Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis

Nature Communications

Volumn 5, Issue , 2014, Pages

  Sakuraba, Yasuhito ^a   Jeong, Jinkil ^b   Kang, Min Young ^a   Kim, Junghyun ^b   Paek, Nam Chon ^a   Choi, Giltsu ^b  

^a Seoul National University   (South Korea)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ABI5 PROTEIN; ABSCISIC ACID; EEL PROTEIN; EIN3 PROTEIN; ELF3 PROTEIN; ETHYLENE; PHYTOCHROME; PHYTOCHROME B; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PIF4; TRANSCRIPTION FACTOR PIF5; UNCLASSIFIED DRUG; ABI5 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; EEL PROTEIN, ARABIDOPSIS; EIN3 PROTEIN, ARABIDOPSIS; NUCLEAR PROTEIN; PIF4 PROTEIN, ARABIDOPSIS; PIF5 PROTEIN, ARABIDOPSIS;

DICOTYLEDON; GENE EXPRESSION; LEAF; MOLECULAR ANALYSIS; PHYTOCHEMISTRY; SENESCENCE; SIGNAL;

ARABIDOPSIS THALIANA; ARTICLE; BINDING SITE; COTYLEDON; DOWN REGULATION; GENE INTERACTION; GENE REPRESSION; IMMUNOBLOTTING; LEAF SENESCENCE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DEGRADATION; PROTEIN PROCESSING; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; UPREGULATION; WILD TYPE; AGING; ARABIDOPSIS; GENETICS; LIGHT; MUTATION; PHYSIOLOGY; PLANT LEAF;

AGING; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; LIGHT; MUTATION; NUCLEAR PROTEINS; PHYTOCHROME; PLANT LEAVES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84907345135     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5636     Document Type: Article

References (69)

