor 1-1; Trp-119 to stop), and atg7-6 (suppressor 8-8;
Trp-344 to stop), while two changed conserved Gly residues
(see Supplemental Figure 1 online) to Asp residues, which we
renamed atg7-7 (suppressor 16-24; Gly-247 to Asp) and atg7-8
(suppressor 4-114; Gly-286 to Asp).
ATG7 is a 697–amino acid ATP-dependent ubiquitin-activating
(E1)-like enzyme that activates two ubiquitin-like modifiers act-
ing in the autophagy conjugation pathway, resulting in ATG8
lipidation with phosphatidylethanolamine (PE). ATG8-PE in the
inner autophagosomal membrane docks via adaptor proteins
with cytosolic components to be engulfed, and ATG8-PE in the
outer membrane is tethered to the microtubule-based transport
machinery to allow autophagosome delivery to the vacuole (re-
viewed in Li and Vierstra, 2012). To determine whether blocking
autophagy affected peroxisome physiology, we compared the
IBA responsiveness and PTS2 processing in atg7 null mutants
to two lon2 alleles and our lon2-2 atg7 suppressors. The atg7-2
and atg7-3 null alleles harbor T-DNA insertions in the 7th exon
and abolish autophagy (Hofius et al., 2009; Chung et al., 2010;
Lai et al., 2011; Wang et al., 2011). lon2-4 carries a splice site
mutation at the 39 end of intron 3 and generates a premature
stop codon, likely truncating the protein. Both atg7-2 and atg7-3
single mutants responded to IBA similarly to the wild type and
Figure 1. Suppressors of lon2 Are IBA Sensitive and Lack PTS2-
(A) Number of lateral roots per millimeter root length of 8-d-old wild-type
(Wt) 35S:PTS2-GFP, lon2-2 35S:PTS2-GFP, and lon2-2 suppressor
seedlings (M5 progeny of original isolates) that were grown under yellow-
filtered light on Suc-supplemented medium for 4 d and then transferred
to Suc-supplemented medium with or without 10 mM IBA for an addi-
tional 4 d. Error bars show SD (n $ 12).
(B) Extracts from 8-d-old wild-type 35S:PTS2-GFP, lon2-2 35S:PTS2-
GFP, and each suppressor line grown in yellow light on Suc- and IBA-
supplemented medium were processed for immunoblotting and serially
probed with antibodies raised against the indicated proteins. PMDH is
expressed as a precursor (p); the PTS2 region is cleaved to the mature
(m) form in the peroxisome. Protein loading was monitored by probing
with antibodies against HSC70. The positions of molecular mass mark-
ers (in kilodaltons) are shown on the right.
[See online article for color version of this figure.]
Peroxisomes Are Regulated by Autophagy4087
Platta, H.W., El Magraoui, F., Bäumer, B.E., Schlee, D., Girzalsky, W.,
and Erdmann, R. (2009). Pex2 and pex12 function as protein-ubiquitin
ligases in peroxisomal protein import. Mol. Cell. Biol. 29: 5505–5516.
Pracharoenwattana, I., Cornah, J.E., and Smith, S.M. (2007).
Arabidopsis peroxisomal malate dehydrogenase functions in b-oxidation
but not in the glyoxylate cycle. Plant J. 50: 381–390.
Ramón, N.M., and Bartel, B. (2010). Interdependence of the
peroxisome-targeting receptors in Arabidopsis thaliana: PEX7
facilitates PEX5 accumulation and import of PTS1 cargo into
peroxisomes. Mol. Biol. Cell 21: 1263–1271.
Ratzel, S.E., Lingard, M.J., Woodward, A.W., and Bartel, B. (2011).
Reducing PEX13 expression ameliorates physiological defects of
late-acting peroxin mutants. Traffic 12: 121–134.
