Peptidyl-prolyl isomerization targets rice Aux/IAAs for proteasomal degradation during auxin signalling

Nature Communications

Volumn 6, Issue , 2015, Pages

  Jing, Hongwei ^a,b   Yang, Xiaolu ^a,b   Zhang, Jian ^a   Liu, Xuehui ^c   Zheng, Huakun ^a,b   Dong, Guojun ^d   Nian, Jinqiang ^a   Feng, Jian ^a   Xia, Bin ^e   Qian, Qian ^d   Li, Jiayang ^a   Zuo, Jianru ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

^d INSTITUTE OF PLANT PROTECTION   (China)

^e PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; CYCLOPHILIN; INDOLEACETIC ACID; LATERAL ROOTLESS2 PROTEIN; PEPTIDYLPROLYL ISOMERASE; PROTEIN TIR1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; AUXIN RECEPTOR, PLANT; CELL SURFACE RECEPTOR; INDOLEACETIC ACID DERIVATIVE; PROTEASOME; REPRESSOR PROTEIN; VEGETABLE PROTEIN;

BIOACCUMULATION; BIODEGRADATION; ENZYME ACTIVITY; GENE EXPRESSION; HORMONE; MUTATION; NUCLEAR MAGNETIC RESONANCE; PHENOTYPE; PROTEIN; PROTEOMICS; RICE; ROOT SYSTEM; SPECTROSCOPY;

ARTICLE; CATALYSIS; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GENE SILENCING; IN VITRO STUDY; ISOMERIZATION; NONHUMAN; PHENOTYPE; PLASMID; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; RICE; ROOT DEVELOPMENT; SIGNAL TRANSDUCTION; STOP CODON; GENETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ORYZA;

CYCLOPHILINS; INDOLEACETIC ACIDS; MAGNETIC RESONANCE SPECTROSCOPY; ORYZA; PEPTIDYLPROLYL ISOMERASE; PLANT PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; RECEPTORS, CELL SURFACE; REPRESSOR PROTEINS;

EID: 84934967910     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8395     Document Type: Article

References (60)

