The U-Box E3 Ubiquitin Ligase TUD1 Functions with a Heterotrimeric G α Subunit to Regulate Brassinosteroid-Mediated Growth in Rice

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Heterotrimeric G proteins are an important group of signaling molecules found in eukaryotes. They function with G-protein-coupled-receptors (GPCRs) to transduce various signals such as steroid hormones in animals. Nevertheless, their functions in plants are not well-defined. Previous studies suggested that the heterotrimeric G protein α subunit known as D1/RGA1 in rice is involved in a phytohormone gibberellin-mediated signaling pathway. Evidence also implicates D1 in the action of a second phytohormone Brassinosteroid (BR) and its pathway. However, it is unclear how D1 functions in this pathway, because so far no partner has been identified to act with D1. In this study, we report a D1 genetic interactor Taihu Dwarf1 (TUD1) that encodes a functional U-box E3 ubiquitin ligase. Genetic, phenotypic, and physiological analyses have shown that tud1 is epistatic to d1 and is less sensitive to BR treatment. Histological observations showed that the dwarf phenotype of tud1 is mainly due to decreased cell proliferation and disorganized cell files in aerial organs. Furthermore, we found that D1 directly interacts with TUD1. Taken together, these results demonstrate that D1 and TUD1 act together to mediate a BR-signaling pathway. This supports the idea that a D1-mediated BR signaling pathway occurs in rice to affect plant growth and development.

Vyšlo v časopise: The U-Box E3 Ubiquitin Ligase TUD1 Functions with a Heterotrimeric G α Subunit to Regulate Brassinosteroid-Mediated Growth in Rice. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003391
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003391

Souhrn

Zdroje

1. ClouseSD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23: 1219–1230.

2. YeH, LiL, YinY (2011) Recent Advances in the Regulation of Brassinosteroid Signaling and Biosynthesis Pathways. Journal of Integrative Plant Biology 53: 455–468.

3. SheJ, HanZ, KimTW, WangJ, ChengW, et al. (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474: 472–476.

4. KimTW, WangZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61: 681–704.

5. YuX, LiL, ZolaJ, AluruM, YeH, et al. (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65: 634–646.

6. YamamuroC, IharaY, WuX, NoguchiT, FujiokaS, et al. (2000) Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12: 1591–1606.

7. BaiMY, ZhangLY, GampalaSS, ZhuSW, SongWY, et al. (2007) Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci U S A 104: 13839.

8. TongH, ChuC (2011) Brassinosteroid Signaling and Application in Rice. J Genet Genomics 39 (1) 3–9 doi:10.1016/j.jgg.2011.12.001

9. MontoyaT, NomuraT, FarrarK, KanetaT, YokotaT, et al. (2002) Cloning the tomato curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling. Plant Cell 14: 3163–3176.

10. ChonoM, HondaI, ZeniyaH, YoneyamaK, SaishoD, et al. (2003) A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant physiol 133: 1209–1219.

11. NomuraT, BishopGJ, KanetaT, ReidJB, ChoryJ, et al. (2003) The LKA gene is a BRASSINOSTEROID INSENSITIVE 1 homolog of pea. Plant J 36: 291–300.

12. BishopGJ (2003) Brassinosteroid Mutants of Crops. J Plant Growth Regul 22: 325–335.

13. WangL, XuYY, MaQB, LiD, XuZH, et al. (2006) Heterotrimeric G protein alpha subunit is involved in rice brassinosteroid response. Cell Res 16: 916–922.

14. OkiK, InabaN, KitagawaK, FujiokaS, KitanoH, et al. (2009) Function of the alpha subunit of rice heterotrimeric G protein in brassinosteroid signaling. Plant Cell Physiol 50: 161–172.

15. GaoY, WangS, AsamiT, ChenJG (2008) Loss-of-function mutations in the Arabidopsis heterotrimeric G-protein α subunit enhance the developmental defects of brassinosteroid signaling and biosynthesis mutants. Plant and Cell Physiol 49: 1013.

16. AssmannSM (2002) Heterotrimeric and unconventional GTP binding proteins in plant cell signaling. Plant Cell 14: S355–S373.

17. Van EpsN, PreiningerAM, AlexanderN, KayaAI, MeierS, et al. (2011) Interaction of a G protein with an activated receptor opens the interdomain interface in the alpha subunit. Proc Natl Acad Sci U S A 108: 9420.

18. UtsunomiyaY, SamejimaC, TakayanagiY, IzawaY, YoshidaT, et al. (2011) Suppression of the rice heterotrimeric G protein beta-subunit gene, RGB1, causes dwarfism and browning of internodes and lamina joint regions. Plant J 67: 907–916.

19. TempleBRS, JonesAM (2007) The plant heterotrimeric G-protein complex. Annu Rev Plant Biol 58: 249–266.

20. KatoC, MizutaniT, TamakiH, KumagaiH, KamiyaT, et al. (2004) Characterization of heterotrimeric G protein complexes in rice plasma membrane. Plant J 38: 320–331.

21. Perfus-BarbeochL, JonesAM, AssmannSM (2004) Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. Curr Opin Plant Biol 7: 719–731.

