The Proteasome Stress Regulon Is Controlled by a Pair of NAC … · 5 132 reported role for 26S proteasome levels in controlling cell size (Kurepa et al., 2009; Sonoda et 133 al.,
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THE PROTEASOME STRESS REGULON IS CONTROLLED BY A PAIR OF 6
NAC TRANSCRIPTION FACTORS IN ARABIDOPSIS 7
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Running Title: Transcriptional Regulation of Proteotoxic Stress 12
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By Nicholas P. Gladman1, Richard S. Marshall1,2, Kwang-Hee Lee1, and Richard D. 16
Vierstra1,2 17
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20 1Department of Genetics, University of Wisconsin, Madison, WI 53706 USA 21
2Department of Biology, Washington University in St. Louis, St. Louis, MO 63130 USA 22
Purification of the Arabidopsis 26S proteasome: biochemical and molecular analyses 1044
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Zhou, J., Wang, J., Cheng, Y., Chi, Y.J., Fan, B., Yu, J.Q., and Chen, Z. (2013). NBR1-1048
mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant 1049
stress responses. PLoS Genet. 9: e1003196. 1050
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Figure 1. Both the Proteasome Inhibitor MG132 and Proteasome Mutants Increase the
Accumulation of Proteasome Components and Ub Conjugates in Arabidopsis.
Wild-type seedlings treated with 100 µM MG132 or untreated rpn10-1 and rpn12a-1 seedlings
were grown for 5 d. Total extracts were probed by immunoblotting with the indicated antibodies,
using anti-histone H3 antibodies to verify near equal protein loading.
(A) Levels of individual subunits of the proteasome. The open and closed arrowheads identify
the unprocessed and processed forms of the β1 subunit PBA1.
(B) Levels of Ub conjugates. Closed arrowheads locate free Ub and poly-Ub chains assembled
with varying numbers of Ub monomers. Bracket locates high molecular mass Ub conjugates.
Figure 2. Expression of Arabidopsis Proteasome Genes is Up-Regulated in Response to
Proteasome Stress.
(A) Expression of 26S proteasome subunit genes following proteasome inhibition with MG132
or in rpn10-1 or rpn12a-1 mutant backgrounds that compromise assembly. Total RNA from 5-d-
old seedlings, either untreated or treated for 3 and 24 hr with 100 µM MG132, was subjected to
qRT-PCR. The expression values were calculated using the ACT2 transcript as a reference
and normalized to those from untreated wild-type (WT) seedlings. Each bar represents the
average of at least three biological replicates (± SD).
(B) Effects of MG132 on the expression of proteasome promoter:GUS transgenes. Transgenic
WT seedlings expressing the fusions were grown for 3 d, treated for 1 d with 100 µM MG132,
and then incubated overnight with the X-Gluc substrate.
(C) Quantitative measure of proteasome promoter:GUS expression following MG132 treatment.
Ten-d-old seedlings were incubated overnight with or without 100 µM MG132 and homogenized,
and the GUS activity in the resulting cell extracts was assayed using the MUG substrate. Each
bar represents the analysis of at least 30 independent T1 lines, each assayed in triplicate (± SD).
The data in panels B and C for the RPT2a and RPT2b promoter-GUS fusions were reported
previously and are included here for comparison (Lee et al., 2011).
Figure 3. Characterization of the Proteasome-Stress Regulon (PSR) in Arabidopsis.
(A) Venn diagrams of transcripts that were differentially expressed significantly (p-value < 0.01,
FDR < 0.05) under three proteasome-stress conditions: wild-type (WT) after a 3-hr treatment
with 100 µM MG132, and the rpn10-1 and rpn12a-1 genetic backgrounds. The shared 119 up-
regulated (including RPN10 and RPN12a) and 33 down-regulated genes determined by edgeR
analysis comprise the PSR.
(B) A heat map of the PSR for the three treatments ranked by the fold-change in expression
obtained with the MG132-treated seedlings. The brackets indicate genes with more or less than
a two-fold increase (log2(fold-change) = 1) in expression as compared to WT. Categories of
enriched gene classes are indicated (TFs = transcription factors). See Supplemental Dataset 3
online for the full list.
(C) Expression change heat maps of 26S proteasome subunit and assembly factor genes after
proteasome stress as compared to untreated WT. EST values obtained from The Arabidopsis
Information Resource (TAIR v10) are listed.
Figure 4. Description of the MG132 Up-regulated Gene Interaction and Co-expression
Network.
(A) An interaction and co-expression map of Arabidopsis proteins encoded by MG132 up-
regulated genes. The connections reflect known protein/protein interactions and co-expression
data collected from the STRING database for the available 275 of the total 336 significantly up-
regulated genes (≥ 2-fold up as compared to untreated wild type) after a 3-hr exposure to 100
µM MG132. Classifications of major functional groups in the network are highlighted. Members
of the NAC transcription factor family are in red. Portions of the map enclosed by the dashed
lines are statistically enriched for genes with the denoted functional categories (DAVID, p-value
<0.01). If available, specific gene names were used instead of the TAIR locus identifier. See
Supplemental Dataset 3 for the full list.
(B) Members of the network that contain the consensus PRCE or MDM cis motifs within their
promoter regions (motif-containing gene nodes are in red).
(C) Sequence descriptions of the PRCE and MDM sequences as determined by MEME.
(D) Interactome maps focusing on the statistically significant central hubs present in the
proteasome, chaperone, and ‘detoxification’ clusters as determined by MCODE analysis, and
colored based on the presence of PRCE and/or MDM sequences.
