Brassinosteroids regulate root meristem development by mediating BIN2-UPB1 module in Arabidopsis


Autoři: Taotao Li aff001;  Wei Lei aff001;  Ruiyuan He aff001;  Xiaoya Tang aff001;  Jifu Han aff001;  Lijuan Zou aff002;  Yanhai Yin aff003;  Honghui Lin aff001;  Dawei Zhang aff001
Působiště autorů: Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, State Key Laboratory of Hydraulics and Mountain River Engineering, College of Life Sciences, Sichuan University, Chengdu, Sichuan, P. R. China aff001;  Ecological Security and Protection Key Laboratory of Sichuan Province, Mianyang Normal University, Mianyang, Sichuan, P. R. China aff002;  Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, Iowa, United States of America aff003
Vyšlo v časopise: Brassinosteroids regulate root meristem development by mediating BIN2-UPB1 module in Arabidopsis. PLoS Genet 16(7): e32767. doi:10.1371/journal.pgen.1008883
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008883

Souhrn

Plant steroid hormones brassinosteroids (BRs) regulate plant growth and development at many levels. While negative regulatory factors that inhibit development and are counteracted by BRs exist in the root meristem, these factors have not been characterized. The functions of UPB1 transcription factor in BR-regulated root growth have not been established, although its role in regulating root are well documented. Here, we found that BIN2 interacts with and phosphorylates the UPB1 transcription factor consequently promoting UPB1 stability and transcriptional activity. Genetic analysis revealed that UPB1 deficiency could partially recover the short-root phenotype of BR-deficient mutants. Expression of a mutated UPB1S37AS41A protein lacking a conserved BIN2 phosphorylation sites can rescue shorter root phenotype of bin2-1 mutant. In addition, UPB1 was repressed by BES1 at the transcriptional level. The paclobutrazol-resistant protein family (PRE2/3) interacts with UPB1 and inhibits its transcriptional activity to promote root meristem development, and BIN2-mediated phosphorylation of UPB1 suppresses its interaction with PRE2/3, and subsequently impairing root meristem development. Taken together, our data elucidate a molecular mechanism by which BR promotes root growth via inhibiting BIN2-UPB1 module.

Klíčová slova:

Arabidopsis thaliana – Genetically modified plants – Immunoprecipitation – Meristems – Phenotypes – Phosphorylation – Seedlings – Meristem development


Zdroje

1. Xi D, Chen X, Wang Y, Zhong R, He J, Shen J, et al. Arabidopsis ANAC092 regulates auxin-mediated root development by binding to the ARF8 and PIN4 promoters. J Integr Plant Biol. 2019;61(9):1015–31. doi: 10.1111/jipb.12735 30415491.

2. Zhang D, Ye H, Guo H, Johnson A, Zhang M, Lin H, et al. Transcription factor HAT1 is phosphorylated by BIN2 kinase and mediates brassinosteroid repressed gene expression in Arabidopsis. Plant J. 2014;77(1):59–70. Epub 2013/10/30. doi: 10.1111/tpj.12368 24164091.

3. Ye H, Liu S, Tang B, Chen J, Xie Z, Nolan TM, et al. RD26 mediates crosstalk between drought and brassinosteroid signalling pathways. Nat Commun. 2017;8:14573. Epub 2017/02/25. doi: 10.1038/ncomms14573 28233777; PubMed Central PMCID: PMC5333127.

4. Nolan TM, Brennan B, Yang M, Chen J, Zhang M, Li Z, et al. Selective Autophagy of BES1 Mediated by DSK2 Balances Plant Growth and Survival. Dev Cell. 2017;41(1):33–46 e7. Epub 2017/04/12. doi: 10.1016/j.devcel.2017.03.013 28399398; PubMed Central PMCID: PMC5720862.

5. Wang H, Tang J, Liu J, Hu J, Chen Y, Cai Z, et al. Abscisic Acid Signaling Inhibits Brassinosteroid Signaling through Dampening the Dephosphorylation of BIN2 by ABI1 and ABI2. Mol Plant. 2018;11(2):315–25. Epub 2017/12/25. doi: 10.1016/j.molp.2017.12.013 29275167.

6. Shang Y, Dai C, Lee MM, Kwak JM, Nam KH. BRI1-Associated Receptor Kinase 1 Regulates Guard Cell ABA Signaling Mediated by Open Stomata 1 in Arabidopsis. Mol Plant. 2016;9(3):447–60. Epub 2016/01/03. doi: 10.1016/j.molp.2015.12.014 26724418.

7. Yin Y, Wang ZY, Mora-Garcia S, Li J, Yoshida S, Asami T, et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell. 2002;109(2):181–91. Epub 2002/05/15. doi: 10.1016/s0092-8674(02)00721-3 12007405.

8. Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D, et al. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell. 2002;2(4):505–13. Epub 2002/04/24. doi: 10.1016/s1534-5807(02)00153-3 11970900.

