Light promotes jasmonate biosynthesis to regulate photomorphogenesis in Arabidopsis

Abstract

Light acts as the pivotal external environment cue to modulate plant growth and development. Seeds germinate in the soil without light to undergo skotomorphogenesis with rapidly elongating hypocotyls that facilitate emergence from the soil, while seedlings upon light exposure undergo photomorphogenesis with significantly inhibited hypocotyl elongation that benefits plants to stand up firmly and cope with the changing environment. In this study, we demonstrate that light promotes jasmonate (JA) biosynthesis to inhibit hypocotyl elongation and orchestrate seedling photomorphogenesis in Arabidopsis. We showed that JAinhibition on hypocotyl elongation is dependent on JA receptor COI1 and signaling components such as repressor proteins JAZs and transcription activators MYC2/MYC3/MYC4. Furthermore, we found that MYC2/MYC3/MYC4 activate the expression of photomorphogenesis regulator HY5 to repress cell elongation-related genes (such as SAUR62 and EXP2) essential for seedling photomorphogenesis. Our findings provide a novel insight into molecular mechanisms underlying how plants integrate light signal with hormone pathway to establish seedling photomorphogenesis.

References

  1. Acosta, I.F., Gasperini, D., Chételat, A., Stolz, S., Santuari, L., and Farmer, E.E. (2013). Role of NINJA in root jasmonate signaling. Proc Natl Acad Sci USA 110, 15473–15478.

    CAS  PubMed  Article  Google Scholar 

  2. Ahmad, M., Jarillo, J.A., Smirnova, O., and Cashmore, A.R. (1998). Cryptochrome blue-light photoreceptors of Arabidopsis implicated in phototropism. Nature 392, 720–723.

    CAS  PubMed  Article  Google Scholar 

  3. Ang, L.H., Chattopadhyay, S., Wei, N., Oyama, T., Okada, K., Batschauer, A., and Deng, X.W. (1998). Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1, 213–222.

    CAS  Article  PubMed  Google Scholar 

  4. Boter, M., Ruíz-Rivero, O., Abdeen, A., and Prat, S. (2004). Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18, 1577–1591.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  5. Browse, J. (2009). Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60, 183–205.

    CAS  PubMed  Article  Google Scholar 

  6. Chakraborty, M., Gangappa, S.N., Maurya, J.P., Sethi, V., Srivastava, A.K., Singh, A., Dutta, S., Ojha, M., Gupta, N., Sengupta, M., et al. (2019). Functional interrelation of MYC 2 and HY 5 plays an important role in Arabidopsis seedling development. Plant J 99, 1080–1097.

    CAS  PubMed  Article  Google Scholar 

  7. Chao, D.Y., and Lin, H.X. (2010). The tricks plants use to reach appropriate light. Sci China Life Sci 53, 916–926.

    PubMed  Article  Google Scholar 

  8. Chen, M., and Chory, J. (2011). Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol 21, 664–671.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Chen, M., Chory, J., and Fankhauser, C. (2004). Light signal transduction in higher plants. Annu Rev Genet 38, 87–117.

    CAS  Article  PubMed  Google Scholar 

  10. Chen, Q., Sun, J., Zhai, Q., Zhou, W., Qi, L., Xu, L., Wang, B., Chen, R., Jiang, H., Qi, J., et al. (2011). The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23, 3335–3352.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. Chory, J. (1992). A genetic model for light-regulated seedling development in Arabidopsis. Development 115, 337–354.

    CAS  Google Scholar 

  12. Cosgrove, D.J. (2000). Loosening of plant cell walls by expansins. Nature 407, 321–326.

    CAS  PubMed  Article  Google Scholar 

  13. Dai, L., Xu, L., Huang, D., Li, X., Luo, K., and Guan, C. (2002). ASK1 physically interacts with COI1 and is required for male fertility in Arabidopsis. Sci China Ser C-Life Sci 45, 631–636.

    CAS  Google Scholar 

  14. Glauser G., and Wolfender J.L. (2013). A non-targeted approach for extended liquid chromatography-mass spectrometry profiling of free and esterified jasmonates after wounding. Methods Mol Biol 1011, 123–134.

    CAS  PubMed  Article  Google Scholar 

  15. Hardtke, C.S. (2000). HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J 19, 4997–5006.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Hu, P., Zhou, W., Cheng, Z., Fan, M., Wang, L., and Xie, D. (2013). JAV1 controls jasmonate-regulated plant defense. Mol Cell 50, 504–515.

