Differences in DNA-binding specificity of floral homeotic ... · Differences in DNA-binding specificity of floral homeotic protein . 4. complexes predict organ-specific target genes.
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1
LARGE-SCALE BIOLOGY ARTICLE 1
2
Differences in DNA-binding specificity of floral homeotic protein 3
complexes predict organ-specific target genes 4
5
Cezary Smaczniak1,2,3,#
, Jose M. Muiño3,4,#
, Dijun Chen2,3
, Gerco C. Angenent1,5
, Kerstin 6
Kaufmann2,3,*
7
8 1
Laboratory of Molecular Biology Wageningen University, Wageningen, 6708PB, The 9
Netherlands 10 2 Institute for Biochemistry and Biology, Potsdam University, Potsdam, 14476, Germany 11
3 Present Address: Institute of Biology, Humboldt-Universität zu Berlin, Berlin, 10115, Germany 12
4 Computational Molecular Biology, Max Planck Institute for Molecular Genetics, Berlin, 14195, 13
Figure 5. Characteristics of SELEX-seq peaks within ChIP-seq peaks. Distribution of complex 933
specific SELEX-seq TFBSs within ChIP-seq TFBSs of SEP3 (top), AP1 (middle) and AG 934
(bottom). Shown is the frequency of distances normalized by the background frequency 935
distances outside of the ChIP-seq peaks, plotted based on the calculated p-values using the 936
hypergeometric test. A distance of zero results when the position of compared TFBSs is the 937
same. 938
31
939
Figure 6. Comparison of activities and protein-DNA binding between various MADS-domain 940
protein complexes to modified AP3 promoters. 941
(A) and (B) Promoter activity quantification in protoplasts using dual luciferase reporter assay 942
with specific protein effector complexes SEP3–AP1 (A) and SEP3–AG (B). Error bars represent 943
standard deviation. Numbers above the boxes represent t-test p-value of the difference between 944
wt and modified promoters. 945
(C) Protein–DNA relative binding intensities of various MADS-domain protein complexes 946
between modified and wt AP3 promoters studied by quMFRA. The quMFRA was performed 947
using two sets of infrared (IR)-labelled DNA sequences (Dy682 and Dy782) where IR 948
fluorophores were reciprocally exchanged between AP3 promoter sequences. Error bars 949
represent standard deviation. Sequences used in EMSA are indicated in Supplemental Table 4. 950
(D) Basal promoter activity quantification in protoplasts using dual luciferase reporter assay. 951
Error bars represent standard deviation. 952
(E) Confocal pictures of the fluorescent reporter expression patterns of the wt and modified AP3 953
promoters. Red arrows indicate the most pronounced changes in spatial GFP expression in 954
modified promoter signal compared to the wt signal. Scale bars = 50 µm. 955
washelution
amplification
binding
immunoprecipitation
re-cycle
ssDNA library
protein-DNA mix
target protein complex
anti-targetantibodies
unbound DNA
eluted DNA
immunoprecipitatedprotein-DNA complexes
SELEXrounds
evolved DNAlibrary
sequencing dsDNA library generation
A
DC
0 1 2 3
0.001
0.01
0.1
Round of SELEX
Freq
uenc
y of
read
s w
ith C
C[A
/T] 6
GG
CAr
G−b
ox
SEP3−SEP3SEP3−AG e1SEP3−AP1SEP3−AG e2AG−AGAP1−AP1
B Protein target: SEP3-AG
protein-DNA
complex
DNAalone
0 1 2 3
0.0002
0.0004
0.0006
0.0008
Med
ian
frequ
ency
of r
eads
with
pe
rmut
ated
Car
G−b
ox
SEP3−SEP3SEP3−AG e1SEP3−AP1SEP3−AG e2AG−AGAP1−AP1
Round of SELEX
0 1 2 3
Round of SELEX
4 5 6
Figure 1. SELEX-seq for MADS-domain protein complexes. (A) Overview of the experimental setup for the SELEX-seq approach performed in this study. (B) EMSA analysis of the DNA libraries obtained in different rounds of SELEX for the SEP3-AG complex. (C) Enrichment of the putative CArG-box consensus sequence (CC[A/T]6GG) in the SELEX-seq rounds (log scale). Frequencies (in %) at Round 3 are: 14.2%, 14.1%, 6.4%, 4.5%, 3.6%, and 0.3% for SEP3–AG e1, SEP3–AG e2, SEP3–AP1, SEP3–SEP3, AG–AG and AP1–AP1 respectively. (D) Enrichment of randomly permutated CArG-box sequences in the SELEX-seq rounds (log scale). SEP3–AG e1 and SEP3–AG e2 indicate two independent experiments where different antibodies were used for immunoprecipitation, SEP3 antibodies (e1) and AG antibodies (e2).
