Santiago Supplementary Materials -...
Transcript of Santiago Supplementary Materials -...
www.sciencemag.org/cgi/content/full/science.1242468/DC1
Supplementary Materials for
Molecular Mechanism for Plant Steroid Receptor Activation by Somatic
Embryogenesis Co-Receptor Kinases
Julia Santiago, Christine Henzler, Michael Hothorn*
*To whom correspondence should be addressed. E-mail: [email protected]
Published 8 August 2013 on Science Express
DOI: 10.1126/science.1242468
This PDF file includes:
Materials and Methods
Figs. S1 to S6
Table S1
References
μΜ
Μ
μ
μ
°
Fig. S1.The wild-type BRI1 and SERK1 ectodomains interact upon brassinolide binding. (A) UVabsorbance traces from analytical size-exclusion chromatography experiments. BL-boundBRI1 wild-type elutes as a monomer (black dotted line), as does the isolated SERK1LRR domain (blue dotted line). The BRI1 wild-type – BL – SERK1 complex elutes as anapparent heterodimer (red line), while a mixture of BRI1 wild-type and SERK1 in theabsence of BL yields two isolated peaks that correspond to the monomeric BRI1 andSERK1 ectodomains, respectively (black line). Void (V0) and total volume (Vt) areshown, together with elution volumes for molecular mass standards (A, Thyroglobulin,669,000 Da; B, Ferritin, 440,00 Da, C, Aldolase, 158,000 Da; D, Conalbumin, 75,000Da; E, Ovalbumin, 44,000 Da; F, Carbonic anhydrase, 29,000 Da). The calculatedmolecular mass for the BRI1 wild-type and SERK1 elution peaks are ~125 and ~35 kDa,respectively. Purified BRI1 wild-type and SERK1 are ~110 and ~30 kDa. (B)SDS-PAGE analysis of elution fractions from the size-exclusion chromatographyexperiments shown in (A).
7
A
0 5 10 15 20 25
050
100
150
200
elution volume (ml)
A 280
(a.u
.)
V0 VtA B C D E F
BRI1 wild-typeSERK1BRI1 wild-type - SERK1 -BL BRI1 wild-type - SERK1 +BL
peak1
peak2
B
marker
comple
x
BRI1 wild
-type
250
130100
70
55
3525
15
SERK1
peak
1pe
ak2
BRI1 wild-type
SERK1
Fig. S2Crystal lattice interactions of the bri1sud1 and SERK1 ectodomains. (A) Orientation of 12bri1sud1 – BL – SERK1 complexes in the unit cell of the P65 crystal structure (a=b=~70 Åand c=874 Å). Cα-traces of BRI1 molecules A and B are shown in dark- and light-blue,respectively, the corresponding SERK1 ectodomains are depicted in yellow and red(chains C, D). Two bri1sud1 – BL – SERK1 complexes form a crystallographic dimer inthe asymmetric unit. (B) Crystal packing brings two BRI1 ectodomain superhelices into ahead-to-head arrangement. The lattice propagates by establishing contacts between theC-termini of two SERK1 LRR domains and the corresponding C-termini of the BRI1ectodomains. This figure has been prepared with the supercell.py script as implementedin the program PYMOL (http://pymol.sourceforge.org).
8
70 70
874
CC C
C
N
N
N
N
A B
Fig. S3SERK1 ectodomain residues participate in the specific recognition of the steroidhormone. (A) The LIGPLOT (41) diagram summarizes key interactions betweenbrassinolide (yellow lines) and hormone binding pocket residues that originate from theBRI1 LRR core (shown in blue), from the BRI1 island domain (in green) and from theSERK1 N-terminal capping domain (shown in orange). His62SERK1 establishes hydrogenbonds with both the 2α and 3α hydroxyl groups of BL, which are known to be critical forbioactivity. Semicircles with radiating lines indicate non-polar interactions. Chemicalstructures of (B) brassinolide and (C) BL 2,3-acetonide are included for comparison.