Reumann, S., Quan, S., Aung, K., Yang, P., Manandhar-Shrestha,
K., Holbrook, D., Linka, N., Switzenberg, R., Wilkerson, C.G.,
Weber, A.P., Olsen, L.J., and Hu, J. (2009). In-depth proteome
analysis of Arabidopsis leaf peroxisomes combined with in vivo
subcellular targeting verification indicates novel metabolic and
regulatory functions of peroxisomes. Plant Physiol. 150: 125–143.
Reumann, S., Voitsekhovskaja, O., and Lillo, C. (2010). From signal
transduction to autophagy of plant cell organelles: Lessons from yeast
and mammals and plant-specific features. Protoplasma 247: 233–256.
Sautter, C. (1986). Microbody transition in greening watermelon
cotyledons. Double immunocytochemical labeling of isocitrate
lyase and hydroxypyruvate reductase. Planta 167: 491–503.
Schuhmann, H., Huesgen, P.F., Gietl, C., and Adamska, I. (2008).
The DEG15 serine protease cleaves peroxisomal targeting signal
2-containing proteins in Arabidopsis. Plant Physiol. 148: 1847–1856.
photochemistry in culture media by long-pass light filters alters
growth of cultured tissues. Plant Physiol. 93: 1365–1369.
Strader, L.C., and Bartel, B. (2011). Transport and metabolism of the
endogenous auxin precursor indole-3-butyric acid. Mol. Plant 4: 477–486.
Strader, L.C., Culler, A.H., Cohen, J.D., and Bartel, B. (2010). Conversion
of endogenous indole-3-butyric acid to indole-3-acetic acid drives cell
expansion in Arabidopsis seedlings. Plant Physiol. 153: 1577–1586.
Suzuki, K., Kubota, Y., Sekito, T., and Ohsumi, Y. (2007). Hierarchy
of Atg proteins in pre-autophagosomal structure organization.
Genes Cells 12: 209–218.
Svenning, S., Lamark, T., Krause, K., and Johansen, T. (2011). Plant NBR1
isa selective autophagysubstrate anda functionalhybridof themammalian
autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7: 993–1010.
Swinkels, B.W., Gould, S.J., Bodnar, A.G., Rachubinski, R.A., and
Subramani, S. (1991). A novel, cleavable peroxisomal targeting
signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase.
EMBO J. 10: 3255–3262.
Thompson, A.R., Doelling, J.H., Suttangkakul, A., and Vierstra, R.D.
(2005). Autophagic nutrientrecycling in Arabidopsis directed by the ATG8
and ATG12 conjugation pathways. Plant Physiol. 138: 2097–2110.
Till, A., Lakhani, R., Burnett, S.F., and Subramani, S. (2012).
Pexophagy: The selective degradation of peroxisomes. Int. J. Cell
Biol. 2012: 512721.
Titus, D.E., and Becker, W.M. (1985). Investigation of the glyoxysome-
peroxisome transition in germinating cucumber cotyledons using double-
label immunoelectron microscopy. J. Cell Biol. 101: 1288–1299.
Tsilibaris, V., Maenhaut-Michel, G., and Van Melderen, L. (2006).
Biological roles of the Lon ATP-dependent protease. Res. Microbiol.
Van der Leij, I., Franse, M.M., Elgersma, Y., Distel, B., and Tabak,
H.F. (1993). PAS10 is a tetratricopeptide-repeat protein that is
essential for the import of most matrix proteins into peroxisomes of
Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 90: 11782–
van Zutphen, T., Veenhuis, M., and van der Klei, I.J. (2011).
Damaged peroxisomes are subject to rapid autophagic degradation
in the yeast Hansenula polymorpha. Autophagy 7: 863–872.
Wanders, R.J., and Waterham, H.R. (2005). Peroxisomal disorders I:
Biochemistry and genetics of peroxisome biogenesis disorders.
Clin. Genet. 67: 107–133.
Wang, Y., Nishimura, M.T., Zhao, T., and Tang, D. (2011). ATG2, an
autophagy-related protein, negatively affects powdery mildew
resistance and mildew-induced cell death in Arabidopsis. Plant J.
