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The nuclear localization signal is required for the function of squamosa promoter binding protein-like gene 9 to promote vegetative phase change in Arabidopsis

  • Hui Zhang
  • Lu Zhang
  • Junyou Han
  • Zhiyuan Qian
  • Bingying Zhou
  • Yunmin XuEmail author
  • Gang WuEmail author
Article
  • 182 Downloads

Abstract

Key message

A mutation in the nuclear localization signal of squamosa promoter binding like-protein 9 (SPL9) delays vegetative phase change by disrupting its nuclear localization.

Abstract

The juvenile-to-adult phase transition is a critical developmental process in plant development, and it is regulated by a decrease in miR156/157 and a corresponding increase in their targets, squamosa promoter binding protein-like (SPL) genes. SPL proteins contain a conserved SBP domain with putative nuclear localization signals (NLSs) at their C-terminals. Some SPLs promote vegetative phase change by promoting miR172 expression, but the function of nuclear localization signals in those SPLs remains unknown. Here, we identified a loss-of-function mutant, which we named del6, with delayed vegetative phase change phenotypes in a forward genetic screen. Map-based cloning, the whole genome resequencing, and allelic complementation test demonstrate that a G-to-A substitution in the SPL9 gene is responsible for the delayed vegetative phase change phenotypes. In del6, the mutation causes a substitution of the glutamine (Gln) for the conserved basic amino acid arginine (Arg) in the NLS of the SBP domain, and disrupts the normal nuclear localization and function of SPL9. Therefore, our work demonstrates that the NLSs in the SBP domain of SPL9 are indispensable for its nuclear localization and normal function in Arabidopsis.

Keywords

Vegetative phase change SPL9 SBP domain Nuclear localization signals (NLS) 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31700249 and No. 31770209).

Author contribution

YX and GW conceived and designed the research, HZ, JH, LZ, ZQ and BZ performed the experiments, YX and GW wrote the manuscript.

Supplementary material

11103_2019_863_MOESM1_ESM.docx (7.5 mb)
Supplementary material 1 (DOCX 7673 kb)

References

  1. Birkenbihl RP, Jach G, Saedler H, Huijser P (2005) Functional dissection of the plant-specific SBP-Domain: overlap of the DNA-binding and nuclear localization domains. J Mol Biol 352:585–596CrossRefGoogle Scholar
  2. Conti E, Kuriyan J (2000) Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin α. Structure 8:329–338CrossRefGoogle Scholar
  3. Conti E, Uy M, Leighton L, Blobel G, Kuriyan J (1998) Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin α. Cell 94:193–204CrossRefGoogle Scholar
  4. Dingwall C, Laskey RA (1991) Nuclear targeting sequences a consensus? Trends Biochem Sci 16:478–481CrossRefGoogle Scholar
  5. Görlich D, Kutay U (1999) Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15:607–660CrossRefGoogle Scholar
  6. Guo A, Zhu Q, Gu X, Ge S, Yang J, Luo J (2008) Genome-wide identification and evolutionary analysis of the plant specific SBP-box transcription factor family. Gene 418:1–8CrossRefGoogle Scholar
  7. Harreman MT, Kline TM, Milford HG, Harben MB, Hodel AE, Corbett AH (2004) Regulation of nuclear import by phosphorylation adjacent to nuclear localization signals. J Biol Chem 279:20613–20621CrossRefGoogle Scholar
  8. He J, Xu M, Willmann MR, McCormick K, Hu T, Yang L, Starker CG, Voytas DF, Meyers BC, Poethig RS (2018) Threshold-dependent repression of SPL gene expression by miR156/miR157 controls vegetative phase change in Arabidopsis thaliana. PLoS Genet 14:e1007337CrossRefGoogle Scholar
  9. Jans DA, Xiao CY, Lam MH (2000) Nuclear targeting signal recognition: a key control point in nuclear transport? BioEssays 22:532–544CrossRefGoogle Scholar
  10. Kaffman A, O’Shea EK (1999) Regulation of nuclear localization: a key to a door. Annu Rev Cell Dev Biol 15:291–339CrossRefGoogle Scholar
  11. Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol Gen Genet 250:7–16Google Scholar
  12. Lange A, McLane LM, Mills RE, Devine SE, Corbett AH (2010) Expanding the definition of the classical bipartite nuclear localization signal. Traffic 11:311–323CrossRefGoogle Scholar
  13. Poethig RS (1990) Phase change and the regulation of shoot morphogenesis in plants. Science 250:923–930CrossRefGoogle Scholar
  14. Poethig RS (2003) Phase change and the regulation of developmental timing in plants. Science 301:334–336CrossRefGoogle Scholar
  15. Poethig RS (2013) Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 105:125–152CrossRefGoogle Scholar
  16. Robbins J, Dilworth SM, Laskey RA, Dingwall C (1991) Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64:615–623CrossRefGoogle Scholar
  17. Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67:183–195CrossRefGoogle Scholar
  18. Stone JM, Liang X, Nekl ER, Stiers JJ (2005) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41:744–754CrossRefGoogle Scholar
  19. Telfer A, Bollman KM, Poethig RS (1997) Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124:645–654Google Scholar
  20. Wang J, Zhou L, Shi H, Chern M, Yu H, Yi H, He M, Yin J, Zhu X, Li Y, Li W, Liu J, Wang J, Chen X, Qing H, Wang Y, Liu G, Wang W, Li P, Wu X, Zhu L, Zhou J, Ronald P, Li S, Li J, Chen X (2018) A single transcription factor promotes both yield and immunity in rice. Science 361:1026–1028CrossRefGoogle Scholar
  21. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547CrossRefGoogle Scholar
  22. Wu F, Shen S, Lee L, Lee S, Chan M, Lin C (2009a) Tape-Arabidopsis Sandwich-a simpler Arabidopsis protoplast isolation method. Plant Methods 5:16CrossRefGoogle Scholar
  23. Wu G, Park M, Conway SR, Wang JW, Weigel D, Poethig RS (2009b) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759CrossRefGoogle Scholar
  24. Xu M, Hu T, Zhao J, Park M, Earley KW, Wu G, Yang L, Poethig RS (2016) Developmental functions of miR156-regulated squamosa promoter binding protein-likE (SPL) genes in Arabidopsis thaliana. PLoS Genet 12:e1006263CrossRefGoogle Scholar
  25. Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Nunokawa E, Ishizuka Y, Terada T, Shirouzu M, Osanai T, Tanaka A, Seki M, Shinozaki K, Yokoyama S (2004) A novel zinc-binding motif revealed by solution structures of DNA-binding domains of arabidopsis SBP-family transcription factors. J Mol Biol 337:49–63CrossRefGoogle Scholar
  26. Zhu M, Fang T, Li S, Meng K, Guo D (2015) Bipartite nuclear localization signal controls nuclear import and DNA-binding activity of IFN regulatory factor 3. J Immunol 195:289–297CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Subtropical Silviculture, Laboratory of Plant Molecular and Developmental BiologyZhejiang Agriculture and Forestry UniversityHangzhouChina
  2. 2.College of Plant ScienceJilin UniversityChangchunChina

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