9
3.072.41
3.30
3.00
2
3
N
ND1
H62
Y597
N
S647
Y642N705
Y599
K601
M657
T729
I563T646
P648
F681
I540
I706
F61
A
B
C
D
A
H
H
CH3
CH3
CH3
OH
OH
OH
OH
CH3
CH3
H3C
HH
H O
O
3
2
B
H
H
CH3
CH3
CH3
OH
OH
CH3
CH3
H3C
HH
H O
O
O
O 3
2
C
Fig. S4BRI1 – SERK1 complex interface residues are conserved among known SERK-family members and in other LRR receptor kinases. Structure-basedsequence alignment of the known BRI1 interacting SERK-family members Arabidopsis thaliana SERK1 (Uniprot (http://www.uniprot.org) identifier:Q94AG2), A. thaliana SERK2 (Uniprot identifier: Q9XIC7), A. thaliana SERK3/BAK1 (Uniprot identifier: Q94F62), A. thaliana SERK4 (Uniprotidentifier: Q9SKG5) and Oryza sativa subsp. japonica BAK1 (Uniprot identifier: Q7XV05) (9–11, 42, 43). Based on the SERK1 interface residues inthe bri1sud1 – BL – SERK1 complex, we identified other, putative, BRI1-interacting receptor kinases (in grey): Selaginella moellendorffii SERKx(Uniprot identifier: D8RKF6), Capsella rubella SERKx (44) (GenBank identifier: EOA30137.1), Vitis vinifera SERKx (Uniprot identifier: D7STF5),Glycine max (Uniprot identifier: I1KR51), Nicotiana benthamiana SERKx (Uniprot identifier: E3VXE7), Medicago truncatula SERKx (Uniprotidentifier: G7ILB9). The alignment includes a secondary structure assignment calculated with the program DSSP (45) and colored according to Fig. 1C.The N- and C-terminal caps and the five LRRs in SERK1 are indicated in red and blue, respectively. Cysteine residues in the N- and C-terminal cappingdomains are highlighted in green. Note that most SERK proteins have the C-terminal disulfide bond replaced by a proline-rich region. N-glycosylationsites observed in SERK1 crystals are marked with a yellow star. The position of the serk3 elg point-mutation (corresponds to Asp123 in SERK1) isindicated in cyan, SERK-residues interacting with BRI1 in the bri1sud1 – BL – SERK1 complex are highlighted in orange.
10
310αN-terminal cap
signal peptide
*AtSERK1 MESSYV----V-FILL--SLILLPNHSLWLASANLEGDALHTLRVTLV--DP-NNVLQSWDPTLVNPCTWFHVTCNNENSVIRVDLGNAELSGHLVPELGVLKNLQYLELYSNNAtSERK2 MGRKKFEAFGF-VCLI--SLLLLFN-SLWLASSNMEGDALHSLRANLV--DP-NNVLQSWDPTLVNPCTWFHVTCNNENSVIRVDLGNADLSGQLVPQLGQLKNLQYLELYSNNAtSERK3 MERR-----LMIPCFF--WLILVLD-LVLRVSGNAEGDALSALKNSLA--DP-NKVLQSWDATLVTPCTWFHVTCNSDNSVTRVDLGNANLSGQLVMQLGQLPNLQYLELYSNNAtSERK4 MTSSKMEQRSL-LCFL--YLLLLFN-FTLRVAGNAEGDALTQLKNSLSSGDPANNVLQSWDATLVTPCTWFHVTCNPENKVTRVDLGNAKLSGKLVPELGQLLNLQYLELYSNNOsBAK1 