DELLA Protein Degradation Is Controlled by a Type-One Protein Phosphatase, TOPP4

English version České info

Gibberellins (GAs) are essential regulators of plant growth and development. They are tightly related to crop productivity in the first “green revolution.” GA triggers its responses by targeting DELLA proteins, the important repressors, for degradation. This process is believed to be regulated by protein phosphorylation and dephosphorylation, but there are not any reports describing the identification of phosphatases regulating this critical event. By screening an ethyl methane sulfonate (EMS)-mutagenized Arabidopsis thaliana population, we identified a protein phosphatase TOPP4, a member of protein phosphatase 1 (PP1), that acts as a positive regulator in the GA signaling pathway. TOPP4 promotes the GA-induced degradation of DELLA proteins by directly dephosphorylating these proteins. This study provides an important insight for the switch role of protein phosphorylation and dephosphorylation in GA signal transduction and sheds light on PP1 protein phosphatases in regulating plant growth and development.

Vyšlo v časopise: DELLA Protein Degradation Is Controlled by a Type-One Protein Phosphatase, TOPP4. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004464
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004464

Souhrn

Zdroje

1. RichardsDE, KingKE, Ait-AliT, HarberdNP (2001) How gibberellin regulates plant growth and development: A molecular genetic analysis of gibberellin signaling. Annu Rev Plant Physiol Plant Mol Biol 52 : 67–88.

2. FleetCM, SunTP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8 : 77–85.

3. SunTP (2008) Gibberellin metabolism, perception and signaling pathways in Arabidopsis. The Arabidopsis Book 6: e0103 doi/10.1199/tab.0103

4. HarberdNP, BelfieldE, YasumuraY (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell 21 : 1328–1339.

5. AchardP, GenschikP (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60 : 1085–1092.

6. PengJ, CarolP, RichardsDE, KingKE, CowlingRJ, et al. (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11 : 3194–3205.

7. SilverstoneAL, CiampaglioCN, SunT (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10 : 155–169.

8. WenCK, ChangC (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14 : 87–100.

9. LeeS, ChengH, KingKE, WangW, HeY, et al. (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16 : 646–658.

10. DillA, SunT (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159 : 777–785.

11. KingKE, MoritzT, HarberdNP (2001) Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159 : 767–776.

12. ChengH, QinL, LeeS, FuX, RichardsDE, et al. (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131 : 1055–1064.

13. TylerL, ThomasSG, HuJ, DillA, AlonsoJM, et al. (2004) Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135 : 1008–1019.

14. YuH, ItoT, ZhaoY, PengJ, KumarP, et al. (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci U S A 101 : 7827–7832.

15. Ueguchi-TanakaM, AshikariM, NakajimaM, ItohH, KatohE, et al. (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437 : 693–698.

16. NakajimaM, ShimadaA, TakashiY, KimYC, ParkSH, et al. (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46 : 880–889.

17. GriffithsJ, MuraseK, RieuI, ZentellaR, ZhangZL, et al. (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18 : 3399–3414.

18. AriizumiT, MuraseK, SunTP, SteberCM (2008) Proteolysis-independent downregulation of DELLA repression in Arabidopsis by the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1. Plant Cell 20 : 2447–2459.

19. DillA, ThomasSG, HuJ, SteberCM, SunTP (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16 : 1392–1405.

20. McGinnisKM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15 : 1120–1130.

21. SasakiA, ItohH, GomiK, Ueguchi-TanakaM, IshiyamaK, et al. (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299 : 1896–1898.

22. FuX, RichardsDE, FleckB, XieD, BurtonN, et al. (2004) The Arabidopsis mutant sleepy1gar2-1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16 : 1406–1418.

23. SunT-p, GublerF (2004) Molecular mechanism of gibberellin signaling in plants. Annual Review of Plant Biology 55 : 197–223.

24. FengS, MartinezC, GusmaroliG, WangY, ZhouJ, et al. (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451 : 475–479.

25. de LucasM, DaviereJM, Rodriguez-FalconM, PontinM, Iglesias-PedrazJM, et al. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451 : 480–484.

26. ZhangZL, OgawaM, FleetCM, ZentellaR, HuJ, et al. (2011) Scarecrow-like 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proc Natl Acad Sci U S A 108 : 2160–2165.

27. ParkJ, NguyenKT, ParkE, JeonJS, ChoiG (2013) DELLA proteins and their interacting RING Finger proteins repress gibberellin responses by binding to the promoters of a subset of gibberellin-responsive genes in Arabidopsis. Plant Cell 25 : 927–943.

28. ZentellaR, ZhangZL, ParkM, ThomasSG, EndoA, et al. (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19 : 3037–3057.

29. WeissD, OriN (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144 : 1240–1246.

30. BaiMY, ShangJX, OhE, FanM, BaiY, et al. (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14 : 810–817.

31. HouX, LeeLY, XiaK, YanY, YuH (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19 : 884–894.

32. AchardP, GongF, CheminantS, AliouaM, HeddenP, et al. (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20 : 2117–2129.

33. AchardP, RenouJP, BerthomeR, HarberdNP, GenschikP (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 18 : 656–660.

34. LocascioA, BlazquezMA, AlabadiD (2013) Dynamic regulation of cortical microtubule organization through prefoldin-DELLA interaction. Curr Biol 23 : 804–809.

35. ShimadaA, Ueguchi-TanakaM, SakamotoT, FujiokaS, TakatsutoS, et al. (2006) The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid synthesis. Plant J 48 : 390–402.