9. Peng P, Yan Z, Zhu Y, Li J. Regulation of the Arabidopsis GSK3-like kinase BRASSINOSTEROID-INSENSITIVE 2 through proteasome-mediated protein degradation. Mol Plant. 2008;1(2):338–46. Epub 2008/08/30. doi: 10.1093/mp/ssn001 18726001; PubMed Central PMCID: PMC2519614.

10. Clouse SD. Molecular genetic studies confirm the role of brassinosteroids in plant growth and development. Plant J. 1996;10(1):1–8. Epub 1996/07/01. doi: 10.1046/j.1365-313x.1996.10010001.x 8758975.

11. Mussig C, Shin GH, Altmann T. Brassinosteroids promote root growth in Arabidopsis. Plant Physiol. 2003;133(3):1261–71. Epub 2003/10/04. doi: 10.1104/pp.103.028662 14526105; PubMed Central PMCID: PMC281621.

12. Gonzalez-Garcia MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-Garcia S, Russinova E, et al. Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development. 2011;138(5):849–59. Epub 2011/01/29. doi: 10.1242/dev.057331 21270057.

13. Vragovic K, Sela A, Friedlander-Shani L, Fridman Y, Hacham Y, Holland N, et al. Translatome analyses capture of opposing tissue-specific brassinosteroid signals orchestrating root meristem differentiation. Proc Natl Acad Sci U S A. 2015;112(3):923–8. Epub 2015/01/07. doi: 10.1073/pnas.1417947112 25561530; PubMed Central PMCID: PMC4311806.

14. Chaiwanon J, Wang ZY. Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots. Curr Biol. 2015;25(8):1031–42. Epub 2015/04/14. doi: 10.1016/j.cub.2015.02.046 25866388; PubMed Central PMCID: PMC4415608.

15. Gao Y, Liu J, Chen Y, Tang H, Wang Y, He Y, et al. Tomato SlAN11 regulates flavonoid biosynthesis and seed dormancy by interaction with bHLH proteins but not with MYB proteins. Hortic Res. 2018;5:27. Epub 2018/06/07. doi: 10.1038/s41438-018-0032-3 29872532; PubMed Central PMCID: PMC5981465.

16. Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J. A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell. 2005;120(2):249–59. Epub 2005/02/01. doi: 10.1016/j.cell.2004.11.044 15680330.

17. Wu J, Wang W, Xu P, Pan J, Zhang T, Li Y, et al. phyB Interacts with BES1 to Regulate Brassinosteroid Signaling in Arabidopsis. Plant Cell Physiol. 2018. Epub 2018/11/06. doi: 10.1093/pcp/pcy212 30388258.

18. Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL, Takabayashi J, et al. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to arabidopsis stomatal differentiation. Plant Cell. 2008;20(7):1775–85. Epub 2008/07/22. doi: 10.1105/tpc.108.060848 18641265; PubMed Central PMCID: PMC2518248.

19. Poirier BC, Feldman MJ, Lange BM. bHLH093/NFL and bHLH061 are required for apical meristem function in Arabidopsis thaliana. Plant Signal Behav. 2018;13(7):e1486146. Epub 2018/08/31. doi: 10.1080/15592324.2018.1486146 30160638; PubMed Central PMCID: PMC6128687.

20. Tsukagoshi H, Busch W, Benfey PN. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell. 2010;143(4):606–16. Epub 2010/11/16. doi: 10.1016/j.cell.2010.10.020 21074051

21. Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S. Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol. 2005;138(2):1117–25. doi: 10.1104/pp.104.058040 15908602; PubMed Central PMCID: PMC1150425.

22. Asami T, Min YK, Nagata N, Yamagishi K, Takatsuto S, Fujioka S, et al. Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor. Plant Physiol. 2000;123(1):93–100. Epub 2000/05/12. doi: 10.1104/pp.123.1.93 10806228; PubMed Central PMCID: PMC58985.

23. Zhao J, Peng P, Schmitz RJ, Decker AD, Tax FE, Li J. Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol. 2002;130(3):1221–9. Epub 2002/11/13. doi: 10.1104/pp.102.010918 12427989; PubMed Central PMCID: PMC166643.

24. Oh E, Zhu JY, Wang ZY. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol. 2012;14(8):802–9. Epub 2012/07/24. doi: 10.1038/ncb2545 22820378; PubMed Central PMCID: PMC3703456.

25. Wang H, Zhu Y, Fujioka S, Asami T, Li J. Regulation of Arabidopsis brassinosteroid signaling by atypical basic helix-loop-helix proteins. Plant Cell. 2009;21(12):3781–91. Epub 2009/12/22. doi: 10.1105/tpc.109.072504 20023194; PubMed Central PMCID: PMC2814491.

26. Lv B, Tian H, Zhang F, Liu J, Lu S, Bai M, et al. Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. PLoS Genet. 2018;14(1):e1007144. Epub 2018/01/13. doi: 10.1371/journal.pgen.1007144 29324765; PubMed Central PMCID: PMC5783399.