MAEARLLRRRR-LCLAVPFVWVVAV-AVSRVGANTEGDALYSLRQSLK--DA-NNVLQSWDPTLVNPCTWFHVTCNPDNSVIRVDLGNAQLSGALVPQLGQLKNLQYLELYSNNSmSERKx MEQDAAA--VL-LLLL--CLFCLLG-VQPSLVCVSPVSALFAFKQSLV--DP-QNAMSGWDKNAVDPCSWIHVSCS-EQNVSRVELPGLQLSGQLSPRLADLANLQYLMLQNNNCrSERKx MEQR-----SL-LCFV--WLILLLV-FTLRAAGNTEGDALIVLKNNLSPADPANNVLQSWDATLVTPCTWFHVTCNNENKVTRVDLGNAELSGKLVPELGQLLNLQYLELYSNNVvSERKx MEAI------F-LC--------LIS-LVLRVSGISEGDALYALKSSLV--DP-KDVLQSWDTSSGNPCIWFHVTCNGDGNVIRVDLGNGSLSGQLDSRVGQLTKLEYLGLYNNNGmSERKx MERMISSFMSL-FFIL--WIFVVLD-LVLKVYGHAEGDALIVLKNSMI--DP-NNALHNWDASLVSPCTWFHVTCS-ENSVIRVELGNANLSGKLVPELGQLPNLQYLELYSNNNbSERKx MDQSVLL---I-CVFL--CLTGLLL-SSSPVAGNAEGDALYAQKTNLG--DP-NTVLQSWDQTLVNPCTWFHVTCNNENSVTRVDLGNANLTGQLVPQLGQLQKLQYLELYSNNMtSERKx MERVSSAS-KV-SFLF--WAILVLH-LLLNASSNVESDTLIALKSNLN--DP-NSVFQSWNATNVNPCEWFHVTCNDDKSVILIDLENANLSGTLISKFGDLSNLQYLELSSNN
Asn104
C-terminal cap
AtSERK1 ITGPIPSNLGNLTNLVSLDLYLNSFSGPIPESLGKLSKLRFLRLNNNSLTGSIPMSLTNITTLQVLDLSNNRLSGSVPDNGSFSLFTPISFANNLDLCG-PVT---S-HPCPGSAtSERK2 ITGPVPSDLGNLTNLVSLDLYLNSFTGPIPDSLGKLFKLRFLRLNNNSLTGPIPMSLTNIMTLQVLDLSNNRLSGSVPDNGSFSLFTPISFANNLDLCG-PVT---S-RPCPGSAtSERK3 ITGTIPEQLGNLTELVSLDLYLNNLSGPIPSTLGRLKKLRFLRLNNNSLSGEIPRSLTAVLTLQVLDLSNNPLTGDIPVNGSFSLFTPISFANTKLTPL-PAS---PPPPISPTAtSERK4 ITGEIPEELGDLVELVSLDLYANSISGPIPSSLGKLGKLRFLRLNNNSLSGEIPMTLTSV-QLQVLDISNNRLSGDIPVNGSFSLFTPISFANNSLTDL-PEP---PPTSTSPTOsBAK1 ISGTIPNELGNLTNLVSLDLYLNNFTGFIPETLGQLYKLRFLRLNNNSLSGSIPKSLTNITTLQVLDLSNNNLSGEVPSTGSFSLFTPISFANNKDLCG-PGT---T-KPCPGASmSERKx LSGPIPPEFGNWSRIISVDLSNNNLSDPIPSTLGKLQTLQYLRLNNNSLSGAFPVSVATIRALDFLDVSFNNLSGNVPNATTANL----NVKGNPLLCG-SKT--SRI--CPGDCrSERKx ITGEIPEELGGLRELVSLDLYANNINGPIPSSLGQLEKLRFLRLNNNSLSGGIPMELTAV-QLQVLDISNNRLSGDIPVNGSFSLFTPISFKNNKLTSL-P---------EPPPVvSERKx ISGKIPEELGNLENLMSLDLYFNNLSGPIPGTLGKLRKLHFLRLNNNILMGTIPMSLTAVSSLEILDLSNNKLTGDIPVNGSFSLFTPISFGNNRLSNNSPKRTLDSPSPISPNGmSERKx ITGEIPVELGNLTNLVSLDLYMNKITGPIPDELANLNQLQSLRLNDNSLLGNIPVGLTTINSLQVLDLSNNNLTGDVPVNGSFSIFTPISFNNNPFLNK-T-------IPVTPANbSERKx ISGRIPNELGNLTELVSLDLYLNNLNGPIPDTLGKLQKLRFLRLNNNSLIGLIPMSLTTILALQVLDLSSNHLTGPVPVNGSFSLFTPISFANNQLEVP-PA--------SPPPMtSERKx ITGKIPEELGNLTNLVSLDLYLNHLSGTILNTLGNLHKLCFLRLNNNSLTGVIPISLSNVATLQVLDLSNNNLEGDIPVNGSFLLFTSSSYQNNPRLKQ-P----------KII
310 310 310 310
D123NSERK3 elg
* *
Asn150 Asn184
310
LRR1 LRR2
LRR2 LRR3 LRR4 LRR5