AG−A
G
SEP3
−SEP
3
AP1−AP
1
SEP3
−AP1
SEP3
−AG
e2
SEP3
−AG
e1
0 0.5 10
500
Color Keyand Histogram
Cou
nt
1
2
3
A
Relative affinity
Position
012
012
1
2
3
1 2 3
3.03.54.04.55.05.56.0
Min
or g
roov
e w
idth
(Å)
B
CPosition
012
Info
rmat
ion
cont
ent
250
Info
rmat
ion
cont
ent
Info
rmat
ion
cont
ent
1 3 5 7 9 11 13 152 4 6 8 10 12 14
1 3 5 7 9 11 132 4 6 8 10 12 14
1 3 5 7 9 11 13 152 4 6 8 10 12 14
Position
Cluster
Cluster
Figure 2. DNA-binding specificities of MADS-domain TF complexes. (A) Relative affinity heatmap based on 12-mer sequences enriched in the 3rd round of SELEX for all studied MADS-domain TF complexes. Each line in the heatmap corresponds to a single 12-mer DNA fragment. High relative affinities for a particular sequence are marked in yellow, low relative affinities are in blue. (B) Sequence logos corresponding to the three main clusters of sequences in the heatmap built from the position weight matrices for all 20N sequences containing group specific 12-mers. (C) Minimal DNA minor groove width predictions of the sequences from clusters 1–3. The mean value differences of the minor groove width are significant with p < 0.05 (t-test) for all pairwise comparisons. Number of sequences used in predictions (sample size) are 1298340, 416077 and 705199 for cluster 1, 2 and 3 respectively.
A
0.2 0.4 0.6 0.8 1.0
0.2
0.4
0.6
0.8
1.0
SEP3−AP1 relative affinity
SEP3
−AG
rela
tive
affin
ity
SEP3−AP1 specific (CyATAAATrG)SEP3−AG specific (CyAwwTnrGG)
B
Clu
ster
1
Clu
ster
2
Clu
ster
3
AP1−specific (555)
common (548)
AG−specific (914)3
10
30
100
-log(p-value)
SELEX-seq
ChIP-seqtarget genes
152
249
421
79
158
282
129
157
225
C D
−2
0
2
≤ -2
-2 < &
< 2 ≥ 2
log 2
Exp
ress
ion
ratio
(AP1
-dom
ain/
AG-d
omai
n)
≤ -2
-2 < &
< 2 ≥ 2
SELEX-seq (SEP3-AG/SEP3-AP1)
ChIP-seq (AG/AP1)
p < 0.02
p < 0.07
p < 0.33
p < 0.05
log2 Score ratio
−4 −2 0 2 4
−0.6
−0.4
−0.2
0.0
0.2
0.4
0.6
log2 SELEX-seq score ratio(SEP3−AG/SEP3−AP1)
Aver
age
log 2
ChI
P-se
q sc
ore
ratio
(AG
/AP1
)
SEP3-AGSEP3-AP1
AP1
AG
SELEX-seq score
ChI
P-se
q sc
ore
Figure 3. Comparison between in vitro SELEX-seq and in vivo ChIP-seq. (A) DNA specificity plots comparing the relative binding affinities of SELEX-seq sequences selected by SEP3–AG (y-axis) and SEP3–AP1 (x-axis). Each point represents a unique sequence that contains a color-coded motif. Black points represent all sequences. (B) Association between SELEX-seq normalized score ratios (SEP3–AG/SEP3–AP1) and ChIP-seq normalized score ratios (AG/AP1) for TFBSs within the top 1500 SEP3 ChIP-seq peaks. The plot represents a moving average of overlapping windows of size 1 over the SELEX-seq log2 score ratio. Windows with less than 5 elements were not considered. (C) Prediction of specific and common ChIP-seq target genes for AG and AP1 based on the SELEX-seq complex-specific motifs. The heatmap shows significance (hypergeometric test) of the enrichment of SELEX-seq cluster motifs obtained in Figure 2C in specific and common ChIP-seq binding regions compared previously by Yan et al. (Yan et al., 2016); numerical values represent gene numbers. For the raw data of this figure see Supplemental Data Set 4. (D) Comparison of the TRAP-seq expression data (Jiao and Meyerowitz, 2010) with the SELEX-seq and the ChIP-seq data (Ó’Maoiléidigh et al., 2013; Pajoro et al., 2014). The violin plot visualizes the distribution of AP1-/AG-domain expression ratios of genes containing TFBSs with a certain SEP3–AG/SEP3–AP1 SELEX-seq score ratio (orange) or with a certain AG/AP1 ChIP-seq score ratio (blue).
