[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.14348/molcells.2016.0126

PIF4 Integrates Multiple Environmental and Hormonal Signals for Plant Growth Regulation in Arabidopsis

Choi, Hyunmo (Forest Biotechnology Division, National Institute of Forest Science)
Oh, Eunkyoo (Department of Bioenergy Science and Technology, Chonnam National University)

Abstract

As sessile organisms, plants must be able to adapt to the environment. Plants respond to the environment by adjusting their growth and development, which is mediated by sophisticated signaling networks that integrate multiple environmental and endogenous signals. Recently, increasing evidence has shown that a bHLH transcription factor PIF4 plays a major role in the multiple signal integration for plant growth regulation. PIF4 is a positive regulator in cell elongation and its activity is regulated by various environmental signals, including light and temperature, and hormonal signals, including auxin, gibberellic acid and brassinosteroid, both transcriptionally and post-translationally. Moreover, recent studies have shown that the circadian clock and metabolic status regulate endogenous PIF4 level. The PIF4 transcription factor cooperatively regulates the target genes involved in cell elongation with hormone-regulated transcription factors. Therefore, PIF4 is a key integrator of multiple signaling pathways, which optimizes growth in the environment. This review will discuss our current understanding of the PIF4-mediated signaling networks that control plant growth.

Keywords

brassinosteroid; high temperature; light; PIF4; signaling integration;

Citations & Related Records

Times Cited By KSCI : 1 (Citation Analysis)