Fig. S5Details of the BRI1 – SERK1 complex interface. (A) Side and (B) front view of the BRI1– SERK1 interface with the BRI1 LRR domain in blue (in surface representation), theSERK1 ectodomain in orange (ribbon diagram) and BL in yellow (in bondsrepresentation). Interface residues are highlighted as sticks. Arg73SERK1 contacts Thr750in the BRI1 C-terminal cap (bri1102), Asp75SERK1 establishes a hydrogen bond withThr729, as does the main-chain oxygen of Gly77 with Thr726. Non-polar contacts aremediated by Tyr97SERK1, Tyr101SERK1, Tyr125SERK1 and Phe145SERK1 and by Met727 andMet745 in BRI1. Asp123SERK1 is centrally located in the complex interface and takes partin a hydrogen-bonding network that involves Glu99SERK1, Ser121SERK1, Tyr125SERK1,Arg147SERK1 and Glu749 in the BRI1 C-terminal cap.
11
LRR4
R73D75 G77
T726
T729 M727
Q747
E99Y97
Y101
Y125
M745
E749
F145R147
S121T750
D123
LRR3
LRR2
N-cap
LRR1
N-cap
R73
D75
G77
T726
T750
T729
Y97
E99Y101
E749
M745
Y125D123
S121
R147
F145
A
B
Fig. S6Conserved surface patches in the SERK1 ectodomain may mediate interaction with otherreceptor kinases. (A) Ribbon diagram of the SERK1 ectodomain colored as in Fig. 1Cand shown in the same orientation as the molecular surfaces in (B) Surface diagram ofthe SERK1 ectodomain with the bri1sud1 – interacting residues shown in blue (left panel),and with the surface colored according to SERK-family sequence conservation (rightpanel, compare fig. S4).
12
N
C
A B
100 %0
B
100 %0
N
C
α, β, γ °
σ
°
References
1. J. Li, J. Chory, A putative leucine-rich repeat receptor kinase involved in brassinosteroid
signal transduction. Cell 90, 929–938 (1997). doi:10.1016/S0092-8674(00)80357-8
Medline
2. M. Ogawa, H. Shinohara, Y. Sakagami, Y. Matsubayashi, Arabidopsis CLV3 peptide directly
binds CLV1 ectodomain. Science 319, 294 (2008). doi:10.1126/science.1150083
3. L. Gómez-Gómez, T. Boller, FLS2: An LRR receptor-like kinase involved in the perception of
the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003–1011 (2000).
doi:10.1016/S1097-2765(00)80265-8 Medline
4. Z.-Y. Wang, M.-Y. Bai, E. Oh, J.-Y. Zhu, Brassinosteroid signaling network and regulation of
photomorphogenesis. Annu. Rev. Genet. 46, 701–724 (2012). doi:10.1146/annurev-genet-
102209-163450 Medline
5. Z. He, Z. Y. Wang, J. Li, Q. Zhu, C. Lamb, P. Ronald, J. Chory, Perception of brassinosteroids
by the extracellular domain of the receptor kinase BRI1. Science 288, 2360–2363 (2000).
doi:10.1126/science.288.5475.2360
6. T. Kinoshita, A. Caño-Delgado, H. Seto, S. Hiranuma, S. Fujioka, S. Yoshida, J. Chory,
Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1.