Woodward, A.W., and Bartel, B. (2005a). The Arabidopsis peroxisomal
targeting signal type 2 receptor PEX7 is necessary for peroxisome function
and dependent on PEX5. Mol. Biol. Cell 16: 573–583.
Woodward, A.W., and Bartel, B. (2005b). Auxin: Regulation, action,
and interaction. Ann. Bot. (Lond.) 95: 707–735.
Xie, Z., and Klionsky, D.J. (2007). Autophagosome formation: Core
machinery and adaptations. Nat. Cell Biol. 9: 1102–1109.
Xiong, Y., Contento, A.L., and Bassham, D.C. (2005). AtATG18a is
required for the formation of autophagosomes during nutrient stress
and senescence in Arabidopsis thaliana. Plant J. 42: 535–546.
Yamaguchi, M., Matoba, K., Sawada, R., Fujioka, Y., Nakatogawa,
H., Yamamoto, H., Kobashigawa, Y., Hoshida, H., Akada, R.,
Ohsumi, Y., Noda, N.N., and Inagaki, F. (2012). Noncanonical
recognition and UBL loading of distinct E2s by autophagy-essential
Atg7. Nat. Struct. Mol. Biol. 19: 1250–1256.
Yoshimoto, K., Jikumaru, Y., Kamiya, Y., Kusano, M., Consonni,
C., Panstruga, R., Ohsumi, Y., and Shirasu, K. (2009). Autophagy
negatively regulates cell death by controlling NPR1-dependent
salicylic acid signaling during senescence and the innate immune
response in Arabidopsis. Plant Cell 21: 2914–2927.
Zhang, X., and Hu, J. (2009). Two small protein families, DYNAMIN-
RELATED PROTEIN3 and FISSION1, are required for peroxisome
fission in Arabidopsis. Plant J. 57: 146–159.
Zhou, J., Wang, J., Cheng, Y., Chi, Y.J., Fan, B., Yu, J.Q., and Chen,
Z. (2013). NBR1-mediated selective autophagy targets insoluble
ubiquitinated protein aggregates in plant stress responses. PLoS
Genet. 9: e1003196.
Zientara-Rytter, K., Lukomska, J., Moniuszko, G., Gwozdecki, R.,
Surowiecki, P., Lewandowska, M., Liszewska, F., Wawrzy? nska,
A., and Sirko, A. (2011). Identification and functional analysis of
Joka2, a tobacco member of the family of selective autophagy
cargo receptors. Autophagy 7: 1145–1158.
Zolman, B.K., and Bartel, B. (2004). An Arabidopsis indole-3-butyric
acid-response mutant defective in PEROXIN6, an apparent ATPase
implicated in peroxisomal function. Proc. Natl. Acad. Sci. USA 101:
Zolman, B.K., Monroe-Augustus, M., Silva, I.D., and Bartel, B.
(2005). Identification and functional characterization of Arabidopsis
PEROXIN4 and the interacting protein PEROXIN22. Plant Cell 17:
Zolman, B.K., Yoder, A., and Bartel, B. (2000). Genetic analysis of
indole-3-butyric acid responses in Arabidopsis thaliana reveals four
mutant classes. Genetics 156: 1323–1337.
4100 The Plant Cell
; originally published online October 31, 2013; 2013;25;4085-4100
Lisa M. Farmer, Mauro A. Rinaldi, Pierce G. Young, Charles H. Danan, Sarah E. Burkhart and Bonnie
Role for the LON2 Protease in Peroxisomal Matrix Protein Degradation
Mutant and Reveals a
Disrupting Autophagy Restores Peroxisome Function to an
This information is current as of November 22, 2015
This article cites 96 articles, 51 of which can be accessed free at:
Sign up for eTOCs at:
Sign up for CiteTrack Alerts at:
is available at:
The Plant Cell
Subscription Information for
ADVANCING THE SCIENCE OF PLANT BIOLOGY
© American Society of Plant Biologists