    CAS  PubMed  Article  Google Scholar 

  17. Huang, H., Wang, C., Tian, H., Sun, Y., Xie, D., and Song, S. (2014). Amino acid substitutions of GLY98, LEU245 and GLU543 in COI1 distinctively affect jasmonate-regulated male fertility in Arabidopsis. Sci China Life Sci 57, 145–154.

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  19. Kami, C., Lorrain, S., Hornitschek, P., and Fankhauser, C. (2010). Lightregulated plant growth and development. Curr Top Dev Biol 91, 29–66.

    CAS  PubMed  Article  Google Scholar 

  20. Lee, J., He, K., Stolc, V., Lee, H., Figueroa, P., Gao, Y., Tongprasit, W., Zhao, H., Lee, I., and Deng, X.W. (2007). Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19, 731–749.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. Leivar, P., Monte, E., Oka, Y., Liu, T., Carle, C., Castillon, A., Huq, E., and Quail, P.H. (2008). Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr Biol 18, 1815–1823.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. Li, T., Jia, K.P., Lian, H.L., Yang, X., Li, L., and Yang, H.Q. (2014). Jasmonic acid enhancement of anthocyanin accumulation is dependent on phytochrome A signaling pathway under far-red light in Arabidopsis. Biochem Biophys Res Commun 454, 78–83.

    CAS  PubMed  Article  Google Scholar 

  23. Liu, H., Liu, B., Zhao, C., Pepper, M., and Lin, C. (2011). The action mechanisms of plant cryptochromes. Trends Plant Sci 16, 684–691.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  25. Paik, I., and Huq, E. (2019). Plant photoreceptors: Multi-functional sensory proteins and their signaling networks. Semin Cell Dev Biol 92, 114–121.

    CAS  PubMed  Article  Google Scholar 

  26. Qi, T., Song, S., Ren, Q., Wu, D., Huang, H., Chen, Y., Fan, M., Peng, W., Ren, C., and Xie, D. (2011). The jasmonate-ZIM-domain proteins interact with the WD-repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 23, 1795–1814.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. Qi, T., Wang, J., Huang, H., Liu, B., Gao, H., Liu, Y., Song, S., and Xie, D. (2015). Regulation of jasmonate-induced leaf senescence by antagonism between bHLH subgroup IIIe and IIId factors in Arabidopsis. Plant Cell 27, 1634–1649.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  28. Quail, P.H. (2002). Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3, 85–93.

    CAS  Article  PubMed  Google Scholar 

  29. Reed, J.W., Nagpal, P., Poole, D.S., Furuya, M., and Chory, J. (1993). Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5, 147–157.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Reymond, P., Bodenhausen, N., Van Poecke, R.M.P., Krishnamurthy, V., Dicke, M., and Farmer, E.E. (2004). A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16, 3132–3147.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. Rowe, H.C., Walley, J.W., Corwin, J., Chan, E.K.F., Dehesh, K., and Kliebenstein, D.J. (2010). Deficiencies in jasmonate-mediated plant defense reveal quantitative variation in Botrytis cinerea pathogenesis. PLoS Pathog 6, e1000861.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  32. Shan, X., Zhang, Y., Peng, W., Wang, Z., and Xie, D. (2009). Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J Exp Bot 60, 3849–3860.

    CAS  PubMed  Article  Google Scholar 

  33. Song, S., Huang, H., Gao, H., Wang, J., Wu, D., Liu, X., Yang, S., Zhai, Q., Li, C., Qi, T., et al. (2014). Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis. Plant Cell 26, 263–279.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. Song, S., Qi, T., Huang, H., and Xie, D. (2013). Regulation of stamen development by coordinated actions of jasmonate, auxin, and gibberellin in Arabidopsis. Mol Plant 6, 1065–1073.

    CAS  PubMed  Article  Google Scholar 

  35. Staswick, P.E., Su, W., and Howell, S.H. (1992). Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89, 6837–6840.

    CAS  PubMed  Article  Google Scholar 

  36. Su, J., Liu, B., Liao, J., Yang, Z., Lin, C., and Oka, Y. (2017). Coordination of cryptochrome and phytochrome signals in the regulation of plant light responses. Agronomy 7, 25.