Nature 433, 167–171 (2005). doi:10.1038/nature03227 Medline
7. J. She, Z. Han, T. W. Kim, J. Wang, W. Cheng, J. Chang, S. Shi, J. Wang, M. Yang, Z. Y.
Wang, J. Chai, Structural insight into brassinosteroid perception by BRI1. Nature 474,
472–476 (2011). doi:10.1038/nature10178 Medline
8. M. Hothorn, Y. Belkhadir, M. Dreux, T. Dabi, J. P. Noel, I. A. Wilson, J. Chory, Structural
basis of steroid hormone perception by the receptor kinase BRI1. Nature 474, 467–471
(2011). doi:10.1038/nature10153 Medline
9. J. Li, J. Wen, K. A. Lease, J. T. Doke, F. E. Tax, J. C. Walker, BAK1, an Arabidopsis LRR
receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling.
Cell 110, 213–222 (2002). doi:10.1016/S0092-8674(02)00812-7 Medline
10. K. H. Nam, J. Li, BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling.
Cell 110, 203–212 (2002). doi:10.1016/S0092-8674(02)00814-0 Medline
11. X. Gou, H. Yin, K. He, J. Du, J. Yi, S. Xu, H. Lin, S. D. Clouse, J. Li, Genetic evidence for
an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid
signaling. PLoS Genet. 8, e1002452 (2012). doi:10.1371/journal.pgen.1002452 Medline
12. R. Karlova, S. Boeren, E. Russinova, J. Aker, J. Vervoort, S. de Vries, The Arabidopsis
SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes
BRASSINOSTEROID-INSENSITIVE1. Plant Cell 18, 626–638 (2006).
doi:10.1105/tpc.105.039412 Medline
13. X. Wang, U. Kota, K. He, K. Blackburn, J. Li, M. B. Goshe, S. C. Huber, S. D. Clouse,
Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts
early events in brassinosteroid signaling. Dev. Cell 15, 220–235 (2008).
doi:10.1016/j.devcel.2008.06.011 Medline
14. Y. Jaillais, M. Hothorn, Y. Belkhadir, T. Dabi, Z. L. Nimchuk, E. M. Meyerowitz, J. Chory,
Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering
membrane release of its kinase inhibitor. Genes Dev. 25, 232–237 (2011).
doi:10.1101/gad.2001911 Medline
15. Y. Belkhadir, Y. Jaillais, P. Epple, E. Balsemão-Pires, J. L. Dangl, J. Chory, Brassinosteroids
modulate the efficiency of plant immune responses to microbe-associated molecular
patterns. Proc. Natl. Acad. Sci. U.S.A. 109, 297–302 (2012).
doi:10.1073/pnas.1112840108 Medline
16. T. Asami, Y. K. Min, N. Nagata, K. Yamagishi, S. Takatsuto, S. Fujioka, N. Murofushi, I.
Yamaguchi, S. Yoshida, Characterization of brassinazole, a triazole-type brassinosteroid
biosynthesis inhibitor. Plant Physiol. 123, 93–100 (2000). doi:10.1104/pp.123.1.93
Medline
17. A. Di Matteo, L. Federici, B. Mattei, G. Salvi, K. A. Johnson, C. Savino, G. De Lorenzo, D.
Tsernoglou, F. Cervone, The crystal structure of polygalacturonase-inhibiting protein
(PGIP), a leucine-rich repeat protein involved in plant defense. Proc. Natl. Acad. Sci.
U.S.A. 100, 10124–10128 (2003). doi:10.1073/pnas.1733690100 Medline
18. M. S. Jin, S. E. Kim, J. Y. Heo, M. E. Lee, H. M. Kim, S. G. Paik, H. Lee, J. O. Lee, Crystal
structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated
lipopeptide. Cell 130, 1071–1082 (2007). doi:10.1016/j.cell.2007.09.008 Medline
19. J. Y. Kang, X. Nan, M. S. Jin, S. J. Youn, Y. H. Ryu, S. Mah, S. H. Han, H. Lee, S. G. Paik,
J. O. Lee, Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6
heterodimer. Immunity 31, 873–884 (2009). doi:10.1016/j.immuni.2009.09.018 Medline
20. T. G. Back, R. P. Pharis, Structure-activity studies of brassinosteroids and the search for
novel analogues and mimetics with improved bioactivity. J. Plant Growth Regul. 22,
350–361 (2003). doi:10.1007/s00344-003-0057-0 Medline
21. T. G. Back, L. Janzen, R. P. Pharis, Z. Yan, Synthesis and bioactivity of C-2 and C-3 methyl
ether derivatives of brassinolide. Phytochemistry 59, 627–634 (2002).