AP3
SEP3
ChIP SEP3
ChIP AP1
ChIP AG
SELEX SEP3-SEP3
SELEX SEP3-AG
SELEX AG-AG
SELEX SEP3-AP1
SELEX AP1-AP1
TAIR10 mRNA (+)
Coordinates
TAIR10 mRNA (−)
ChIP SEP3
ChIP AP1
ChIP AG
SELEX SEP3-SEP3
SELEX SEP3-AG
SELEX AG-AG
SELEX SEP3-AP1
SELEX AP1-AP1
TAIR10 mRNA (+)
Coordinates
TAIR10 mRNA (−)
Figure 4. Examples of SELEX-seq TFBSs and ChIP-seq profiles mapped to the genome of Arabidopsis. (Top) AP3 genomic locus. (Bottom) SEP3 genomic locus.
−600 −400 −200 0 200 400 6000
2
4
6
8SEP3-AP1
Distance
−log
p-v
alue
−600 −400 −200 0 200 400 60002468
12SEP3-SEP3
Distance−l
og p
-val
ue 10
−600 −400 −200 0 200 400 600
05
10
20
SEP3-AG
Distance
−log
p-v
alue
15
25
Figure 5. Characteristics of SELEX-seq peaks within ChIP-seq peaks. Distribution of complex specific SELEX-seq TFBSs within ChIP-seq TFBSs of SEP3 (top), AP1 (middle) and AG (bottom). Shown is the frequency of distances normalized by the background frequency distances outside of the ChIP-seq peaks, plotted based on the calculated p-values using the hypergeometric test. A distance of zero results when the position of compared TFBSs is the same.
pAP3_(SEP3−AG)
pAP3_mut
pAP3_wt
02
04
06
08
0
+ SEP3-AP1
Re
sp
on
se
to
th
e e
ffe
cto
r
(fo
ld e
nri
ch
me
nt o
f F
/R L
UC
sig
na
l)
1.53e−11
8.00e−02
SEP
3-SEP
3
AG-A
G
AP1-
AP1
SEP
3-AG
SEP
3-AP1
Dy682/Dy782 Dy782/Dy682
Re
lative
bin
din
g in
ten
sity
pAP3_(SEP3-AG)/pAP3_wt
05
10
15
20
25
30
+ SEP3-AG
Re
sp
on
se
to
th
e e
ffe
cto
r
(fo
ld e
nri
ch
me
nt o
f F
/R L
UC
sig
na
l)
1.26e−07
4.26e−04
pAP3_(SEP3−AG)
pAP3_mut
pAP3_wt
0
0.05
0.10
0.15
0.20
0.25
0.30
Pro
mo
ter
activity a
s L
UC
sig
na
l
with
ou
t th
e e
ffe
cto
r [A
U]
pAP3_wt
pAP3_mut
pAP3_(SEP3−AG)
pAP3_wt:GFP pAP3_(SEP3-AG):GFPpAP3_mut:GFP
A B
C D
E
0.03125
0.0625
0.125
0.25
0.5
1
2
4
8
Figure 6. Comparison of activities and protein-DNA binding between various MADS-domain protein complexes to modified AP3 promoters. (A) and (B) Promoter activity quantification in protoplasts using dual luciferase reporter assay with specific protein effector complexes SEP3–AP1 (A) and SEP3–AG (B). Error bars represent standard deviation. Numbers above the boxes represent t-test p-value of the difference between wt and modified promoters. (C) Protein–DNA relative binding intensities of various MADS-domain protein complexes between modified and wt AP3 promoters studied by quMFRA. The quMFRA was performed using two sets of infrared (IR)-labelled DNA sequences (Dy682 and Dy782) where IR fluorophores were reciprocally exchanged between AP3 promoter sequences. Error bars represent standard deviation. Sequences used in EMSA are indicated in Supplemental Table 4. (D) Basal promoter activity quantification in protoplasts using dual luciferase reporter assay. Error bars represent standard deviation. (E) Confocal pictures of the fluorescent reporter expression patterns of the wt and modified AP3 promoters. Red arrows indicate the most pronounced changes in spatial GFP expression in modified promoter signal compared to the wt signal. Scale bars = 50 µm.