1. Dharmasiri, N. & Estelle, M. Auxin signaling and regulated protein degradation. Trends Plant Sci. 9, 302-308 (2004).
2. Peer, W. A. From perception to attenuation: auxin signalling and responses. Curr. Opin. Plant Biol. 16, 561-568 (2013).
3. Wang, R. & Estelle, M. Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway. Curr. Opin. Plant Biol. 21, 51-58 (2014).
4. Kepinski, S. & Leyser, O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446-451 (2005).
5. Dharmasiri, N., Dharmasiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445 (2005).
6. Tan, X. et al. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640-645 (2007).
7. Gray, W. M., Kepinski, S., Rouse, D., Leyser, O. & Estelle, M. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271-276 (2001).
8. Tiwari, S. B., Wang, X.-J., Hagen, G. & Guilfoyle, T. J. AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13, 2809-2822 (2001).
9. Liscum, E. & Reed, J. W. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol. Biol. 49, 387-400 (2002).
10. Reed, J. W. Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 6, 420-425 (2001).
11. Mockaitis, K. & Estelle, M. Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24, 55-80 (2008).
12. Ramos, J. A., Zenser, N., Leyser, O. & Callis, J. Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13, 2349-2360 (2001).
13. Tian, Q., Nagpal, P. & Reed, J. W. Regulation of Arabidopsis SHY2/IAA3 protein turnover. Plant J. 36, 643-651 (2003).
14. Yang, X. et al. The IAA1 protein is encoded by AXR5 and is a substrate of SCFTIR1. Plant J. 40, 772-782 (2004).
15. Dharmasiri, N., Dharmasiri, S., Jones, A. M. & Estelle, M. Auxin action in a cell-free system. Curr. Biol. 13, 1418-1422 (2003).
16. Zheng, H. et al. LATERAL ROOTLESS2, a cyclophilin protein, regulates lateral root initiation and auxin signaling pathway in rice. Mol. Plant 6, 1719-1721 (2013).
17. Kang, B. et al. OsCYP2, a chaperone involved in degradation of auxinresponsive proteins, plays crucial roles in rice lateral root initiation. Plant J. 74, 86-97 (2013).
18. Romano, P. G. N., Horton, P. & Gray, J. E. The Arabidopsis cyclophilin gene family. Plant Physiol. 134, 1268-1282 (2004).
19. Lu, K. P., Finn, G., Lee, T. H. & Nicholson, L. K. Prolyl cis-trans isomerization as a molecular timer. Nat. Chem. Biol. 3, 619-629 (2007).
20. Gasser, C. S., Gunning, D. A., Budelier, K. A. & Brown, S. M. Structure and expression of cytosolic cyclophilin/peptidyl-prolyl cis-trans isomerase of higher plants and production of active tomato cyclophilin in Escherichia coli. Proc. Natl Acad. Sci. USA 87, 9519-9523 (1990).
21. Kumari, S., Roy, S., Singh, P., Singla-Pareek, S. & Pareek, A. Cyclophilins: proteins in search of function. Plant Signal Behav. 8, e22734 (2013).
22. Vasudevan, D. et al. Plant immunophilins: a review of their structure-function relationship. Biochim. Biophys. Acta doi:10.1016/j.bbagen.2014.12.017 (19 December 2014).
23. Trupkin, S. A., Mora-García, S. & Casal, J. J. The cyclophilin ROC1 links phytochrome and cryptochrome to brassinosteroid sensitivity. Plant J. 71, 712-723 (2012).
24. Ma, X., Song, L., Yang, Y. & Liu, D. A gain-of-function mutation in the ROC1 gene alters plant architecture in Arabidopsis. New Phytol. 197, 751-762 (2013).
25. Zhang, Y. et al. The cyclophilin CYP20-2 modulates the conformation of BRASSINAZOLE-RESISTANT1, which binds the promoter of FLOWERING LOCUS D to regulate flowering in Arabidopsis. Plant Cell 25, 2504-2521 (2013).
26. Wang, Y., Liu, C., Yang, D., Yu, H. & Liou, Y.-C. Pin1At encoding a peptidylprolyl cis/trans isomerase regulates flowering time in Arabidopsis. Mol. Cell 37, 112-122 (2010).
27. Li, M. et al. Proline isomerization of the immune receptor-interacting protein RIN4 by a cyclophilin inhibits effector-triggered immunity in Arabidopsis. Cell Host Microbe. 16, 473-483 (2014).
28. Oh, K., Ivanchenko, M., White, T. J. & Lomax, T. The diageotropica gene of tomato encodes a cyclophilin: a novel player in auxin signaling. Planta 224, 133-144 (2006).
29. Ivanchenko, M. G., Coffeen, W. C., Lomax, T. L. & Dubrovsky, J. G. Mutations in the Diageotropica (Dgt) gene uncouple patterned cell division during lateral root initiation from proliferative cell division in the pericycle. Plant J. 46, 436-447 (2006).
30. Lavy, M., Prigge, M. J., Tigyi, K. & Estelle, M. The cyclophilin DIAGEOTROPICA has a conserved role in auxin signaling. Development 139, 1115-1124 (2012).
