Brassinosteroids (BRs) regulate rice plant architecture, including leaf bending, which affects grain yield. Although BR signaling has been investigated in Arabidopsis thaliana, the components negatively regulating this pathway are less well understood. Here, we demonstrate that Oryza sativa LEAF and TILLER ANGLE INCREASED CONTROLLER (LIC) acts as an antagonistic transcription factor of BRASSINAZOLE-RESISTANT 1 (BZR1) to attenuate the BR signaling pathway. The gain-of-function mutant lic-1 and LIC–overexpressing lines showed erect leaves, similar to BZR1–depleted lines, which indicates the opposite roles of LIC and BZR1 in regulating leaf bending. Quantitative PCR revealed LIC transcription rapidly induced by BR treatment. Image analysis and immunoblotting showed that upon BR treatment LIC proteins translocate from the cytoplasm to the nucleus in a phosphorylation-dependent fashion. Phosphorylation assay in vitro revealed LIC phosphorylated by GSK3–like kinases. For negative feedback, LIC bound to the core element CTCGC in the BZR1 promoter on gel-shift and chromatin immunoprecipitation assay and repressed its transcription on transient transformation assay. LIC directly regulated target genes such as INCREASED LEAF INCLINATION 1 (ILI1) to oppose the action of BZR1. Repression of LIC in ILI1 transcription in protoplasts was partially rescued by BZR1. Phenotypic analysis of the crossed lines depleted in both LIC and BZR1 suggested that BZR1 functionally depends on LIC. Molecular and physiology assays revealed that LIC plays a dominant role at high BR levels, whereas BZR1 is dominant at low levels. Thus, LIC regulates rice leaf bending as an antagonistic transcription factor of BZR1. The phenotypes of lic-1 and LIC–overexpressing lines in erect leaves contribute to ideal plant architecture. Improving this phenotype may be a potential approach to molecular breeding for high yield in rice.
Vyšlo v časopise: Dynamics of Brassinosteroid Response Modulated by Negative Regulator LIC in Rice. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002686 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002686
1. SakamotoT 2006 Phytohormones and rice crop yield: strategies and opportunities for genetic improvement. Transgenic Res 15 399 404
2. SakamotoTMorinakaYOhnishiTSunoharaHFujiokaS 2006 Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol 24 105 109
3. ClouseSDSasseJM 1998 BRASSINOSTEROIDS: Essential Regulators of Plant Growth and Development. Annu Rev Plant Physiol Plant Mol Biol 49 427 451
4. BishopGJKonczC 2002 Brassinosteroids and plant steroid hormone signaling. Plant Cell 14 Suppl S97 110
5. FukudaH 2004 Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5 379 391
6. ChoryJNagpalPPetoCA 1991 Phenotypic and Genetic Analysis of det2, a New Mutant That Affects Light-Regulated Seedling Development in Arabidopsis. Plant Cell 3 445 459
7. SzekeresMNemethKKoncz-KalmanZMathurJKauschmannA 1996 Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85 171 182
8. LiJChoryJ 1997 A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90 929 938
9. MoriMNomuraTOokaHIshizakaMYokotaT 2002 Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol 130 1152 1161
10. WangLXuYZhangCMaQJooSH 2008 OsLIC, a Novel CCCH-Type Zinc Finger Protein with Transcription Activation, Mediates Rice Architecture via Brassinosteroids Signaling. PLoS ONE 3 e3521 doi:10.1371/journal.pone.0003521
11. KimTWWangZY 2010 Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61 681 704
12. TangWDengZWangZY 2009 Proteomics shed light on the brassinosteroid signaling mechanisms. Curr Opin Plant Biol 13 27 33
13. WangZYSetoHFujiokaSYoshidaSChoryJ 2001 BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410 380 383
14. NamKHLiJ 2002 BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110 203 212
15. LiJWenJLeaseKADokeJTTaxFE 2002 BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110 213 222
16. WangXChoryJ 2006 Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313 1118 1122
17. GouXPYinHJHeKDuJBYiJ 2011 Genetic Evidence for an Indispensable Role of Somatic Embryogenesis Receptor Kinases in Brassinosteroid Signaling. PLoS Genet 8 e1002452 doi:10.1371/journal.pgen.1002452
18. TangWKimTWOses-PrietoJASunYDengZ 2008 BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321 557 560
19. WangZYNakanoTGendronJHeJChenM 2002 Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2 505 513
20. RyuHKimKChoHParkJChoeS 2007 Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19 2749 2762
21. HeJXGendronJMYangYLiJWangZY 2002 The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc Natl Acad Sci U S A 99 10185 10190
22. LiJNamKHVafeadosDChoryJ 2001 BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiol 127 14 22
23. RyuHKimKChoHHwangI 2010 Predominant actions of cytosolic BSU1 and nuclear BIN2 regulate subcellular localization of BES1 in brassinosteroid signaling. Mol Cells 29 291 296
24. YanZZhaoJPengPChiharaRKLiJ 2009 BIN2 functions redundantly with other Arabidopsis GSK3-like kinases to regulate brassinosteroid signaling. Plant Physiol 150 710 721