Parsed CitationsBemer, M., van Dijk, A.D., Immink, R.G., and Angenent, G.C. (2017). Cross-Family Transcription Factor Interactions: An AdditionalLayer of Gene Regulation. Trends Plant Sci 22, 66-80.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Brambilla, V., Battaglia, R., Colombo, M., Masiero, S., Bencivenga, S., Kater, M.M., and Colombo, L. (2007). Genetic and molecularinteractions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell 19, 2544-2556.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsisthaliana. Plant J 16, 735-743.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
de Folter, S., and Angenent, G.C. (2006). trans meets cis in MADS science. Trends Plant Sci 11, 224-231.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Deng, W., Ying, H., Helliwell, C.A., Taylor, J.M., Peacock, W.J., and Dennis, E.S. (2011). FLOWERING LOCUS C (FLC) regulatesdevelopment pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci USA 108, 6680-6685.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Diaz-Trivino, S., Long, Y., Scheres, B., and Blilou, I. (2017). Analysis of a Plant Transcriptional Regulatory Network Using TransientExpression Systems. Methods Mol Biol 1629, 83-103.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dickerson, R.E. (1998). DNA bending: the prevalence of kinkiness and the virtues of normality. Nucleic Acids Res 26, 1906-1926.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Egea-Cortines, M., Saedler, H., and Sommer, H. (1999). Ternary complex formation between the MADS-box proteins SQUAMOSA,DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J 18, 5370-5379.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Franco-Zorrilla, J.M., Lopez-Vidriero, I., Carrasco, J.L., Godoy, M., Vera, P., and Solano, R. (2014). DNA-binding specificities of planttranscription factors and their potential to define target genes. Proc Natl Acad Sci USA 111, 2367-2372.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Grant, C.E., Bailey, T.L., and Noble, W.S. (2011). FIMO: scanning for occurrences of a given motif. Bioinformatics 27, 1017-1018.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gregis, V., Sessa, A., Dorca-Fornell, C., and Kater, M.M. (2009). The Arabidopsis floral meristem identity genes AP1, AGL24 and SVPdirectly repress class B and C floral homeotic genes. The Plant Journal 60, 626-637.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gremski, K., Ditta, G., and Yanofsky, M.F. (2007). The HECATE genes regulate female reproductive tract development inArabidopsis thaliana. Development 134, 3593-3601.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Haran, T.E., and Mohanty, U. (2009). The unique structure of A-tracts and intrinsic DNA bending. Q Rev Biophys 42, 41-81.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Honma, T., and Goto, K. (2001). Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409,525-529.