36. WangF, ZhuD, HuangX, LiS, GongY, et al. (2009) Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21 : 2378–2390.

37. DaiC, XueHW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J 29 : 1916–1927.

38. ShiY (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139 : 468–484.

39. CeulemansH, BollenM (2004) Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol Rev 84 : 1–39.

40. LinQ, LiJ, SmithRD, WalkerJC (1998) Molecular cloning and chromosomal mapping of type one serine/threonine protein phosphatases in Arabidopsis thaliana. Plant Mol Biol 37 : 471–481.

41. TakemiyaA, AriyoshiC, ShimazakiK (2009) Identification and functional characterization of inhibitor-3, a regulatory subunit of protein phosphatase 1 in plants. Plant Physiol 150 : 144–156.

42. TakemiyaA, YamauchiS, YanoT, AriyoshiC, ShimazakiK (2013) Identification of a regulatory subunit of protein phosphatase 1 which mediates blue light signaling for stomatal opening. Plant Cell Physiol 54 : 24–35.

43. KoornneefM, van der VeenJH (1980) Induction and analysis of gibberellin sensitive mutants. Theor Appl Genet 58 : 257–263.

44. KoornneefM, ElgersmaA, HanhartCJ, van Loenen-MartinetEP, van RijnL, et al. (1985) A gibberellin insensitive mutant of Arabidopsis thaliana. Physiol Plant 65 : 33–39.

45. OssowskiS, SchwabR, WeigelD (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53 : 674–690.

46. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 : 735–743.

47. SunT, GoodmanHM, AusubelFM (1992) Cloning the Arabidopsis GA1 locus by genomic subtraction. Plant Cell 4 : 119–128.

48. MichniewiczM, ZagoMK, AbasL, WeijersD, SchweighoferA, et al. (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130 : 1044–1056.

49. TangW, YuanM, WangR, YangY, WangC, et al. (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13 : 124–131.

50. UmezawaT, SugiyamaN, MizoguchiM, HayashiS, MyougaF, et al. (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci U S A 106 : 17588–17593.

51. DaiM, ZhangC, KaniaU, ChenF, XueQ, et al. (2012) A PP6-type phosphatase holoenzyme directly regulates PIN phosphorylation and auxin efflux in Arabidopsis. Plant Cell 24 : 2497–2514.

52. LiuY, ZhangS (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16 : 3386–3399.

53. SkottkeKR, YoonGM, KieberJJ, DeLongA (2011) Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genet 7: e1001370.

54. FuX, RichardsDE, Ait-AliT, HynesLW, OughamH, et al. (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14 : 3191–3200.

55. GomiK, SasakiA, ItohH, Ueguchi-TanakaM, AshikariM, et al. (2004) GID2, an F-box subunit of the SCF E3 complex, specifically interacts with phosphorylated SLR1 protein and regulates the gibberellin-dependent degradation of SLR1 in rice. Plant J 37 : 626–634.

56. ItohH, SasakiA, Ueguchi-TanakaM, IshiyamaK, KobayashiM, et al. (2005) Dissection of the phosphorylation of rice DELLA protein, SLENDER RICE1. Plant Cell Physiol 46 : 1392–1399.

57. HussainA, CaoD, ChengH, WenZ, PengJ (2005) Identification of the conserved serine/threonine residues important for gibberellin-sensitivity of Arabidopsis RGL2 protein. Plant J 44 : 88–99.

58. TangW, KimTW, Oses-PrietoJA, SunY, DengZ, et al. (2008) BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321 : 557–560.

59. KerkD, BulgrienJ, SmithDW, BarsamB, VeretnikS, et al. (2002) The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiol 129 : 908–925.

60. TakemiyaA, KinoshitaT, AsanumaM, ShimazakiK (2006) Protein phosphatase 1 positively regulates stomatal opening in response to blue light in Vicia faba. Proc Natl Acad Sci U S A 103 : 13549–13554.

61. CohenPT (2002) Protein phosphatase 1-targeted in many directions. J Cell Sci 115 : 241–256.

62. MoorheadGB, Trinkle-MulcahyL, Ulke-LemeeA (2007) Emerging roles of nuclear protein phosphatases. Nat Rev Mol Cell Biol 8 : 234–244.

63. TempletonGW, NimickM, MorriceN, CampbellD, GoudreaultM, et al. (2011) Identification and characterization of AtI-2, an Arabidopsis homologue of an ancient protein phosphatase 1 (PP1) regulatory subunit. Biochem J 435 : 73–83.

64. HeroesE, LesageB, GornemannJ, BeullensM, Van MeerveltL, et al. (2013) The PP1 binding code: a molecular-lego strategy that governs specificity. FEBS J 280 : 584–595.

65. KoniecznyA, AusubelFM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4 : 403–410.

66. BellCJ, EckerJR (1994) Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19 : 137–144.

67. HouX, LiL, PengZ, WeiB, TangS, et al. (2010) A platform of high-density INDEL/CAPS markers for map-based cloning in Arabidopsis. Plant J 63 : 880–888.

68. MurashigeT, SkoogF (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15 : 473–497.

69. YuanT, FujiokaS, TakatsutoS, MatsumotoS, GouX, et al. (2007) BEN1, a gene encoding a dihydroflavonol 4-reductase (DFR)-like protein, regulates the levels of brassinosteroids in Arabidopsis thaliana. Plant J 51 : 220–233.

70. YooSD, ChoYH, SheenJ (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2 : 1565–1572.

71. LiJ, WenJ, LeaseKA, DokeJT, TaxFE, et al. (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110 : 213–222.

72. JangIC, YangJY, SeoHS, ChuaNH (2005) HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev 19 : 593–602.

73. SongY, WuK, DhaubhadelS, AnL, TianL (2010) Arabidopsis DNA methyltransferase AtDNMT2 associates with histone deacetylase AtHD2s activity. Biochem Biophys Res Commun 396 : 187–192.

74. LuQ, TangX, TianG, WangF, LiuK, et al. (2010) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J 61 : 259–270.