31. Zhu, Z.-X. et al. A gain-of-function mutation in OsIAA11 affects lateral root development in rice. Mol. Plant 5, 154-161 (2012).
32. Kitomi, Y., Inahashi, H., Takehisa, H., Sato, Y. & Inukai, Y. OsIAA13-mediated auxin signaling is involved in lateral root initiation in rice. Plant Sci. 190, 116-122 (2012).
33. Jun, N. et al. OsIAA23-mediated auxin signaling defines postembryonic maintenance of QC in rice. Plant J. 68, 433-442 (2011).
34. Sekhon, S. S. et al. Structural and biochemical characterization of the cytosolic wheat cyclophilin TaCypA-1. Acta Crystallogr. D Biol. Crystallogr. 69, 555-563 (2013).
35. Reimer, U. et al. Side-chain effects on peptidyl-prolyl cis/trans isomerisation. J. Mol. Biol. 279, 449-460 (1998).
36. Schönbrunner, E. R. et al. Catalysis of protein folding by cyclophilins from different species. J. Biol. Chem. 266, 3630-3635 (1991).
37. Endrich, M. M., Gehrig, P. & Gehring, H. Maturation-induced conformational changes of HIV-1 capsid protein and identification of two high affinity sites for cyclophilins in the C-terminal domain. J. Biol. Chem. 274, 5326-5332 (1999).
38. Kepinski, S. & Leyser, O. Auxin-induced SCFTIR1-Aux/IAA interaction involves stable modification of the SCFTIR1 complex. Proc. Natl Acad. Sci. USA 101, 12381-12386 (2004).
39. Gray, W. M., Muskett, P. R., Chuang, H.-W. & Parker, J. E. Arabidopsis SGT1b is required for SCFTIR1-mediated auxin response. Plant Cell 15, 1310-1319 (2003).
40. Zhao, Y., Dai, X., Blackwell, H. E., Schreiber, S. L. & Chory, J. SIR1, an upstream component in auxin signaling identified by chemical genetics. Science 301, 1107-1110 (2003).
41. Pérez-Pérez, J. M., Ponce, M. R. & Micol, J. L. The ULTRACURVATA2 gene of Arabidopsis encodes an FK506-binding protein involved in auxin and brassinosteroid signaling. Plant Physiol. 134, 101-117 (2004).
42. Li, B. et al. Integrative study on proteomics, molecular physiology, and genetics reveals an accumulation of cyclophilin-like protein, TaCYP20-2, leading to an increase of Rht protein and dwarf in a novel GA-insensitive mutant (gaid) in wheat. J. Proteome Res. 9, 4242-4253 (2010).
43. Park, S.-W. et al. Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. Proc. Natl. Acad. Sci. USA 110, 9559-9564 (2013).
44. Hirano, K., Ueguchi-Tanaka, M. & Matsuoka, M. GID1-mediated gibberellin signaling in plants. Trends Plant Sci. 13, 192-199 (2008).
45. Sun, T.-p. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr. Biol. 21, R338-R345 (2011).
46. Pérez, A. C. & Goossens, A. Jasmonate signalling: a copycat of auxin signalling? Plant Cell Environ. 36, 2071-2084 (2013).
47. Jiang, L. et al. DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504, 401-405 (2013).
48. Zhou, F. et al. D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504, 406-410 (2013).
49. Wang, H., Taketa, S., Miyao, A., Hirochika, H. & Ichii, M. Isolation of a novel lateral-rootless mutant in rice (Oryza sativa L.) with reduced sensitivity to auxin. Plant Sci. 170, 70-77 (2006).
50. Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271-282 (1994).
51. Chen, H. et al. Firefly luciferase complementation imaging assay for proteinprotein interactions in plants. Plant Physiol. 146, 368-376 (2008).
52. Wang, Z. et al. A practical vector for efficient knockdown of gene expression in rice (Oryza sativa L.). Plant Mol. Biol. Rep. 22, 409-417 (2004).
53. Ding, Y.-H., Liu, N.-Y., Tang, Z.-S., Liu, J. & Yang, W.-C. Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 18, 815-830 (2006).
54. Feng, J. et al. S-nitrosylation of phosphotransfer proteins represses cytokinin signaling. Nat. Commun. 4, 1529 (2013).
55. Liu, H. et al. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322, 1535-1539 (2008).
56. Nakamura, A. et al. Production and characterization of auxin-insensitive rice by overexpression of a mutagenized rice IAA protein. Plant J. 46, 297-306 (2006).
57. Dharmasiri, N. et al. Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9, 109-119 (2005).
58. Ramelot, T. A. & Nicholson, L. K. Phosphorylation-induced structural changes in the amyloid precursor protein cytoplasmic tail detected by NMR. J. Mol. Biol. 307, 871-884 (2001).
59. Pastorino, L. et al. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-b production. Nature 440, 528-534 (2006).
60. Pastorino, L. et al. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-b production. Nature 446, 342-342 (2007).