22. Ueguchi-TanakaM, FujisawaY, KobayashiM, AshikariM, IwasakiY, et al. (2000) Rice dwarf mutant d1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc Natl Acad Sci U S A 97: 11638–11643.

23. SuharsonoU, FujisawaY, KawasakiT, IwasakiY, SatohH, et al. (2002) The heterotrimeric G protein α subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci U S A 99: 13307.

24. OkiK, InabaN, KitanoH, TakahashiS, FujisawaY, et al. (2009) Study of novel d1 alleles, defective mutants of the alpha subunit of heterotrimeric G-protein in rice. Genes Genet Syst 84: 35–42.

25. Nakagawa H, Tanaka A, Mori M (2011) Brassinosteroid signaling in rice. In: Hayat S, Ahmad A, editors. Brassinosteroids: A Class of Plant Hormone: Springer Science+Business Media B.V. pp. 83–117.

26. VierstraRD (2009) The ubiquitin–26S proteasome system at the nexus of plant biology. Nature Reviews Molecular Cell Biol 10: 385–397.

27. MoonJ, ParryG, EstelleM (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16: 3181–3195.

28. AndersenP, KragelundBB, OlsenAN, LarsenFH, ChuaNH, et al. (2004) Structure and biochemical function of a prototypical Arabidopsis U-box domain. J Biol Chem 279: 40053–40061.

29. AzevedoC, Santos-RosaMJ, ShirasuK (2001) The U-box protein family in plants. Trends Plant Sci 6: 354–358.

30. YeeD, GoringDR (2009) The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J Exp Bot 60: 1109–1121.

31. ZengLR, ParkCH, VenuRC, GoughJ, WangGL (2008) Classification, expression pattern, and E3 ligase activity assay of rice U-box-containing proteins. Mol Plant 1: 800–815.

32. AmadorV, MonteE, PratS (2001) Gibberellins signal nuclear import of PHOR1, a photoperiod-responsive protein with homology to Drosophila armadillo. Cell 106: 343–354.

33. ZengLR, QuS, BordeosA, YangC, BaraoidanM, et al. (2004) Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16: 2795–2808.

34. ChoSK, RyuMY, SongC, KwakJM, KimWT (2008) Arabidopsis PUB22 and PUB23 are homologous U-Box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell 20: 1899–1914.

35. StoneSL, AndersonEM, MullenRT, GoringDR (2003) ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15: 885–898.

36. TakedaK (1977) Internode elongation and dwarfism in some gramineous plants. Gamma Field Sym 16: 1–18.

37. IkedaA, Ueguchi-TanakaM, SonodaY, KitanoH, KoshiokaM, et al. (2001) slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13: 999–1010.

38. ItohH, SasakiA, Ueguchi-TanakaM, IshiyamaK, KobayashiM, et al. (2005) Dissection of the phosphorylation of rice DELLA protein, SLENDER RICE1. Plant and Cell Physiol 46: 1392.

39. ZhuY, NomuraT, XuY, ZhangY, PengY, et al. (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18: 442–456.

40. TsaiYC, WeirNR, HillK, ZhangW, KimHJ, et al. (2012) Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol 158: 1666–1684.

41. WadaK, MarumoS, IkekawaN, MorisakiM, MoriK (1981) Brassinolide and homobrassinolide promotion of lamina inclination of rice seedlings. Plant and Cell Physiol 22: 323–325.

42. HongZ, Ueguchi-TanakaM, Shimizu-SatoS, et al. (2002) Loss-of-function of a rice brassinosteroid biosynthetic enzyme, c-6 oxidase, prevents the organized arrangement and polar elongation of cells in the leaves and stem. Plant J 32: 495–508.

43. SakamotoT, MorinakaY, OhnishiT, et al. (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nature Biotech 24: 105–109.

44. HongZ, Ueguchi-TanakaM, UmemuraK, et al. (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.

45. HieiY, OhtaS, KomariT, KumashiroT (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6: 271–282.

46. XieQ, GuoHS, DallmanG, FangS, WeissmanAM, et al. (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419: 167–170.

47. WaadtR, SchmidtLK, LohseM, HashimotoK, BockR, et al. (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J 56: 505–516.

48. QiaoH, WangF, ZhaoL, ZhouJ, LaiZ, et al. (2004) The F-box protein AhSLF-S2 controls the pollen function of S-RNase–based self-incompatibility. Plant Cell 16: 2307–2322.

49. ChenJG, GaoY, JonesAM (2006) Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots. Plant Physiol 141: 887–897.

50. Perfus-BarbeochL, JonesAM, AssmannSM (2004) Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. Curr Opin Plant Biol 7: 719–731.

51. ChenJG (2008) Heterotrimeric G-proteins in plant development. Front Biosci 13: 3321–3333.

52. FanC, XingY, MaoH, LuT, HanB, et al. (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112: 1164–1171.

53. HuangX, QianQ, LiuZ, SunH, HeS, et al. (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41: 494–497.

54. BotellaJR (2012) Can heterotrimeric G proteins help to feed the world? Trends Plant Sci 17: 563–568.