1. Lim, P. O., Kim, H. J. &Nam, H. G. Leaf senescence. Annu. Rev. Plant Biol. 58, 115-136 (2007).
2. Rousseaux, M. C., Hall, A. J. &Sánchez, R. A. Far-red enrichment and photosynthetically active radiation level influence leaf senescence in fieldgrown sunflower. Physiol. Plant. 96, 217-224 (1996).
3. Liu, X. et al. LSD: a leaf senescence database. Nucleic Acids Res. 39, D1103-D1107 (2011).
4. Kim, J. H. et al. Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323, 1053-1057 (2009).
5. Balazadeh, S., Riano-Pachón, D. M. &Mueller-Roeber, B. Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol. 10, 63-75 (2008). (Pubitemid 352020109)
6. Balazadeh, S. et al. A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J. 62, 250-264 (2010).
7. Matallana-Ramirez, L. P. et al. NAC transcription factor ORE1 and senescence induced BIFUNCTIONAL NUCLEASE1 (BFN1) constitute a regulatory cascade in Arabidopsis. Mol. Plant 6, 14321452 (2013).
8. He, X.-J. et al. AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J. 44, 903-916 (2005). (Pubitemid 43906720)
9. Guo, Y. &Gan, S. AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46, 601-612 (2006).
10. Kim, Y.-S., Sakuraba, Y., Han, S.-H., Yoo, S.-C. &Paek, N.-C. Mutation of the Arabidopsis NAC016 transcription factor delays leaf senescence. Plant Cell Physiol. 54, 1660-1672 (2013).
11. Yang, S.-D., Seo, P. J., Yoon, H.-K. &Park, C.-M. The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23, 2155-2168 (2011).
12. Wu, A. et al. JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24, 482-506 (2012).
13. Gepstein, S. &Thimann, K. V. The role of ethylene in the senescence of Oat leaves. Plant Physiol. 68, 349-354 (1981).
14. Grbić, V. &Bleecker, A. B. Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J. 8, 595-602 (1995).
15. Oh, S. A. et al. Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J. 12, 527-535 (1997). (Pubitemid 27434032)
16. Li, Z., Peng, J., Wen, X. &Guo, H. ETHYLENE-INSENSITIVE3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 25, 3311-3328 (2013).
17. Nooden, L. D. &Leopold, A. C. Senescence and Aging in Plants (Academic Press, 1988).
18. Lee, I. C. et al. Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves. Plant Cell Physiol. 52, 651-662 (2011).
19. Zhang, K., Xia, X., Zhang, Y. &Gan, S.-S. An ABA-regulated and Golgilocalized protein phosphatase controls water loss during leaf senescence in Arabidopsis. Plant J. 69, 667-678 (2012).
20. Ueda, J., Kato, J., Yamane, H. &Takahashi, N. Inhibitory effect of methyl jasmonate and its related compounds on kinetin-induced retardation of oat leaf senescence. Physiol. Plant. 52, 305-309 (1981).
21. Morris, K. et al. Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J. 23, 677-685 (2000).
22. Gan, S. &Amasino, R. M. Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270, 1986-1988 (1995). (Pubitemid 26097187)
23. Whitelam, G. C. &Halliday, K. J. Light and Plant Development (Blackwell, 2007).
24. Biswal, U. C. &Biswal, B. Photocontrol of leaf senescence. Photochem. Photobiol. 39, 875-879 (1984).
25. Rousseaux, M. C., Ballaré, C. L., Jordan, E. T. &Vierstra, R. D. Directed overexpression of PHYA locally suppresses stem elongation and leaf senescence responses to far-red radiation. Plant Cell Environ. 20, 1551-1558 (1997). (Pubitemid 28073222)
26. Jeong, J. &Choi, G. Phytochrome-interacting factors have both shared and distinct biological roles. Mol. Cells 35, 371-380 (2013).
27. Park, E. et al. Phytochrome B inhibits binding of phytochrome-interacting factors to their target promoters. Plant J. 72, 537-546 (2012).
28. Bauer, D. et al. Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16, 1433-1445 (2004). (Pubitemid 38774240)
29. Park, E. et al. Degradation of phytochrome interacting factor 3 in phytochrome-mediated light signaling. Plant Cell Physiol. 45, 968-975 (2004). (Pubitemid 39260274)
30. Nusinow, D. A. et al. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475, 398-402 (2011).
31. Borthwick, H. A., Hendricks, S. B., Toole, E. H. &Toole, V. K. Action of light on lettuce-seed germination. Bot. Gaz. 115, 205-225 (1954).
32. Leivar, P. et al. Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr. Biol. 18, 1815-1823 (2008).
33. Shin, J. et al. Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome-interacting factors. Proc. Natl Acad. Sci. USA 106, 7660-7665 (2009).
34. Hornitschek, P. et al. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 71, 699-711 (2012).
35. Liu, X. L., Covington, M. F., Fankhauser, C., Chory, J. &Wagner, D. R. ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13, 1293-1304 (2001). (Pubitemid 32592904)
36. Yu, J.-W. et al. COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol. Cell 32, 617-630 (2008).
37. Imaizumi, T. Arabidopsis circadian clock and photoperiodism: time to think about location. Curr. Opin. Plant Biol. 13, 83-89 (2010).