Reference
Cited By KSCI

1	Khanna, R., Huq, E., Kikis, E.A., Al-Sady, B., Lanzatella, C., and Quail, P.H. (2004) A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell 16, 3033-3044. DOI
2	Khanna, R., Shen, Y., Marion, C.M., Tsuchisaka, A., Theologis, A., Schafer, E., and Quail, P.H. (2007) The basic helix-loop-helix transcription factor PIF5 acts on ethylene biosynthesis and phytochrome signaling by distinct mechanisms. Plant Cell 19, 3915-3929. DOI
3	Kim, J., Yi, H., Choi, G., Shin, B., Song, P.S., and Choi, G. (2003). Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15, 2399-2407. DOI
4	Koini, M.A., Alvey, L., Allen, T., Tilley, C.A., Harberd, N.P., Whitelam, G.C., and Franklin, K.A. (2009). High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408-413.
5	Kumar, S.V., and Wigge, P.A. (2010). H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136-147. DOI
6	Kumar, S.V., Lucyshyn, D., Jaeger, K.E., Alos, E., Alvey, E., Harberd, N.P., and Wigge, P.A. (2012). Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484, 242-245. DOI
7	Lee, H.J., Jung, J.H., Cortes Llorca, L., Kim, S.G., Lee, S., Baldwin, I.T., and Park, C.M. (2014). FCA mediates thermal adaptation of stem growth by attenuating auxin action in Arabidopsis. Nat. Commun. 5, 5473. DOI
8	Leivar, P., and Quail, P.H. (2011). PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16, 19-28.
9	Leivar, P., Tepperman, J.M., Monte, E., Calderon, R.H., Liu, T.L., and Quail, P.H. (2009). Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell 21, 3535-3553. DOI
10	Lorrain, S., Allen, T., Duek, P.D., Whitelam, G.C., and Fankhauser, C. (2008). Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 53, 312-323.
11	Lorrain, S., Trevisan, M., Pradervand, S., and Fankhauser, C. (2009). Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J. 60, 449-461. DOI
12	Lucyshyn, D., and Wigge, P.A. (2009). Plant development: PIF4 integrates diverse environmental signals. Curr. Biol. 19, R265-266. DOI
13	Ma, D., Li, X., Guo, Y., Chu, J., Fang, S., Yan, C., Noel, J.P., and Liu, H. (2016). Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light. Proc. Natl. Acad. Sci. USA 113, 224-229. DOI
14	Mizuno, T., Nomoto, Y., Oka, H., Kitayama, M., Takeuchi, A., Tsubouchi, M., and Yamashino, T. (2014) Ambient temperature signal feeds into the circadian clock transcriptional circuitry through the EC night-time repressor in Arabidopsis thaliana. Plant Cell Physiol. 55, 958-976. DOI
15	Ni, M., Tepperman, J.M., and Quail, P.H. (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95, 657-667. DOI
16	Oh, E., Zhu, J.Y., and Wang, Z.Y. (2012). Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802-809. DOI
17	Ni, W., Xu, S.L., Tepperman, J.M., Stanley, D.J., Maltby, D.A., Gross, J.D., Burlingame, A.L., Wang, Z.Y. and Quail, P.H. (2014) A mutually assured destruction mechanism attenuates light signaling in Arabidopsis. Science 344, 1160-1164. DOI
18	Nozue, K., Covington, M.F., Duek, P.D., Lorrain, S., Fankhauser, C., Harmer, S.L., and Maloof, J.N. (2007). Rhythmic growth explained by coincidence between internal and external cues. Nature 448, 358-361. DOI
19	Nusinow, D.A., Helfer, A., Hamilton, E.E., King, J.J., Imaizumi, T., Schultz, T.F., Farre, E.M., and Kay, S.A. (2011). The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475, 398-402. DOI
20	Oh, E., Zhu, J.Y., Bai, M.Y., Arenhart, R.A., Sun, Y., and Wang, Z.Y. (2014). Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife 3, e03031.
21	Park, E., Park, J., Kim, J., Nagatani, A., Lagarias, J.C. and Choi, G. (2012). Phytochrome B inhibits binding of phytochromeinteracting factors to their target promoters. Plant J. 72, 537-546. DOI
22	Pedmale, U.V., Huang, S.S., Zander, M., Cole, B.J., Hetzel, J., Ljung, K., Reis, P.A., Sridevi, P., Nito, K., Nery, J.R., et al. (2016). Cryptochromes interact directly with PIFs to control plant growth in limiting blue light. Cell 164, 233-245. DOI
23	Pfeiffer, A., Shi, H., Tepperman, J.M., Zhang, Y., and Quail, P.H. (2014). Combinatorial complexity in a transcriptionally centered signaling hub in Arabidopsis. Mol. Plant 7, 1598-1618. DOI
24	Seaton, D.D., Smith, R.W., Song, Y.H., MacGregor, D.R., Stewart, K., Steel, G., Foreman, J., Penfield, S., Imaizumi, T., Millar, A.J., et al. (2015). Linked circadian outputs control elongation growth and flowering in response to photoperiod and temperature. Mol. Syst. Biol. 11, 776. DOI
25	Quint, M., Delker, C., Franklin, K.A., Wigge, P.A., Halliday, K.J., and Zanten, M. (2016). Molecular and genetic control of plant thermomorphogenesis. Nat. Plants 2, 15190. DOI
26	Raschke, A., Ibanez, C., Ullrich, K.K., Anwer, M.U., Becker, S., Glockner, A., Trenner, J., Denk, K., Saal, B., Sun, X., et al. (2015). Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes. BMC Plant Biol. 15, 197. DOI
27	Sakuraba, Y., Jeong, J., Kang, M.Y., Kim, J., Paek, N.C., and Choi, G. (2014). Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat. Commun. 5, 4636. DOI
28	Shen, Y., Khanna, R., Carle, C.M., and Quail, P.H. (2007). Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol. 145, 1043-1051. DOI
29	Shin, J., Kim, K., Kang, H., Zulfugarov, I.S., Bae, G., Lee, C.H., Lee, D., and Choi, G. (2009). Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochromeinteracting factors. Proc. Natl. Acad. Sci. USA 106, 7660-7665. DOI
30	Song, Y., Yang, C., Gao, S., Zhang, W., Li, L., and Kuai, B. (2014) Age-triggered and dark-induced leaf senescence require the bHLH transcription factors PIF3, 4, and 5. Mol. Plant 7, 1776-1787. DOI
31	Sun, J., Qi, L., Li, Y., Zhai, Q., and Li, C. (2013). PIF4 and PIF5 transcription factors link blue light and auxin to regulate the phototropic response in Arabidopsis. Plant Cell 25, 2102-2114. DOI