Pubmed: Author and TitleCrossRef: Author and Title
Google Scholar: Author Only Title Only Author and Title
Horstman, A., Fukuoka, H., Muino, J.M., Nitsch, L., Guo, C., Passarinho, P., Sanchez-Perez, G., Immink, R., Angenent, G., andBoutilier, K. (2015). AIL and HDG proteins act antagonistically to control cell proliferation. Development 142, 454-464.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Huang, H., Mizukami, Y., Hu, Y., and Ma, H. (1993). Isolation and characterization of the binding sequences for the product of theArabidopsis floral homeotic gene AGAMOUS. Nucleic Acids Res 21, 4769-4776.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Huang, H., Tudor, M., Weiss, C.A., Hu, Y., and Ma, H. (1995). The Arabidopsis MADS-box gene AGL3 is widely expressed andencodes a sequence-specific DNA-binding protein. Plant Mol Biol 28, 549-567.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Huang, H., Tudor, M., Su, T., Zhang, Y., Hu, Y., and Ma, H. (1996). DNA binding properties of two Arabidopsis MADS domainproteins: binding consensus and dimer formation. The Plant cell 8, 81-94.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Huang, K., Louis, J.M., Donaldson, L., Lim, F.L., Sharrocks, A.D., and Clore, G.M. (2000). Solution structure of the MEF2A-DNAcomplex: structural basis for the modulation of DNA bending and specificity by MADS-box transcription factors. EMBO J 19, 2615-2628.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Immink, R.G., Pose, D., Ferrario, S., Ott, F., Kaufmann, K., Valentim, F.L., de Folter, S., van der Wal, F., van Dijk, A.D., Schmid, M.,and Angenent, G.C. (2012). Characterization of SOC1's central role in flowering by the identification of its upstream anddownstream regulators. Plant Physiol 160, 433-449.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jetha, K., Theissen, G., and Melzer, R. (2014). Arabidopsis SEPALLATA proteins differ in cooperative DNA-binding during theformation of floral quartet-like complexes. Nucleic Acids Res 42, 10927-10942.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jiao, Y., and Meyerowitz, E.M. (2010). Cell-type specific analysis of translating RNAs in developing flowers reveals new levels ofcontrol. Mol Syst Biol 6, 419.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jolma, A., Yin, Y., Nitta, K.R., Dave, K., Popov, A., Taipale, M., Enge, M., Kivioja, T., Morgunova, E., and Taipale, J. (2015). DNA-dependent formation of transcription factor pairs alters their binding specificity. Nature 527, 384-388.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jolma, A., Kivioja, T., Toivonen, J., Cheng, L., Wei, G., Enge, M., Taipale, M., Vaquerizas, J.M., Yan, J., Sillanpaa, M.J., Bonke, M.,Palin, K., Talukder, S., Hughes, T.R., Luscombe, N.M., Ukkonen, E., and Taipale, J. (2010). Multiplexed massively parallel SELEX forcharacterization of human transcription factor binding specificities. Genome Res 20, 861-873.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jolma, A., Yan, J., Whitington, T., Toivonen, J., Nitta, K.R., Rastas, P., Morgunova, E., Enge, M., Taipale, M., Wei, G., Palin, K.,Vaquerizas, J.M., Vincentelli, R., Luscombe, N.M., Hughes, T.R., Lemaire, P., Ukkonen, E., Kivioja, T., and Taipale, J. (2013). DNA-binding specificities of human transcription factors. Cell 152, 327-339.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kaufmann, K., Melzer, R., and Theissen, G. (2005). MIKC-type MADS-domain proteins: structural modularity, protein interactionsand network evolution in land plants. Gene 347, 183-198.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kaufmann, K., Muino, J.M., Jauregui, R., Airoldi, C.A., Smaczniak, C., Krajewski, P., and Angenent, G.C. (2009). Target genes of theMADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol
7, e1000090.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kaufmann, K., Wellmer, F., Muino, J.M., Ferrier, T., Wuest, S.E., Kumar, V., Serrano-Mislata, A., Madueno, F., Krajewski, P.,Meyerowitz, E.M., Angenent, G.C., and Riechmann, J.L. (2010). Orchestration of floral initiation by APETALA1. Science 328, 85-89.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kneidl, C., Dinkl, E., and Grummt, F. (1995). An intrinsically bent region upstream of the transcription start site of the rRNA genesof Arabidopsis thaliana interacts with an HMG-related protein. Plant Mol Biol 27, 705-713.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Krizek, B.A., and Meyerowitz, E.M. (1996). Mapping the protein regions responsible for the functional specificities of theArabidopsis MADS domain organ-identity proteins. Proc Natl Acad Sci USA 93, 4063-4070.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Krizek, B.A., Riechmann, J.L., and Meyerowitz, E.M. (1999). Use of the APETALA1 promoter to assay the in vivo function of chimericMADS box genes. Sex Plant Reprod 12, 14-26.