Advertisement

Science China Life Sciences

, Volume 61, Issue 2, pp 199–203 | Cite as

Arabidopsis noncoding RNA modulates seedling greening during deetiolation

  • Yuqiu Wang
  • Jian Li
  • Xing-Wang Deng
  • Danmeng Zhu
Research Paper

Abstract

Seedling greening is essential for the survival of plants emerging from the soil. The abundance of chlorophyll precursors, including protochlorophyllide (Pchlide), is precisely controlled during the dark-to-light transition, as over-accumulation of Pchlide can lead to cellular photooxidative damage. Previous studies have identified and characterized multiple regulators controlling this important process. HID1 (hidden treasure 1) is the first noncoding RNA (ncRNA) found in photomorphogenesis. Under continuous red light, HID1 has been shown to inhibit hypocotyl elongation by repressing the transcription of PIF3 (phytochrome interacting factor 3). Here, we report that HID1 acts as a negative regulator of cotyledon greening. Knockdown of HID1 resulted in an increased greening rate of etiolated seedlings relative to wild type when exposed to white light. Genetically, HID1 acts downstream of PIF3 during the dark-to-light transition. The expression of HID1 is not regulated by PIF3 in the dark. Molecularly, the Pchlide content was reduced in dark-grown hid1 mutants than WT. Meanwhile, transcript levels of the protochlorophyllide oxidoreductases known to catalyze Pchlide to chlorophyllide conversion were significantly increased in hid1 seedlings. Thus, our study reveals an additional role of HID1 in the dark-to-light transition in Arabidopsis. Moreover, these results suggest HID1 could regulate distinct targets in different light-mediated developmental processes, and thus is essential to the control of these mechanisms.

Keywords

Arabidopsis noncoding RNA cotyledon greening 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We thank Dr. Peter Quail (UC Berkley, USA) for providing pif3-3 mutant seeds and Dr. Giltsu Choi (KAIST, Korea) for providing the PIF3OX line. We thank Abigail Coplin for critical reading of the manuscript. This work was supported by National Key Basic Research Program (2016YFA0500800), China Postdoctoral Science Foundation (2015M580013 to Yuqiu Wang), Major Program of National Natural Science Foundation of China (91540105 to Danmeng Zhu), and Junior Program of National Natural Science Foundation of China (31500974 to Yuqiu Wang). We also received support from the State Key Laboratory of Protein and Plant Gene Research at Peking University, and Peking-Tsinghua Center for Life Sciences. Yuqiu Wang and Jian Li are supported in part by the postdoctoral fellowship of Peking-Tsinghua Center for Life Sciences. Yuqiu Wang is supported in part by Boya postdoctoral fellowship of Peking University.

Supplementary material

11427_2017_9187_MOESM1_ESM.jpg (103 kb)
Figure S1 The expression of chlorophyll biosynthesis genes in 7-day-old dark-grown Col and hid1 mutant seedlings. Actin7 is used as the internal control.
11427_2017_9187_MOESM2_ESM.docx (20 kb)
Table S1 Primers used in this study

