Solution structure of the PsIAA4 oligomerization domain reveals interaction modes for transcription factors in early auxin response

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 19, 2015, Pages 6230-6235

  Dinesh, Dhurvas Chandrasekaran ^a   Kovermann, Michael ^b,e   Gopalswamy, Mohanraj ^b,f   Hellmuth, Antje ^a   Villalobos, Luz Irina A Calderón ^a   Lilie, Hauke ^c   Balbach, Jochen ^b   Abel, Steffen ^a,c,d  

^a LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^b Institute of Physics Biophysics and Mitteldeutsches Zentrum fur Struktur und Dynamik der Proteine   (Germany)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UMEÅ UNIVERSITY   (Sweden)

^f Munich Center for Integrated Protein Science   (Germany)

Author keywords

AUX IAA proteins; Auxin signaling; NMR structure; PB1 domain; Transcription factors

Indexed keywords

AUXIN; TRANSCRIPTION FACTOR; AMINO ACID; ARABIDOPSIS PROTEIN; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE; PROTEIN BINDING; VEGETABLE PROTEIN;

ARTICLE; BINDING AFFINITY; CALORIMETRY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA BINDING; GENE EXPRESSION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HYDROGEN BOND; MOLECULAR INTERACTION; OLIGOMERIZATION; PEA; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY; STOICHIOMETRY; TITRIMETRY; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PH; PROTEIN ANALYSIS; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

PISUM SATIVUM;

AMINO ACID SEQUENCE; AMINO ACIDS; ARABIDOPSIS PROTEINS; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION REGULATION, PLANT; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; INDOLEACETIC ACIDS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PEAS; PLANT PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84929224112     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1424077112     Document Type: Article

References (42)

1. Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265-285.
2. Tan X, et al. (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446(7136):640-645.
3. Calderón Villalobos LI, et al. (2012) A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat Chem Biol 8(5):477-485.
4. Wang R, Estelle M (2014) Diversity and specificity: Auxin perception and signaling through the TIR1/AFB pathway. Curr Opin Plant Biol 21:51-58.
5. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414(6861):271-276.
6. Kim J, Harter K, Theologis A (1997) Protein-protein interactions among the Aux/IAA proteins. Proc Natl Acad Sci USA 94(22):11786-11791.
7. Vernoux T, et al. (2011) The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 7:508.
8. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10(5):453-460.
9. Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319(5868):1384-1386.
10. Krogan NT, Hogan K, Long JA (2012) APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139(22):4180-4190.
11. Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111(1):9-17.
12. Abel S, Nguyen MD, Theologis A (1995) The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J Mol Biol 251(4):533-549.
13. Boer DR, et al. (2014) Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 156(3):577-589.
14. Burroughs AM, Balaji S, Iyer LM, Aravind L (2007) Small but versatile: The extraordinary functional and structural diversity of the beta-grasp fold. Biol Direct 2:18.
15. Sumimoto H, Kamakura S, Ito T (2007) Structure and function of the PB1 domain, a protein interaction module conserved in animals, fungi, amoebas, and plants. Sci STKE 2007(401):re6.
16. Guilfoyle TJ, Hagen G (2012) Getting a grasp on domain III/IV responsible for Auxin Response Factor-IAA protein interactions. Plant Sci 190:82-88.
17. Nanao MH, et al. (2014) Structural basis for oligomerization of auxin transcriptional regulators. Nat Commun 5:3617-3624.
18. Korasick DA, et al. (2014) Molecular basis for AUXIN RESPONSE FACTOR protein interaction and the control of auxin response repression. Proc Natl Acad Sci USA 111(14):5427-5432.
19. Han M, et al. (2014) Structural basis for the auxin-induced transcriptional regulation by Aux/IAA17. Proc Natl Acad Sci USA 111(52):18613-18618.
20. Abel S, Theologis A (2010) Odyssey of auxin. Cold Spring Harb Perspect Biol 2(10):a004572.
21. Theologis A, Ray PM (1982) Early auxin-regulated polyadenylylated mRNA sequences in pea stem tissue. Proc Natl Acad Sci USA 79(2):418-421.
22. Theologis A, Huynh TV, Davis RW (1985) Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J Mol Biol 183(1):53-68.
23. Oeller PW, Keller JA, Parks JE, Silbert JE, Theologis A (1993) Structural characterization of the early indoleacetic acid-inducible genes, PS-IAA4/5 and PS-IAA6, of pea (Pisum sativum L.). J Mol Biol 233(4):789-798.
24. Ballas N, Wong LM, Theologis A (1993) Identification of the auxin-responsive element, AuxRE, in the primary indoleacetic acid-inducible gene, PS-IAA4/5, of pea (Pisum sativum). J Mol Biol 233(4):580-596.
25. Abel S, Oeller PW, Theologis A (1994) Early auxin-induced genes encode short-lived nuclear proteins. Proc Natl Acad Sci USA 91(1):326-330.
26. Oeller PW, Theologis A (1995) Induction kinetics of the nuclear proteins encoded by the early indoleacetic acid-inducible genes, PS-IAA4/5 and PS-IAA6, in pea (Pisum sativum L.). Plant J 7(1):37-48.
27. Koshiba T, Ballas N, Wong LM, Theologis A (1995) Transcriptional regulation of PS-IAA4/5 and PS-IAA6 early gene expression by indoleacetic acid and protein synthesis inhibitors in pea (Pisum sativum). J Mol Biol 253(3):396-413.
28. Ballas N, Wong LM, Ke M, Theologis A (1995) Two auxin-responsive domains interact positively to induce expression of the early indoleacetic acid-inducible gene PS-IAA4/5. Proc Natl Acad Sci USA 92(8):3483-3487.
29. Wong LM, et al. (1996) Differential activation of the primary auxin response genes, PS-IAA4/5 and PS-IAA6, during early plant development. Plant J 9(5):587-599.
30. Colón-Carmona A, Chen DL, Yeh KC, Abel S (2000) Aux/IAA proteins are phosphorylated by phytochrome in vitro. Plant Physiol 124(4):1728-1738.
31. Morgan KE, Zarembinski TI, Theologis A, Abel S (1999) Biochemical characterization of recombinant polypeptides corresponding to the predicted βαα fold in Aux/IAA proteins. FEBS Lett 454(3):283-287.
32. Rieping W, et al. (2007) ARIA2: Automated NOE assignment and data integration in NMR structure calculation. Bioinformatics 23(3):381-382.
33. Abel S, Theologis A (1995) A polymorphic bipartite motif signals nuclear targeting of early auxin-inducible proteins related to PS-IAA4 from pea (Pisum sativum). Plant J 8(1):87-96.
34. Dominguez C, Boelens R, Bonvin AM (2003) HADDOCK: A protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125(7):1731-1737.
35. Theologis A (1989) Auxin-regulated gene expression in plants. Biotechnology 12: 229-243.
36. Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: Biochemical insight into an auxin mutant phenotype. Plant Cell 13(4):829-841.
37. Rouse D, Mackay P, Stirnberg P, Estelle M, Leyser O (1998) Changes in auxin response from mutations in an AUX/IAA gene. Science 279(5355):1371-1373.
38. Delaglio F, et al. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6(3):277-293.
39. Johnson BA, Blevins RA (1994) NMR View: A computer program for the visualization and analysis of NMR data. J Biomol NMR 4(5):603-614.
40. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13(3):289-302.
41. Ramachandran GN, Ramakrishnan C, Sasisekharan V (1963) Stereochemistry of polypeptide chain configurations. J Mol Biol 7:95-99.
42. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8(4):477-486.