32	Stavang, J.A., Gallego-Bartolome, J., Gomez, M.D., Yoshida, S., Asami, T., Olsen, J.E., Garcia-Martinez, J.L., Alabadi, D., and Blazquez, M.A. (2009). Hormonal regulation of temperatureinduced growth in Arabidopsis. Plant J. 60, 589-601. DOI
33	Sun, T.P. (2011). The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21, R338-345. DOI
34	Sun, J., Qi, L., Li, Y., Chu, J., and Li, C. (2012). PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating arabidopsis hypocotyl growth. PLoS Genet. 8, e1002594. DOI
35	Wang, Z.Y., Bai, M.Y., Oh, E., and Zhu, J.Y. (2012). Brassinosteroid signaling network and regulation of photomorphogenesis. Annu. Rev. Genet. 46, 701-724. DOI
36	Yamashino, T., Matsushika, A., Fujimori, T., Sato, S., Kato, T., Tabata, S., and Mizuno, T. (2003). A Link between circadiancontrolled bHLH factors and the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol. 44, 619-629. DOI
37	Yamashino, T., Nomoto, Y., Lorrain, S., Miyachi, M., Ito, S., Nakamichi, N., Fankhauser, C., and Mizuno, T. (2013). Verification at the protein level of the PIF4-mediated external coincidence model for the temperature-adaptive photoperiodic control of plant growth in Arabidopsis thaliana. Plant Signal. Behav. 8, e23390. DOI
38	Al-Sady, B., Ni, W., Kircher, S., Schafer, E. and Quail, P.H. (2006). Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol. Cell 23, 439-446. DOI
39	Zhang, Y., Mayba, O., Pfeiffer, A., Shi, H., Tepperman, J.M., Speed, T.P., and Quail, P.H. (2013). 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. DOI
40	Zhang, D., Jing, Y., Jiang, Z., and Lin, R. (2014). The chromatinremodeling factor PICKLE integrates brassinosteroid and gibberellin signaling during skotomorphogenic growth in Arabidopsis. Plant Cell 26, 2472-2485. DOI
41	Bai, M.Y., Shang, J.X., Oh, E., Fan, M., Bai, Y., Zentella, R., Sun, T.P., and Wang, Z.Y. (2012). Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat. Cell Biol. 14, 810-817. DOI
42	Bernardo-Garcia, S., de Lucas, M., Martinez, C., Espinosa-Ruiz, A., Daviere, J.M., and Prat, S. (2014). BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth. Genes Dev. 28, 1681-1694. DOI
43	Box, M.S., Huang, B.E., Domijan, M., Jaeger, K.E., Khattak, A.K., Yoo, S.J., Sedivy, E.L., Jones, D.M., Hearn, T.J., Webb, A.A., et al. (2015). ELF3 controls thermoresponsive growth in Arabidopsis. Curr. Biol. 25, 194-199. DOI
44	Crawford, A.J., McLachlan, D.H., Hetherington, A.M., and Franklin, K.A. (2012). High temperature exposure increases plant cooling capacity. Curr. Biol. 22, R396-397. DOI
45	Casson, S.A., Franklin, K.A., Gray, J.E., Grierson, C.S., Whitelam, G.C., and Hetherington, A.M. (2009). phytochrome B and PIF4 regulate stomatal development in response to light quantity. Curr. Biol. 19, 229-234. DOI
46	Chaiwanon, J., Wang, W., Zhu, J.Y., Oh, E., and Wang, Z.Y. (2016). Information integration and communication in plant growth regulation. Cell 164, 1257-1268. DOI
47	Christians, M.J., Gingerich, D.J., Hua, Z., Lauer, T.D., and Vierstra, R.D. (2012). The light-response BTB1 and BTB2 proteins assemble nuclear ubiquitin ligases that modify phytochrome B and D signaling in Arabidopsis. Plant Physiol. 160, 118-134. DOI
48	de Lucas, M., and Prat, S. (2014). PIFs get BRright: PHYTOCHROME INTERACTING FACTORs as integrators of light and hormonal signals. New Phytol. 202, 1126-1141. DOI
49	de Lucas, M., Daviere, J.M., Rodriguez-Falcon, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blazquez, M.A., Titarenko, E., and Prat, S. (2008). A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480-484. DOI
50	Delker, C., Sonntag, L., James, G.V., Janitza, P., Ibanez, C., Ziermann, H., Peterson, T., Denk, K., Mull, S., Ziegler, J., et al. (2014). The DET1-COP1-HY5 pathway constitutes a multipurpose signaling module regulating plant photomorphogenesis and thermomorphogenesis. Cell Rep. 9, 1983-1989. DOI
51	Feng, S., Martinez, C., Gusmaroli, G., Wang, Y., Zhou, J., Wang, F., Chen, L., Yu, L., Iglesias-Pedraz, J.M., Kircher, S., et al. (2008). Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475-479. DOI
52	Gray, W.M., Ostin, A., Sandberg, G., Romano, C.P., and Estelle, M. (1998). High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl. Acad. Sci. USA 95, 7197-7202. DOI
53	Foreman, J., Johansson, H., Hornitschek, P., Josse, E.M., Fankhauser, C., and Halliday, K.J. (2011). Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J. 65, 441-452. DOI
54	Franklin, K.A., Lee, S.H., Patel, D., Kumar, S.V., Spartz, A.K., Gu, C., Ye, S., Yu, P., Breen, G., Cohen, J.D., et al. (2011). Phytochromeinteracting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc. Natl. Acad. Sci. USA 108, 20231-20235. DOI
55	Galvao, V.C., Collani, S., Horrer, D., and Schmid, M. (2015). Gibberellic acid signaling is required for ambient temperaturemediated induction of flowering in Arabidopsis thaliana. Plant J. 84, 949-962. DOI
56	Hao, Y., Oh, E., Choi, G., Liang, Z., and Wang, Z.Y. (2012). Interactions between HLH and bHLH factors modulate lightregulated plant development. Mol. Plant 5, 688-697. DOI
57	Hardtke, C.S. (2007). Transcriptional auxin-brassinosteroid crosstalk: who's talking? Bioessays 29, 1115-1123. DOI
58	Hornitschek, P., Lorrain, S., Zoete, V., Michielin, O., and Fankhauser, C. (2009) Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J. 28, 3893-3902. DOI
59	Huq, E., and Quail, P.H. (2002). PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 21, 2441-2450. DOI
60	Jeong, J., and Choi, G. (2013). Phytochrome-interacting factors have both shared and distinct biological roles. Mol. Cells 35, 371-380. DOI

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