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Li, L. (2009). GADEM: a genetic algorithm guided formation of spaced dyads coupled with an EM algorithm for motif discovery. JComput Biol 16, 317-329.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Li, R., Yu, C., Li, Y., Lam, T.W., Yiu, S.M., Kristiansen, K., and Wang, J. (2009). SOAP2: an improved ultrafast tool for short readalignment. Bioinformatics 25, 1966-1967.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Man, T.K., and Stormo, G.D. (2001). Non-independence of Mnt repressor-operator interaction determined by a new quantitativemultiple fluorescence relative affinity (QuMFRA) assay. Nucleic Acids Res 29, 2471-2478.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Mathelier, A., Xin, B., Chiu, T.P., Yang, L., Rohs, R., and Wasserman, W.W. (2016). DNA Shape Features Improve TranscriptionFactor Binding Site Predictions In Vivo. Cell Syst 3, 278-286 e274.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Melzer, R., and Theissen, G. (2009). Reconstitution of 'floral quartets' in vitro involving class B and class E floral homeoticproteins. Nucleic Acids Res 37, 2723-2736.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Melzer, R., Verelst, W., and Theissen, G. (2009). The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in 'floralquartet'-like complexes in vitro. Nucleic Acids Res 37, 144-157.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Muino, J.M., Kaufmann, K., van Ham, R.C.H.J., Angenent, G.C., and Krajewski, P. (2011). ChIP-seq Analysis in R (CSAR): An Rpackage for the statistical detection of protein-bound genomic regions. Plant Methods 7.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Muino, J.M., Smaczniak, C., Angenent, G.C., Kaufmann, K., and van Dijk, A.D. (2014). Structural determinants of DNA recognition byplant MADS-domain transcription factors. Nucleic Acids Res 42, 2138-2146.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Nelson, H.B., and Laughon, A. (1990). The DNA binding specificity of the Drosophila fushi tarazu protein: a possible role for DNAbending in homeodomain recognition. New Biol 2, 171-178.
CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
O'Malley, R.C., Huang, S.S., Song, L., Lewsey, M.G., Bartlett, A., Nery, J.R., Galli, M., Gallavotti, A., and Ecker, J.R. (2016). Cistromeand Epicistrome Features Shape the Regulatory DNA Landscape. Cell 165, 1280-1292.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ó'Maoiléidigh, D.S., Wuest, S.E., Rae, L., Raganelli, A., Ryan, P.T., Kwasniewska, K., Das, P., Lohan, A.J., Loftus, B., Graciet, E., andWellmer, F. (2013). Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS.Plant Cell 25, 2482-2503.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pajoro, A., Madrigal, P., Muino, J.M., Matus, J.T., Jin, J., Mecchia, M.A., Debernardi, J.M., Palatnik, J.F., Balazadeh, S., Arif, M.,O'Maoileidigh, D.S., Wellmer, F., Krajewski, P., Riechmann, J.L., Angenent, G.C., and Kaufmann, K. (2014). Dynamics of chromatinaccessibility and gene regulation by MADS-domain transcription factors in flower development. Genome Biol 15, R41.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Parenicova, L., de Folter, S., Kieffer, M., Horner, D.S., Favalli, C., Busscher, J., Cook, H.E., Ingram, R.M., Kater, M.M., Davies, B.,Angenent, G.C., and Colombo, L. (2003). Molecular and phylogenetic analyses of the complete MADS-box transcription factor familyin Arabidopsis: new openings to the MADS world. The Plant cell 15, 1538-1551.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Payne, C.T., Zhang, F., and Lloyd, A.M. (2000). GL3 encodes a bHLH protein that regulates trichome development in arabidopsisthrough interaction with GL1 and TTG1. Genetics 156, 1349-1362.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pellegrini, L., Tan, S., and Richmond, T.J. (1995). Structure of serum response factor core bound to DNA. Nature 376, 490-498.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pollock, R., and Treisman, R. (1990). A sensitive method for the determination of protein-DNA binding specificities. Nucleic AcidsRes 18, 6197-6204.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Riechmann, J.L., and Meyerowitz, E.M. (1997). Determination of floral organ identity by Arabidopsis MADS domain homeoticproteins AP1, AP3, PI, and AG is independent of their DNA-binding specificity. Mol Biol Cell 8, 1243-1259.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Riechmann, J.L., Wang, M., and Meyerowitz, E.M. (1996a). DNA-binding properties of Arabidopsis MADS domain homeotic proteinsAPETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res 24, 3134-3141.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Riechmann, J.L., Krizek, B.A., and Meyerowitz, E.M. (1996b). Dimerization specificity of Arabidopsis MADS domain homeoticproteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci USA 93, 4793-4798.