    Article  CAS  Google Scholar 

  37. Sun, N., Wang, J., Gao, Z., Dong, J., He, H., Terzaghi, W., Wei, N., Deng, X.W., and Chen, H. (2016). Arabidopsis SAURs are critical for differential light regulation of the development of various organs. Proc Natl Acad Sci USA 113, 6071–6076.

    CAS  PubMed  Article  Google Scholar 

  38. Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G.A., and Browse, J. (2007). JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661–665.

    CAS  PubMed  Article  Google Scholar 

  39. von Arnim, A.G., and Deng, X.W. (1994). Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cellspecific regulation of its nucleocytoplasmic partitioning. Cell 79, 1035–1045.

    Article  Google Scholar 

  40. Wasternack, C., and Hause, B. (2013). Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111, 1021–1058.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. Whitelam, G.C., Johnson, E., Peng, J., Carol, P., Anderson, M.L., Cowl, J. S., and Harberd, N.P. (1993). Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5, 757–768.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Xie, D., Feys, B., James, S., Nieto-Rostro, M., and Turner, J. (1998). COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091–1094.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. Xu, X., Paik, I., Zhu, L., and Huq, E. (2015). Illuminating progress in phytochrome-mediated light signaling pathways. Trends Plant Sci 20, 641–650.

    CAS  PubMed  Article  Google Scholar 

  44. Yan, C., Fan, M., Yang, M., Zhao, J., Zhang, W., Su, Y., Xiao, L., Deng, H., and Xie, D. (2018). Injury activates Ca2+/calmodulin-dependent phosphorylation of JAV1-JAZ8-WRKY51 complex for jasmonate biosynthesis. Mol Cell 70, 136–149.e7.

    CAS  PubMed  Article  Google Scholar 

  45. Yan, J., Zhang, C., Gu, M., Bai, Z., Zhang, W., Qi, T., Cheng, Z., Peng, W., Luo, H., Nan, F., et al. (2009). The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21, 2220–2236.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Yang, Z., Liu, B., Su, J., Liao, J., Lin, C., and Oka, Y. (2017). Cryptochromes orchestrate transcription regulation of diverse blue light responses in plants. Photochem Photobiol 93, 112–127.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. Yuan, Z., and Zhang, D. (2015). Roles of jasmonate signalling in plant inflorescence and flower development. Curr Opin Plant Biol 27, 44–51.

    CAS  PubMed  Article  Google Scholar 

  48. Zhai, Q., Zhang, X., Wu, F., Feng, H., Deng, L., Xu, L., Zhang, M., Wang, Q., and Li, C. (2015). Transcriptional mechanism of jasmonate receptor COI1-mediated delay of flowering time in Arabidopsis. Plant Cell 27, 2814–2828.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Zhang, H., He, H., Wang, X., Wang, X., Yang, X., Li, L., and Deng, X.W. (2011). Genome-wide mapping of the HY5-mediated genenetworks in Arabidopsis that involve both transcriptional and post-transcriptional regulation. Plant J 65, 346–358.

    CAS  PubMed  Article  Google Scholar 

  50. Zheng, Y., Cui, X., Su, L., Fang, S., Chu, J., Gong, Q., Yang, J., and Zhu, Z. (2017). Jasmonate inhibits COP1 activity to suppress hypocotyl elongation and promote cotyledon opening in etiolated Arabidopsis seedlings. Plant J 90, 1144–1155.

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Deng X.W. (Peking University) for providing hy5-205, pifq mutant seeds; Dr. Yang H.Q. (Fudan University) for providing cry1/2, phyB-9, phyA-211 mutant seeds; and Lu Meng, Dr. Ran Du for their technical support. This work was supported by the National Key R&D Program of China (2016YFA0500501) and National Natural Science Foundation of China (31630085).

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Jianbin Yan or Daoxin Xie.

Ethics declarations

Compliance and ethics The author(s) declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yi, R., Yan, J. & Xie, D. Light promotes jasmonate biosynthesis to regulate photomorphogenesis in Arabidopsis. Sci. China Life Sci. 63, 943–952 (2020). https://doi.org/10.1007/s11427-019-1584-4

Download citation

Keywords

  • photomorphogenesis
  • jasmonate
  • COI1
  • MYC2
  • HY5
  • hypocotyl elongation