25. ZhaoJPengPSchmitzRJDeckerADTaxFE 2002 Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol 130 1221 1229
26. HeJXGendronJMSunYGampalaSSGendronN 2005 BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307 1634 1638
27. YinYWangZYMora-GarciaSLiJYoshidaS 2002 BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109 181 191
28. GuoHYeHLiLYinY 2009 A family of receptor-like kinases are regulated by BES1 and involved in plant growth in Arabidopsis thaliana. Plant Signal Behav 4 784 786
29. LiLYuXThompsonAGuoMYoshidaS 2009 Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene expression. Plant J 58 275 286
30. LiLYeHGuoHYinY 2010 Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc Natl Acad Sci U S A 107 3918 3923
31. SunYFanXYCaoDMTangWHeK 2010 Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19 765 777
32. YuXLiLZolaJAluruMYeH 2011 A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65 634 646
33. Di RubboSIraniNGRussinovaE 2011 PP2A Phosphatases: The “On-Off” Regulatory Switches of Brassinosteroid Signaling. Sci Signal 4 pe25
34. WuGWangXLiXKamiyaYOteguiMS 2011 Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Sci Signal 4 ra29
35. TangWYuanMWangRYangYWangC 2011 PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13 124 131
36. HongZUeguchi-TanakaMUmemuraKUozuSFujiokaS 2003 A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15 2900 2910
37. TanabeSAshikariMFujiokaSTakatsutoSYoshidaS 2005 A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17 776 790
38. HongZUeguchi-TanakaMFujiokaSTakatsutoSYoshidaS 2005 The Rice brassinosteroid-deficient dwarf2 mutant, defective in the rice homolog of Arabidopsis DIMINUTO/DWARF1, is rescued by the endogenously accumulated alternative bioactive brassinosteroid, dolichosterone. Plant Cell 17 2243 2254
39. WangLXuYYMaQBLiDXuZH 2006 Heterotrimeric G protein alpha subunit is involved in rice brassinosteroid response. Cell Res 16 916 922
40. LiDWangLWangMXuYYLuoW 2009 Engineering OsBAK1 gene as a molecular tool to improve rice architecture for high yield. Plant Biotechnol J 7 791 806
41. UllahHChenJGYoungJCImKHSussmanMR 2001 Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292 2066 2069
42. BaiMYZhangLYGampalaSSZhuSWSongWY 2007 Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci U S A 104 13839 13844
43. KohSLeeSCKimMKKohJHLeeS 2007 T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant Mol Biol 65 453 466
44. YamamuroCIharaYWuXNoguchiTFujiokaS 2000 Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12 1591 1606
45. ZhangLYBaiMYWuJZhuJYWangH 2009 Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21 3767 3780
46. ZhangJLiCWuCXiongLChenG 2006 RMD: a rice mutant database for functional analysis of the rice genome. Nucleic Acids Res 34 D745 748
47. WadaKMarumoSIkekawaNMorisakiMMoriK 1981 Brassinolide and homobrassinolide promotion of lamina inclination of rice seedlings. Plant Cell Physiol 22 323 325
48. MaedaE 1965 Rate of lamina inclination in excised rice leaves. Physiol Plant 18 813 827
49. LiJNamKH 2002 Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295 1299 1301
50. GampalaSSKimTWHeJXTangWDengZ 2007 An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell 13 177 189
51. YinYVafeadosDTaoYYoshidaSAsamiT 2005 A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120 249 259
52. WangHZhuYFujiokaSAsamiTLiJ 2009 Regulation of Arabidopsis brassinosteroid signaling by atypical basic helix-loop-helix proteins. Plant Cell 21 3781 3791
53. SchefeJHLehmannKEBuschmannIRUngerTFunke-KaiserH 2006 Quantitative real-time RT-PCR data analysis: current concepts and the novel “gene expression's CT difference” formula. J Mol Med (Berl) 84 901 910
54. WangZChenCXuYJiangRHanYXuZChongK 2004 A practical vector for efficient knockdown of gene expression in rice (Oryza sativa L.). Plant Mol Biol Rep 22 409 417
55. CloughSJBentAF 1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 735 743
56. ZhaoJZhangWZhaoYGongXGuoL 2007 SAD2, an importin -like protein, is required for UV-B response in Arabidopsis by mediating MYB4 nuclear trafficking. Plant Cell 19 3805 3818
57. YamamotoYYMatsuiMAngLHDengXW 1998 Role of a COP1 interactive protein in mediating light-regulated gene expression in arabidopsis. Plant Cell 10 1083 1094
58. KovtunYChiuWLTenaGSheenJ 2000 Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97 2940 2945
59. MaQDaiXXuYGuoJLiuY 2009 Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol 150 244 256
60. TongHJinYLiuWLiFFangJ 2009 DWARF AND LOW-TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signaling in rice. Plant J 58 803 816
61. YanagisawaSYooSDSheenJ 2003 Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425 521 525
62. XuYYWangXMLiJLiJHWuJS 2005 Activation of the WUS gene induces ectopic initiation of floral meristems on mature stem surface in Arabidopsis thaliana. Plant Mol Biol 57 773 784
63. WangLWangZXuYJooSHKimSK 2009 OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice. Plant J 57 498 510
64. KumarSTamuraKNeiM 2004 MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5 150 163
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