27. Cho H, Ryu H, Rho S, Hill K, Smith S, Audenaert D, et al. A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nat Cell Biol. 2014;16(1):66–76. Epub 2013/12/24. doi: 10.1038/ncb2893 24362628.

28. Cheng Y, Zhu W, Chen Y, Ito S, Asami T, Wang X. Brassinosteroids control root epidermal cell fate via direct regulation of a MYB-bHLH-WD40 complex by GSK3-like kinases. Elife. 2014. Epub 2014/04/29. doi: 10.7554/eLife.02525 24771765; PubMed Central PMCID: PMC4005458.

29. Li J, Nam KH, Vafeados D, Chory J. BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiol. 2001;127(1):14–22. Epub 2001/09/13. doi: 10.1104/pp.127.1.14 11553730; PubMed Central PMCID: PMC117958.

30. Ikeda M, Fujiwara S, Mitsuda N, Ohme-Takagi M. A triantagonistic basic helix-loop-helix system regulates cell elongation in Arabidopsis. Plant Cell. 2012;24(11):4483–97. Epub 2012/11/20. doi: 10.1105/tpc.112.105023 23161888; PubMed Central PMCID: PMC3531847.

31. Kim Y, Song JH, Park SU, Jeong YS, Kim SH. Brassinosteroid-Induced Transcriptional Repression and Dephosphorylation-Dependent Protein Degradation Negatively Regulate BIN2-Interacting AIF2 (a BR Signaling-Negative Regulator) bHLH Transcription Factor. Plant Cell Physiol. 2017;58(2):227–39. Epub 2017/01/11. doi: 10.1093/pcp/pcw223 28069895.

32. Ye K, Li H, Ding Y, Shi Y, Song CP, Gong Z, et al. BRASSINOSTEROID-INSENSITIVE2 Negatively Regulates the Stability of Transcription Factor ICE1 in Response to Cold Stress in Arabidopsis. Plant Cell. 2019. doi: 10.1105/tpc.19.00058 31409630.

33. Van Leene J, Eeckhout D, Cannoot B, De Winne N, Persiau G, Van De Slijke E, et al. An improved toolbox to unravel the plant cellular machinery by tandem affinity purification of Arabidopsis protein complexes. Nat Protoc. 2015;10(1):169–87. Epub 2014/12/19. doi: 10.1038/nprot.2014.199 25521792.

34. Yoo SD, Cho YH, Sheen J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc. 2007;2(7):1565–72. Epub 2007/06/23. doi: 10.1038/nprot.2007.199 17585298.

35. Tan W, Zhang D, Zhou H, Zheng T, Yin Y, Lin H. Transcription factor HAT1 is a substrate of SnRK2.3 kinase and negatively regulates ABA synthesis and signaling in Arabidopsis responding to drought. PLoS Genet. 2018;14(4):e1007336. Epub 2018/04/17. doi: 10.1371/journal.pgen.1007336 29659577; PubMed Central PMCID: PMC5919683.

36. Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthelemy J, et al. High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis. Plant Cell. 2008;20(6):1494–503. Epub 2008/06/05. doi: 10.1105/tpc.107.056069 18523061; PubMed Central PMCID: PMC2483377.

37. Mu RL, Cao YR, Liu YF, Lei G, Zou HF, Liao Y, et al. An R2R3-type transcription factor gene AtMYB59 regulates root growth and cell cycle progression in Arabidopsis. Cell Res. 2009;19(11):1291–304. Epub 2009/07/08. doi: 10.1038/cr.2009.83 19581938.

38. Lee BD, Kim MR, Kang MY, Cha JY, Han SH, Nawkar GM, et al. The F-box protein FKF1 inhibits dimerization of COP1 in the control of photoperiodic flowering. Nat Commun. 2017;8(1):2259. Epub 2017/12/24. doi: 10.1038/s41467-017-02476-2 29273730; PubMed Central PMCID: PMC5741637.

39. Huang X, Hou L, Meng J, You H, Li Z, Gong Z, et al. The Antagonistic Action of Abscisic Acid and Cytokinin Signaling Mediates Drought Stress Response in Arabidopsis. Mol Plant. 2018;11(7):970–82. Epub 2018/05/13. doi: 10.1016/j.molp.2018.05.001 29753021.

40. Li T, Yang S, Kang X, Lei W, Qiao K, Zhang D, et al. The bHLH transcription factor gene AtUPB1 regulates growth by mediating cell cycle progression in Arabidopsis. Biochem Biophys Res Commun. 2019;518(3):565–72. doi: 10.1016/j.bbrc.2019.08.088 31445703.

41. Yang Y, Liang T, Zhang L, Shao K, Gu X, Shang R, et al. UVR8 interacts with WRKY36 to regulate HY5 transcription and hypocotyl elongation in Arabidopsis. Nat Plants. 2018;4(2):98–107. Epub 2018/01/31. doi: 10.1038/s41477-017-0099-0 29379156.


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 7

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×