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Convergence of light and chloroplast signals for de-etiolation through ABI4–HY5 and COP1

Abstract

Seedling de-etiolation prepares plants to switch from heterotrophic to photoautotrophic growth, a transition essential for plant survival. This delicate de-etiolation process is precisely controlled by environmental and endogenous signals. Although intracellular plastid-derived retrograde signalling is essential for the de-etiolation process, the molecular nature of these retrograde signals remains elusive13. Here we show that chloroplast and light signals antagonistically fine-tune a suite of developmental and physiological responses associated with de-etiolation through a transcriptional module of ABA INSENSITIVE 4 (ABI4) and ELONGATED HYPOCOTYL 5 (HY5). Moreover, ABI4 and HY5 antagonistically regulate the expression of CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) and the subsequent greening process. In turn, ABI4 and HY5 are targeted for degradation by COP1 in the light and dark, respectively, to ensure a proper interplay of ABI4 and HY5 actions during seedling de-etiolation. Our study provides a new molecular mechanism for understanding how chloroplast signals converge with light signals to optimize early plant development.

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Figure 1: ABI4 and HY5 antagonistically regulate hypocotyl elongation and cell-expansion-related genes.
Figure 2: Increased levels of ROS and Pchlide in plastid signalling mutants.
Figure 3: ABI4 and HY5 antagonistically regulate COP1 expression and the subsequent greening process.
Figure 4: COP1 targets ABI4 for proteosomal degradation.

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References

  1. Nott, A., Jung, H. S., Koussevitzky, S. & Chory, J. Plastid-to-nucleus retrograde signaling. Annu. Rev. Plant Biol. 57, 739–759 (2006).

    Article  CAS  Google Scholar 

  2. Woodson, J. D. & Chory, J. Coordination of gene expression between organellar and nuclear genomes. Nature Rev. Genet. 9, 383–395 (2008).

    Article  CAS  Google Scholar 

  3. Chi, W., Sun, X. & Zhang, L. Intracellular signaling from plastid to nucleus. Annu. Rev. Plant Biol. 64, 559–582 (2013).

    Article  CAS  Google Scholar 

  4. Jiao, Y., Lau, O. S. & Deng, X. W. Light-regulated transcriptional networks in higher plants. Nature Rev. Genet. 8, 217–230 (2007).

    Article  CAS  Google Scholar 

  5. Feng, S. et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475–479 (2008).

    Article  CAS  Google Scholar 

  6. Bai, M. Y. et al. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nature Cell Biol. 14, 810–817 (2012).

    Article  CAS  Google Scholar 

  7. Zhong, S. et al. EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. Proc. Natl Acad. Sci. USA 106, 21431–21436 (2009).

    Article  CAS  Google Scholar 

  8. Osterlund, M. T., Hardtke, C. S., Wei, N. & Deng, X. W. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405, 462–466 (2000).

    Article  CAS  Google Scholar 

  9. Ang, L. H. et al. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol. Cell 1, 213–222 (1998).

    Article  CAS  Google Scholar 

  10. Dyall, S. D., Brown, M. T. & Johnson, P. J. Ancient invasions: from endosymbionts to organelles. Science 304, 253–257 (2004).

    Article  CAS  Google Scholar 

  11. Martin, W. et al. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162–165 (1998).

    Article  CAS  Google Scholar 

  12. Leister, D. Chloroplast research in the genomic age. Trends Genet. 19, 47–56 (2003).

    Article  CAS  Google Scholar 

  13. Leon, P., Arroyo, A. & Mackenzie, S. Nuclear control of plastid and mitochondrial development in higher plants. Annu. Rev. Plant Physiol. 49, 453–480 (1998).

    Article  CAS  Google Scholar 

  14. Sun, X. et al. A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nature Commun. 2, 477 (2011).

    Article  Google Scholar 

  15. Koussevitzky, S. et al. Signals from chloroplasts converge to regulate nuclear gene expression. Science 316, 715–719 (2007).

    Article  CAS  Google Scholar 

  16. Ruckle, M. E. & Larkin, R. M. Plastid signals that affect photomorphogenesis in Arabidopsis thaliana are dependent on GENOMES UNCOUPLED 1 and cryptochrome 1. New Phytol. 182, 367–379 (2009).

    Article  CAS  Google Scholar 

  17. Jing, Y. et al. Arabidopsis chromatin remodeling factor PICKLE interacts with transcription factor HY5 to regulate hypocotyl cell elongation. Plant Cell 25, 242–256 (2013).

    Article  CAS  Google Scholar 

  18. Mochizuki, N., Susek, R. & Chory, J. An intracellular signal transduction pathway between the chloroplast and nucleus is involved in de-etiolation. Plant Physiol. 112, 1465–1469 (1996).

    Article  CAS  Google Scholar 

  19. Reinbothe, S., Reinbothe, C., Apel, K. & Lebedev, N. Evolution of chlorophyll biosynthesis – the challenge to survive photooxidation. Cell 86, 703–705 (1996).

    Article  CAS  Google Scholar 

  20. Sperling, U. et al. Etioplast differentiation in Arabidopsis: both PORA and PORB restore the prolamellar body and photoactive protochlorophyllide-F655 to the cop1 photomorphogenic mutant. Plant Cell 10, 283–296 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Huq, E. et al. PHYTOCHROME-INTERACTING FACTOR 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305, 1937–1941 (2004).

    Article  CAS  Google Scholar 

  22. Moon, J., Zhu, L., Shen, H. & Huq, E. PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proc. Natl Acad. Sci. USA 105, 9433–9438 (2008).