doi:10.1016/S0031-9422(02)00019-5 Medline
22. T. Muto, Y. Todoroki, Brassinolide-2,3-acetonide: A brassinolide-induced rice lamina joint
inclination antagonist. Bioorg. Med. Chem. 21, 4413–4419 (2013).
doi:10.1016/j.bmc.2013.04.048 Medline
23. D. M. Friedrichsen, C. A. Joazeiro, J. Li, T. Hunter, J. Chory, Brassinosteroid-insensitive-1 is
a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant
Physiol. 123, 1247–1256 (2000). doi:10.1104/pp.123.4.1247 Medline
24. Z. Y. Wang, H. Seto, S. Fujioka, S. Yoshida, J. Chory, BRI1 is a critical component of a
plasma-membrane receptor for plant steroids. Nature 410, 380–383 (2001).
doi:10.1038/35066597 Medline
25. Y. Jaillais, Y. Belkhadir, E. Balsemão-Pires, J. L. Dangl, J. Chory, Extracellular leucine-rich
repeats as a platform for receptor/coreceptor complex formation. Proc. Natl. Acad. Sci.
U.S.A. 108, 8503–8507 (2011). doi:10.1073/pnas.1103556108 Medline
26. X. Tan, L. I. Calderon-Villalobos, M. Sharon, C. Zheng, C. V. Robinson, M. Estelle, N.
Zheng, Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640–
645 (2007). doi:10.1038/nature05731 Medline
27. L. B. Sheard, X. Tan, H. Mao, J. Withers, G. Ben-Nissan, T. R. Hinds, Y. Kobayashi, F. F.
Hsu, M. Sharon, J. Browse, S. Y. He, J. Rizo, G. A. Howe, N. Zheng, Jasmonate
perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468, 400–
405 (2010). doi:10.1038/nature09430 Medline
28. D. Chinchilla, C. Zipfel, S. Robatzek, B. Kemmerling, T. Nürnberger, J. D. Jones, G. Felix,
T. Boller, A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant
defence. Nature 448, 497–500 (2007). doi:10.1038/nature05999 Medline
29. B. Schwessinger, M. Roux, Y. Kadota, V. Ntoukakis, J. Sklenar, A. Jones, C. Zipfel,
Phosphorylation-dependent differential regulation of plant growth, cell death, and innate
immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 7, e1002046 (2011).
doi:10.1371/journal.pgen.1002046 Medline
30. M. Roux, B. Schwessinger, C. Albrecht, D. Chinchilla, A. Jones, N. Holton, F. G.
Malinovsky, M. Tör, S. de Vries, C. Zipfel, The Arabidopsis leucine-rich repeat receptor-
like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to
hemibiotrophic and biotrophic pathogens. Plant Cell 23, 2440–2455 (2011).
doi:10.1105/tpc.111.084301 Medline
31. M. Hothorn, W. Van den Ende, W. Lammens, V. Rybin, K. Scheffzek, Structural insights
into the pH-controlled targeting of plant cell-wall invertase by a specific inhibitor protein.
Proc. Natl. Acad. Sci. U.S.A. 107, 17427–17432 (2010). doi:10.1073/pnas.1004481107
Medline
32. Y. Hashimoto, S. Zhang, G. W. Blissard, Ao38, a new cell line from eggs of the black witch
moth, Ascalapha odorata (Lepidoptera: Noctuidae), is permissive for AcMNPV infection
and produces high levels of recombinant proteins. BMC Biotechnol. 10, 50 (2010).
doi:10.1186/1472-6750-10-50 Medline
33. W. Kabsch, Automatic processing of rotation diffraction data from crystals of initially
unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795–800 (1993).
doi:10.1107/S0021889893005588
34. P. Emsley, K. Cowtan, Coot: Model-building tools for molecular graphics. Acta Crystallogr.
60, 2126–2132 (2004). doi:10.1107/S0907444904019158 Medline
35. P. D. Adams, P. V. Afonine, G. Bunkóczi, V. B. Chen, I. W. Davis, N. Echols, J. J. Headd,
L. W. Hung, G. J. Kapral, R. W. Grosse-Kunstleve, A. J. McCoy, N. W. Moriarty, R.
Oeffner, R. J. Read, D. C. Richardson, J. S. Richardson, T. C. Terwilliger, P. H. Zwart,
PHENIX: A comprehensive Python-based system for macromolecular structure solution.