Figure 5. NAC53 and NAC78 Are Closely Related and Physically Interact.
(A) A Bayesian phylogenetic tree of all 109 NAC proteins in Arabidopsis rooted to a
Physcomitrella patens NAC protein (gi_168025227). Nodes highlighted in red indicate the NTL
subclass with a predicted transmembrane-spanning motif. The same tree with the included
names for each protein is in Supplementary Figure 6 and a text file of the alignment used is
presented as Supplemental Data Set 5.
(B) Y2H assays showing that NAC53 and NAC78 homo- and hetero-dimerize. The full-length
proteins were expressed as N-terminal fusions with either the GAL4 activating (AD) or binding
(BD) domains. Shown are cells grown on selective medium lacking Leu and Trp, or lacking Leu,
Trp and His, and containing 50 mM 3-AT.
(C) Bimolecular fluorescence complementation (BiFC) analysis showing that NAC53 and
NAC78 homo- and hetero-dimerize in planta and partially localize to the nucleus. N.
benthamiana leaf epidermal cells were co-infiltrated with plasmids expressing the N- and C-
terminal fragments of YFP (nYFP and cYFP, respectively) fused to the N-terminus of NAC53 or
NAC78. Shown are reconstituted BiFC signals, as detected by confocal fluorescence
microscopy of leaf epidermal cells 36 hr after infiltration, along with DAPI staining of nuclei
(white arrowheads) and a bright field (BF) image of the cells. Scale bar = 10 µm.
(D) Y2H assays testing interactions between NAC53 and NAC78 and other NAC proteins within
the PSR. The assays were conducted as in panel (B) with the selective medium lacking Leu,
Trp and His, and containing 25 mM 3-AT.
Figure 6. NAC78 Overexpression Induces the Expression of Some Arabidopsis PSR
Genes.
Up-regulation of proteasome subunit and other PSR genes in seedlings expressing NAC78 from
an estradiol-inducible promoter. Total RNA from 6-d-old wild type (WT) and pEST:NAC78
seedlings incubated for 24 hr with or without 10 µM β-estradiol were subjected to RT-qPCR.
The expression values were calculated using ACT2 (black) and PP2A (grey) transcripts as
references and normalized to those obtained from untreated wild-type (WT) seedlings. Bars
represent the average of at least three biological replicates (± SD), each measured in triplicate.
Asterisks indicate significant differences between pEST:NAC78 and WT based on Student’s t-
test (p <0.05). Dashed lines indicate the average values for untreated WT seedlings.
Figure 7. Generation of Mutants Impacting NAC53 and NAC78.
(A) Diagrams of the NAC53 and NAC78 transcribed regions. Boxes represent coding regions
(colored) and predicted UTRs (white). The blue and orange boxes identify the DNA-binding
NAM domains and the predicted membrane-spanning regions, respectively. Lines represent
introns. The positions of the T-DNA insertions are indicated by the red triangles; their exact
locations in the amino acid sequences are indicated in Supplemental Figure 8.
(B) RT-PCR analysis of the NAC53 and NAC78 transcripts in the single and double mutants.
Total RNA isolated from wild-type (WT) or homozygous mutant plants was subjected to RT-PCR
using the primer pairs indicated in (A). RT-PCR with primers specific for ACT2 was included to
confirm analysis of equal amounts of cDNA.
Figure 8. Loss of NAC53 and NAC78 Compromises Activation of the Proteasome Stress
Regulon.
(A) RT-qPCR analysis of representative PSR mRNAs during proteasome stress. Total RNA
was extracted from 6-d-old wild-type (WT) and nac mutant seedlings after a 24-hr incubation
with or without 100 µM MG132. Transcript abundance was determined via RT-qPCR using the
ACT2 (black) and PP2A (grey) mRNAs as references and normalized to those obtained from
untreated wild-type (WT) seedlings. Bars represent the average of at least three biological
replicates (± SD), each measured in triplicate. Asterisks indicate significant differences between
the nac51-1 nac78-1 seedlings and WT (+MG132) based on Student’s t-test (p-value <0.05).
Dashed lines indicate the average values for untreated WT seedlings.
(B) Increased levels of several 26S proteasome subunits during proteasome stress depends on
NAC53 and NAC78. Seedlings were treated +/- MG132 as in panel (A) and the resulting crude
extracts were immunoblotted with the indicated antibodies. Histone H3 was included to confirm
near equal loading.
Figure 9. Plants Lacking Both NAC53 and NAC78 Are Hypersensitive to Proteasome
Inhibitors.
(A) Double homozygous nac53-1 nac78-1 plants are hypersensitive to MG132. Ten-day old
seedlings of the indicated genotypes were germinated and grown on MS medium plus sucrose
and containing either DMSO (control) or 30 or 50 µM MG132.
(B) Quantification of seedling fresh weight in shown in panel A.
(C) Growth inhibition of 6-d-old nac53-1 nac78-1 seedlings first germinated on MG132-free
medium and then transferred to medium containing 50 µM MG132 2 d after germination. .
(D) Double homozygous nac53-1 nac78-1 plants are strongly hypersensitive to bortezomib.
Seedlings were germinated and grown for 7 d on various concentrations of bortezomib.
(E) Fresh weight of 7-d-old seedlings of WT, nac53-1 nac78-1 and nac53-2 nac78-2 seedlings
grown on 1 µM bortezomib (Btz).
Asterisks in panels B, C, and E indicate a p-value <0.01 based on one-way ANOVA.
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