References

  1. Chekanova, J.A. (2015). Long non-coding RNAs and their functions in plants. Curr Opin Plant Biol 27, 207–216.CrossRefPubMedGoogle Scholar
  2. Frick, G., Su, Q., Apel, K., and Armstrong, G.A. (2003). An Arabidopsis porB porC double mutant lacking light-dependent NADPH:protochlorophyllide oxidoreductases B and C is highly chlorophyll-deficient and developmentally arrested. Plant J 35, 141–153.CrossRefPubMedGoogle Scholar
  3. Geisler, S., and Coller, J. (2013). RNA in unexpected places: long noncoding RNA functions in diverse cellular contexts. Nat Rev Mol Cell Biol 14, 699–712.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Huq, E., Al-Sady, B., Hudson, M., Kim, C., Apel, K., and Quail, P.H. (2004). PHYTOCHROME-INTERACTING FACTOR 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305, 1937–1941.CrossRefPubMedGoogle Scholar
  5. Kapusta, A., and Feschotte, C. (2014). Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications. Trends Genets 30, 439–452.CrossRefGoogle Scholar
  6. Kobayashi, K., and Masuda, T. (2016). Transcriptional regulation of tetrapyrrole biosynthesis in Arabidopsis thaliana. Front Plant Sci 7, 1811.PubMedPubMedCentralGoogle Scholar
  7. Liu, J., Wang, H., and Chua, N.H. (2015). Long noncoding RNA transcriptome of plants. Plant Biotechnol J 13, 319–328.CrossRefPubMedGoogle Scholar
  8. Liu, T.T., Zhu, D., Chen, W., Deng, W., He, H., He, G., Bai, B., Qi, Y., Chen, R., and Deng, X.W. (2013). A global identification and analysis of small nucleolar RNAs and possible intermediate-sized non-coding RNAs in Oryza sativa. Mol Plant 6, 830–846.CrossRefPubMedGoogle Scholar
  9. Ma, Z., Hu, X., Cai, W., Huang, W., Zhou, X., Luo, Q., Yang, H., Wang, J., and Huang, J. (2014). Arabidopsis miR171-targeted scarecrow-like proteins bind to GT cis-elements and mediate gibberellin-regulated chlorophyll biosynthesis under light conditions. PLoS Genet 10, e1004519.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Masuda, T., Fusada, N., Oosawa, N., Takamatsu, K., Yamamoto, Y.Y., Ohto, M., Nakamura, K., Goto, K., Shibata, D., Shirano, Y., Hayashi, H., Kato, T., Tabata, S., Shimada, H., Ohta, H., and Takamiya, K. (2003). Functional analysis of isoforms of NADPH: protochlorophyllide oxidoreductase (POR), PORB and PORC, in Arabidopsis thaliana. Plant Cell Physiol 44, 963–974.CrossRefPubMedGoogle Scholar
  11. Monte, E., Tepperman, J.M., Al-Sady, B., Kaczorowski, K.A., Alonso, J.M., Ecker, J.R., Li, X., Zhang, Y., and Quail, P.H. (2004). The phytochromeinteracting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. Proc Natl Acad Sci USA 101, 16091–16098.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Moon, J., Zhu, L., Shen, H., and Huq, E. (2008). PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proc Natl Acad Sci USA 105, 9433–9438.CrossRefPubMedPubMedCentralGoogle Scholar
  13. op den Camp, R.G.L., Przybyla, D., Ochsenbein, C., Laloi, C., Kim, C., Danon, A., Wagner, D., Hideg, E., Göbel, C., Feussner, I., Nater, M., and Apel, K. (2003). Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15, 2320–2332.CrossRefGoogle Scholar
  14. Paddock, T.N., Mason, M.E., Lima, D.F., and Armstrong, G.A. (2010). Arabidopsis protochlorophyllide oxidoreductase A (PORA) restores bulk chlorophyll synthesis and normal development to a porB porC double mutant. Plant Mol Biol 72, 445–457.CrossRefPubMedGoogle Scholar
  15. Reinbothe, S., Reinbothe, C., Apel, K., and Lebedev, N. (1996). Evolution of chlorophyll biosynthesis—The challenge to survive photooxidation. Cell 86, 703–705.CrossRefPubMedGoogle Scholar
  16. Shafiq, S., Li, J., and Sun, Q. (2016). Functions of plants long non-coding RNAs. Biochim Biophys Acta 1859, 155–162.CrossRefPubMedGoogle Scholar
  17. 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 phytochrome-interacting factors. Proc Natl Acad Sci USA 106, 7660–7665.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Stephenson, P.G., Fankhauser, C., and Terry, M.J. (2009). PIF3 is a repressor of chloroplast development. Proc Natl Acad Sci USA 106, 7654–7659.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Tanaka, R., Kobayashi, K., and Masuda, T. (2011). Tetrapyrrole metabolism in Arabidopsis thaliana. Arabidopsis Book 9, e0145.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Tang, W., Wang, W., Chen, D., Ji, Q., Jing, Y., Wang, H., and Lin, R. (2012). Transposase-derived proteins FHY3/FAR1 interact with PHYTOCHROME- INTERACTING FACTOR1 to regulate chlorophyll biosynthesis by modulating HEMB1 during deetiolation in Arabidopsis. Plant Cell 24, 1984–2000.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Wang, Y., Fan, X., Lin, F., He, G., Terzaghi, W., Zhu, D., and Deng, X.W. (2014a). Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light. Proc Natl Acad Sci USA 111, 10359–10364.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Wang, Y., Wang, X., Deng, W., Fan, X., Liu, T.T., He, G., Chen, R., Terzaghi, W., Zhu, D., and Deng, X.W. (2014b). Genomic features and regulatory roles of intermediate-sized non-coding RNAs in Arabidopsis. Mol Plant 7, 514–527.CrossRefPubMedGoogle Scholar
  23. Zhong, S., Zhao, M., Shi, T., Shi, H., An, F., Zhao, Q., and Guo, H. (2009). EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. Proc Natl Acad Sci USA 106, 21431–21436.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.State Key Laboratory of Protein and Plant Gene Research, Peking-Tsinghua Center for Life Sciences, School of Advanced Agricultural Sciences and School of Life SciencesPeking UniversityBeijingChina

Personalised recommendations