    Article  CAS  Google Scholar 

  23. Stephenson, P. G., Fankhauser, C. & Terry, M. J. PIF3 is a repressor of chloroplast development. Proc. Natl Acad. Sci. USA 106, 7654–7659 (2009).

    Article  CAS  Google Scholar 

  24. Apitz, J., Schmied, J., Lehmann, M. J., Hedtke, B. & Grimm, B. GluTR2 complements a hema1 mutant lacking glutamyl-tRNA reductase 1, but is differently regulated at the post-translational level. Plant Cell Physiol. 55, 645–657 (2014).

    Article  CAS  Google Scholar 

  25. Huang, X. et al. Arabidopsis FHY3 and HY5 positively mediate induction of COP1 transcription in response to photomorphogenic UV-B light. Plant Cell 24, 4590–4606 (2012).

    Article  CAS  Google Scholar 

  26. Chen, D. et al. Antagonistic basic helix-loop-helix/bZIP transcription factors form transcriptional modules that integrate light and reactive oxygen species signaling in Arabidopsis. Plant Cell 25, 1657–1673 (2013).

    Article  CAS  Google Scholar 

  27. Finkelstein, R., Lynch, T., Reeves, W., Petitfils, M. & Mostachetti, M. Accumulation of the transcription factor ABA-insensitive (ABI)4 is tightly regulated post-transcriptionally. J. Exp. Bot. 62, 3971–3979 (2011).

    Article  CAS  Google Scholar 

  28. Gregorio, J., Hernandez-Bernal, A. F., Cordoba, E. & Leon, P. Characterization of evolutionarily conserved motifs involved in activity and regulation of the ABA-INSENSITIVE (ABI)4 transcription factor. Mol. Plant 7, 422–436 (2014).

    Article  CAS  Google Scholar 

  29. Jang, I. C., Henriques, R., Seo, H. S., Nagatani, A. & Chua, N. H. Arabidopsis PHYTOCHROME INTERACTING FACTOR proteins promote phytochrome B polyubiquitination by COP1 E3 ligase in the nucleus. Plant Cell 22, 2370–2383 (2010).

    Article  CAS  Google Scholar 

  30. Kusnetsov, V. et al. Evidence that the plastid signal and light operate via the same cis-acting elements in the promoters of nuclear genes for plastid proteins. Mol. Gen. Genet. 252, 631–639 (1996).

    CAS  PubMed  Google Scholar 

  31. Hills, A. C., Khan, S. & Lopez-Juez, E. Chloroplast biogenesis-associated nuclear genes: control by plastid signals evolved prior to their regulation as part of photomorphogenesis. Front. Plant Sci. 6, 1078 (2015).

    Article  Google Scholar 

  32. Larkin, R. M. Influence of plastids on light signalling and development. Philos. Trans R. Soc. B 369, 20130232 (2014).

    Article  Google Scholar 

  33. Lepisto, A. & Rintamaki, E. Coordination of plastid and light signaling pathways upon development of Arabidopsis leaves under various photoperiods. Mol. Plant 5, 799–816 (2012).

    Article  Google Scholar 

  34. Ruckle, M. E., Burgoon, L. D., Lawrence, L. A., Sinkler, C. A. & Larkin, R. M. Plastids are major regulators of light signaling in Arabidopsis. Plant Physiol. 159, 366–390 (2012).

    Article  CAS  Google Scholar 

  35. Ruckle, M. E., DeMarco, S. M. & Larkin, R. M. Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19, 3944–3960 (2007).

    Article  CAS  Google Scholar 

  36. Wind, J. J., Peviani, A., Snel, B., Hanson, J. & Smeekens, S. C. ABI4 versatile activator and repressor. Trends Plant Sci. 18, 125–132 (2013).

    Article  CAS  Google Scholar 

  37. Tang, W. et al. FAR-RED ELONGATED HYPOCOTYL3 and FAR-RED IMPAIRED RESPONSE1 transcription factors integrate light and abscisic acid signaling in Arabidopsis. Plant Physiol. 163, 857–866 (2013).

    Article  CAS  Google Scholar 

  38. Wang, F. W. et al. Heat shock factor 1 upregulates transcription of Epstein–Barr Virus nuclear antigen 1 by binding to a heat shock element within the BamHI-Q promoter. Virology 421, 184–191 (2011).

    Article  CAS  Google Scholar 

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Acknowledgements

The work in our laboratory was supported by the Major State Basic Research Development Program (grant 2015CB150100), the National Natural Science Foundation of China (grant 31370273) and Chinese Academy of Sciences Grant KGZD-EW-T05. We thank Q. Xie for help in ubiquitination analysis.

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Authors and Affiliations

Authors

Contributions

L.Z. conceived this project. X.X. performed the phenotypic analysis, yeast two-hybrid assay, ChIP, qRT–PCR and DNA-binding assay and, together with P.F., carried out the ubiquitination assay. H.G. and J.L. constructed the transgenic plants. W.C., X.S., R.L., C.L., H.W. and D.L. joined in the discussion and data analysis. X.X. and L.Z. designed all experiments, analysed data and wrote the manuscript.

Corresponding author

Correspondence to Lixin Zhang.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Figs 1-11, Supplementary Table 2 and Supplementary References. (PDF 1403 kb)

Supplementary Data

Supplementary Table 1 (XLSX 18022 kb)

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Xu, X., Chi, W., Sun, X. et al. Convergence of light and chloroplast signals for de-etiolation through ABI4–HY5 and COP1. Nature Plants 2, 16066 (2016). https://doi.org/10.1038/nplants.2016.66

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