38. Keller, M. M. et al. Cryptochrome 1 and phytochrome B control shadeavoidance responses in Arabidopsis via partially-independent hormonal cascades. Plant J. 67, 195-207 (2011).
39. van der Graaff, E. et al. Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol. 141, 776-792 (2006). (Pubitemid 43974570)
40. Oh, E., Zhu, J. Y. &Wang, Z. Y. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802-809 (2012).
41. Martinez-Garcia, J. F., Huq, E. &Quail, P. H. Direct targeting of light signals to a promoter element-bound transcription factor. Science 288, 859-863 (2000). (Pubitemid 30257735)
42. Zhang, Y. et al. A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis. PLoS Genet. 9, e1003244 (2013).
43. Oh, E. et al. Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 21, 403-419 (2009).
44. Choi, H., Hong, J., Ha, J., Kang, J. &Kim, S. Y. ABFs, a family of ABAresponsive element binding factors. J. Biol. Chem. 275, 1723-1730 (2000). (Pubitemid 30060792)
45. Park, S.-Y. et al. The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19, 1649-1664 (2007). (Pubitemid 47025383)
46. Kusaba, M. et al. Rice NON-YELLOW COLORING1 is involved in lightharvesting complex II and grana degradation during leaf senescence. Plant Cell 19, 1362-1375 (2007). (Pubitemid 46941659)
47. Koini, M. A. et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408-413 (2009).
48. Le, D.-H. &Kwon, Y.-K. A coherent feedforward loop design principle to sustain robustness of biological networks. Bioinformatics 29, 630-637 (2013).
49. Kim, H. J. et al. Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis. J. Exp. Bot. 65, 4023-4036 (2014).
50. Reed, J. W. et al. Independent action of ELF3 and phyB to control hypocotyl elongation and flowering time. Plant Physiol. 122, 1149-1160 (2000). (Pubitemid 30221394)
51. Hicks, K. A. et al. Conditional circadian dysfunction of the Arabidopsis earlyflowering 3 mutant. Science 274, 790-792 (1996).
52. Lu, S. X. et al. CCA1 and ELF3 interact in the control of hypocotyl length and flowering time in Arabidopsis. Plant Physiol. 158, 1079-1088 (2012).
53. Cherry, J. R., Hershey, H. P. &Vierstra, R. D. Characterization of tobacco expressing functional Oat phytochrome: domains responsible for the rapid degradation of Pfr are conserved between monocots and dicots. Plant Physiol. 96, 775-785 (1991). (Pubitemid 21914082)
54. Weller, J. L., Murfet, I. C. &Reid, J. B. Pea mutants with reduced sensitivity to far-red light define an important role for phytochrome A in day-length detection. Plant Physiol. 114, 1225-1236 (1997). (Pubitemid 28382284)
55. Whitelam, G. C. et al. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5, 757-768 (1993).
56. Boylan, M. T. &Quail, P. H. Phytochrome A overexpression inhibits hypocotyl elongation in transgenic Arabidopsis. Proc. Natl Acad. Sci. USA 88, 10806-10810 (1991). (Pubitemid 21915927)
57. Reed, J. W., Nagatani, A., Elich, T. D., Fagan, M. &Chory, J. Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol. 104, 1139-1149 (1994).
58. Biswal, B. &Choudhury, N. K. Photocontrol of chlorophyll loss in papaya leaf discs. Plant Cell Physiol. 27, 1439-1444 (1986).
59. Meng, Y., Li, H., Wang, Q., Liu, B. &Lin, C. Blue light-dependent interaction between cryptochrome2 and CIB1 regulates transcription and leaf senescence in Soybean. Plant Cell 25, 4405-4420 (2013).
60. Guiamet, J. J., Willemoes, J. G. &Montaldi, E. R. Modulation of progressive leaf senescence by the red:far-red ratio of incident light. Bot. Gaz. 150, 148-151 (1989).
61. Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R. &Abrams, S. R. Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679 (2010).
62. Lopez-Molina, L. &Chua, N. H. A null mutation in a bZIP factor confers ABAinsensitivity in Arabidopsis thaliana. Plant Cell Physiol. 41, 541-547 (2000). (Pubitemid 30388055)
63. Lichtenthaler, H. K. in Methods in Enzymology Vol. 148 (eds Douce, R. &Packer, L.) 350-382 (Academic Press, 1987).
64. Smyth, G. K. in Bioinformatics and Computational Biology Solutions Using R and Bioconductor Statistics for Biology and Health Ch. 23 (eds Gentleman, R. et al.) 397-420 (Springer, 2005).
65. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005). (Pubitemid 41528093)
66. Nemhauser, J. L., Hong, F. &Chory, J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126, 467-475 (2006). (Pubitemid 44163606)
67. Fujita, Y. et al. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 50, 2123-2132 (2009).
68. Reeves, W. M., Lynch, T. J., Mobin, R. &Finkelstein, R. R. Direct targets of the transcription factors ABA-insensitive(ABI)4 and ABI5 reveal synergistic action by ABI4 and several bZIP ABA response factors. Plant Mol. Biol. 75, 347-363 (2011).
69. Usadel, B. et al. Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol. 146, 1834-1861 (2008).(Pubitemid 352844087)