DOI QR코드

DOI QR Code

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)
  • Received : 2016.05.16
  • Accepted : 2016.06.10
  • Published : 2016.08.31

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.

Acknowledgement

Supported by : National Research Foundation of Korea (NRF)

References

  1. 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. https://doi.org/10.1016/j.molcel.2006.06.011
  2. 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. https://doi.org/10.1038/ncb2546
  3. 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. https://doi.org/10.1101/gad.243675.114
  4. 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. https://doi.org/10.1016/j.cub.2014.10.076
  5. 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. https://doi.org/10.1016/j.cub.2008.12.046
  6. 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. https://doi.org/10.1016/j.cell.2016.01.044
  7. 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. https://doi.org/10.1104/pp.112.199109
  8. 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. https://doi.org/10.1016/j.cub.2012.03.044
  9. 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. https://doi.org/10.1111/nph.12725
  10. 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. https://doi.org/10.1038/nature06520
  11. 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. https://doi.org/10.1016/j.celrep.2014.11.043
  12. 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. https://doi.org/10.1038/nature06448
  13. 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. https://doi.org/10.1111/j.1365-313X.2010.04434.x
  14. 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. https://doi.org/10.1073/pnas.1110682108
  15. 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. https://doi.org/10.1111/tpj.13051
  16. 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. https://doi.org/10.1073/pnas.95.12.7197
  17. 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. https://doi.org/10.1093/mp/sss011
  18. Hardtke, C.S. (2007). Transcriptional auxin-brassinosteroid crosstalk: who's talking? Bioessays 29, 1115-1123. https://doi.org/10.1002/bies.20653
  19. 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. https://doi.org/10.1038/emboj.2009.306
  20. 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. https://doi.org/10.1093/emboj/21.10.2441
  21. Jeong, J., and Choi, G. (2013). Phytochrome-interacting factors have both shared and distinct biological roles. Mol. Cells 35, 371-380. https://doi.org/10.1007/s10059-013-0135-5
  22. 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. https://doi.org/10.1105/tpc.104.025643
  23. 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. https://doi.org/10.1105/tpc.107.051508
  24. 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. https://doi.org/10.1105/tpc.014498
  25. 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.
  26. Kumar, S.V., and Wigge, P.A. (2010). H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136-147. https://doi.org/10.1016/j.cell.2009.11.006
  27. 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. https://doi.org/10.1038/nature10928
  28. 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. https://doi.org/10.1038/ncomms6473
  29. Leivar, P., and Quail, P.H. (2011). PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16, 19-28.
  30. 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. https://doi.org/10.1105/tpc.109.070672
  31. 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.
  32. 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. https://doi.org/10.1111/j.1365-313X.2009.03971.x
  33. Lucyshyn, D., and Wigge, P.A. (2009). Plant development: PIF4 integrates diverse environmental signals. Curr. Biol. 19, R265-266. https://doi.org/10.1016/j.cub.2009.01.051
  34. 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. https://doi.org/10.1073/pnas.1511437113
  35. 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. https://doi.org/10.1093/pcp/pcu030
  36. 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. https://doi.org/10.1016/S0092-8674(00)81636-0
  37. 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. https://doi.org/10.1126/science.1250778
  38. 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. https://doi.org/10.1038/nature05946
  39. 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. https://doi.org/10.1038/nature10182
  40. 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. https://doi.org/10.1038/ncb2545
  41. 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.
  42. 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. https://doi.org/10.1111/j.1365-313X.2012.05114.x
  43. 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. https://doi.org/10.1016/j.cell.2015.12.018
  44. 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. https://doi.org/10.1093/mp/ssu087
  45. 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. https://doi.org/10.1038/nplants.2015.190
  46. 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. https://doi.org/10.1186/s12870-015-0566-6
  47. 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. https://doi.org/10.1038/ncomms5636
  48. 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. https://doi.org/10.15252/msb.20145766
  49. 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. https://doi.org/10.1104/pp.107.105601
  50. 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. https://doi.org/10.1073/pnas.0812219106
  51. 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. https://doi.org/10.1093/mp/ssu109
  52. 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. https://doi.org/10.1111/j.1365-313X.2009.03983.x
  53. Sun, T.P. (2011). The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21, R338-345. https://doi.org/10.1016/j.cub.2011.02.036
  54. 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. https://doi.org/10.1371/journal.pgen.1002594
  55. 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. https://doi.org/10.1105/tpc.113.112417
  56. 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. https://doi.org/10.1146/annurev-genet-102209-163450
  57. 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. https://doi.org/10.1093/pcp/pcg078
  58. 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. https://doi.org/10.4161/psb.23390
  59. 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. https://doi.org/10.1371/journal.pgen.1003244
  60. 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. https://doi.org/10.1105/tpc.113.121848

Cited by

  1. Molecular mechanisms and ecological function of far-red light signalling 2017, https://doi.org/10.1111/pce.12915
  2. PIF4 Promotes Expression of LNG1 and LNG2 to Induce Thermomorphogenic Growth in Arabidopsis vol.8, 2017, https://doi.org/10.3389/fpls.2017.01320
  3. PIF4-controlled auxin pathway contributes to hybrid vigor inArabidopsis thaliana vol.114, pp.17, 2017, https://doi.org/10.1073/pnas.1703179114
  4. Analysis of bHLH genes from foxtail millet (Setaria italica) and their potential relevance to drought stress vol.13, pp.11, 2018, https://doi.org/10.1371/journal.pone.0207344
  5. A Functional Connection between the Circadian Clock and Hormonal Timing in Arabidopsis vol.9, pp.12, 2018, https://doi.org/10.3390/genes9120567
  6. Coordinated regulation of Arabidopsis microRNA biogenesis and red light signaling through Dicer-like 1 and phytochrome-interacting factor 4 vol.14, pp.3, 2018, https://doi.org/10.1371/journal.pgen.1007247
  7. POWERDRESS-mediated histone deacetylation is essential for thermomorphogenesis in Arabidopsis thaliana vol.14, pp.3, 2018, https://doi.org/10.1371/journal.pgen.1007280
  8. Molecular mechanisms governing plant responses to high temperatures vol.60, pp.9, 2018, https://doi.org/10.1111/jipb.12701
  9. Essential Roles of Local Auxin Biosynthesis in Plant Development and in Adaptation to Environmental Changes vol.69, pp.1, 2018, https://doi.org/10.1146/annurev-arplant-042817-040226
  10. Genome-Wide Characterization of bHLH Genes in Grape and Analysis of their Potential Relevance to Abiotic Stress Tolerance and Secondary Metabolite Biosynthesis vol.9, pp.1664-462X, 2018, https://doi.org/10.3389/fpls.2018.00064
  11. hypocotyl pp.00319317, 2019, https://doi.org/10.1111/ppl.12865
  12. INDETERMINATE-DOMAIN 4 (IDD4) coordinates immune responses with plant-growth in Arabidopsis thaliana vol.15, pp.1, 2019, https://doi.org/10.1371/journal.ppat.1007499