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rohs, R., West, S.M., Sosinsky, A., Liu, P., Mann, R.S., and Honig, B. (2009). The role of DNA shape in protein-DNA recognition.Nature 461, 1248-1253.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., Thumfahrt, J., Jurgens, G., and Hulskamp, M. (2002).TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21, 5036-5046.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schwarz-Sommer, Z., Huijser, P., Nacken, W., Saedler, H., and Sommer, H. (1990). Genetic Control of Flower Development byHomeotic Genes in Antirrhinum majus. Science 250, 931-936.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schwarz-Sommer, Z., Hue, I., Huijser, P., Flor, P.J., Hansen, R., Tetens, F., Lonnig, W.E., Saedler, H., and Sommer, H. (1992).Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of itspersistent expression throughout flower development. EMBO J 11, 251-263.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Simonini, S., Roig-Villanova, I., Gregis, V., Colombo, B., Colombo, L., and Kater, M.M. (2012). Basic pentacysteine proteins mediateMADS domain complex binding to the DNA for tissue-specific expression of target genes in Arabidopsis. Plant Cell 24, 4163-4172.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Slattery, M., Riley, T., Liu, P., Abe, N., Gomez-Alcala, P., Dror, I., Zhou, T., Rohs, R., Honig, B., Bussemaker, H.J., and Mann, R.S.(2011). Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 147, 1270-1282.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Smaczniak, C., Immink, R.G., Angenent, G.C., and Kaufmann, K. (2012a). Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139, 3081-3098.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Smaczniak, C., Immink, R.G., Muino, J.M., Blanvillain, R., Busscher, M., Busscher-Lange, J., Dinh, Q.D., Liu, S., Westphal, A.H.,Boeren, S., Parcy, F., Xu, L., Carles, C.C., Angenent, G.C., and Kaufmann, K. (2012b). Characterization of MADS-domaintranscription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci USA 109, 1560-1565.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Stella, S., Cascio, D., and Johnson, R.C. (2010). The shape of the DNA minor groove directs binding by the DNA-bending proteinFis. Genes Dev 24, 814-826.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tang, W., and Perry, S.E. (2003). Binding site selection for the plant MADS domain protein AGL15: an in vitro and in vivo study. JBiol Chem 278, 28154-28159.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Theissen, G., and Saedler, H. (2001). Plant biology. Floral quartets. Nature 409, 469-471.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Tilly, J.J., Allen, D.W., and Jack, T. (1998). The CArG boxes in the promoter of the Arabidopsis floral organ identity gene APETALA3mediate diverse regulatory effects. Development 125, 1647-1657.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
West, A.G., Shore, P., and Sharrocks, A.D. (1997). DNA binding by MADS-box transcription factors: a molecular mechanism fordifferential DNA bending. Mol Cell Biol 17, 2876-2887.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
West, A.G., Causier, B.E., Davies, B., and Sharrocks, A.D. (1998). DNA binding and dimerisation determinants of Antirrhinum majusMADS-box transcription factors. Nucleic Acids Res 26, 5277-5287.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wuest, S.E., O'Maoileidigh, D.S., Rae, L., Kwasniewska, K., Raganelli, A., Hanczaryk, K., Lohan, A.J., Loftus, B., Graciet, E., andWellmer, F. (2012). Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proc Natl Acad Sci USA 109,13452-13457.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Yan, W., Chen, D., and Kaufmann, K. (2016). Molecular mechanisms of floral organ specification by MADS domain proteins. CurrOpin Plant Biol 29, 154-162.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ye, L., Wang, B., Zhang, W., Shan, H., and Kong, H. (2016). Gains and Losses of Cis-regulatory Elements Led to Divergence of theArabidopsis APETALA1 and CAULIFLOWER Duplicate Genes in the Time, Space, and Level of Expression and Regulation of OneParalog by the Other. Plant Physiol 171, 1055-1069.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expressionanalysis. Nat Protoc 2, 1565-1572.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zheng, Y., Ren, N., Wang, H., Stromberg, A.J., and Perry, S.E. (2009). Global identification of targets of the Arabidopsis MADSdomain protein AGAMOUS-Like15. The Plant cell 21, 2563-2577.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Zhou, T., Yang, L., Lu, Y., Dror, I., Dantas Machado, A.C., Ghane, T., Di Felice, R., and Rohs, R. (2013). DNAshape: a method for thehigh-throughput prediction of DNA structural features on a genomic scale. Nucleic Acids Res 41, W56-62.
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title