Acta Crystallogr. 66, 213–221 (2010). doi:10.1107/S0907444909052925 Medline
36. I. W. Davis, A. Leaver-Fay, V. B. Chen, J. N. Block, G. J. Kapral, X. Wang, L. W. Murray,
W. B. Arendall 3rd, J. Snoeyink, J. S. Richardson, D. C. Richardson, MolProbity: All-
atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res.
35, W375–W383 (2007). doi:10.1093/nar/gkm216 Medline
37. A. J. McCoy, R. W. Grosse-Kunstleve, P. D. Adams, M. D. Winn, L. C. Storoni, R. J. Read,
Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
doi:10.1107/S0021889807021206 Medline
38. T. C. Terwilliger, R. W. Grosse-Kunstleve, P. V. Afonine, N. W. Moriarty, P. H. Zwart, L.
W. Hung, R. J. Read, P. D. Adams, Iterative model building, structure refinement and
density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. 64, 61–69
(2008). doi:10.1107/S090744490705024X Medline
39. T. D. Fenn, D. Ringe, G. A. Petsko, POVScript+: A program for model and data
visualization using persistence of vision ray-tracing. J. Appl. Crystallogr. 36, 944–947
(2003). doi:10.1107/S0021889803006721
40. Y. Yin, Z. Y. Wang, S. Mora-Garcia, J. Li, S. Yoshida, T. Asami, J. Chory, BES1
accumulates in the nucleus in response to brassinosteroids to regulate gene expression
and promote stem elongation. Cell 109, 181–191 (2002). doi:10.1016/S0092-
8674(02)00721-3 Medline
41. R. A. Laskowski, M. B. Swindells, LigPlot+: Multiple ligand-protein interaction diagrams
for drug discovery. J. Chem. Inf. Model. 51, 2778–2786 (2011). doi:10.1021/ci200227u
Medline
42. D. Li, L. Wang, M. Wang, Y. Y. Xu, W. Luo, Y. J. Liu, Z. H. Xu, J. Li, K. Chong,
Engineering OsBAK1 gene as a molecular tool to improve rice architecture for high
yield. Plant Biotechnol. J. 7, 791–806 (2009). doi:10.1111/j.1467-7652.2009.00444.x
Medline
43. C. Albrecht, E. Russinova, B. Kemmerling, M. Kwaaitaal, S. C. de Vries, Arabidopsis
SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-
dependent and -independent signaling pathways. Plant Physiol. 148, 611–619 (2008).
doi:10.1104/pp.108.123216 Medline
44. T. Slotte, K. M. Hazzouri, J. A. Agren, D. Koenig, F. Maumus, Y. L. Guo, K. Steige, A. E.
Platts, J. S. Escobar, L. K. Newman, W. Wang, T. Mandáková, E. Vello, L. M. Smith, S.
R. Henz, J. Steffen, S. Takuno, Y. Brandvain, G. Coop, P. Andolfatto, T. T. Hu, M.
Blanchette, R. M. Clark, H. Quesneville, M. Nordborg, B. S. Gaut, M. A. Lysak, J.
Jenkins, J. Grimwood, J. Chapman, S. Prochnik, S. Shu, D. Rokhsar, J. Schmutz, D.
Weigel, S. I. Wright, The Capsella rubella genome and the genomic consequences of
rapid mating system evolution. Nat. Genet. 45, 831–835 (2013). doi:10.1038/ng.2669
Medline
45. W. Kabsch, C. Sander, Dictionary of protein secondary structure: Pattern recognition of
hydrogen-bonded and geometrical features. Biopolymers 22, 2577–2637 (1983).
doi:10.1002/bip.360221211 Medline