#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Convergence of Light and ABA Signaling on the Promoter


Light is one of the most important environmental cues regulating multiple aspects of plant growth and development, and abscisic acid (ABA) is a plant hormone that plays important roles during many phases of the plant life cycle and in plants' responses to various environmental stresses. How plants integrate the external light signal with endogenous ABA pathway for better adaptation and survival remains poorly understood. Here, we show that BBX21 (also known as SALT TOLERANCE HOMOLOG 2), a B-box (BBX) protein previously shown to positively regulate seedling photomorphogenesis, is also involved in ABA signaling. Our genetic data show that BBX21 may act upstream of several ABA INSENSITIVE (ABI) genes and ELONGATED HYPOCOTYL 5 (HY5) in ABA control of seed germination. Previous studies showed that HY5 acts as a direct activator of ABI5 expression, and that BBX21 interacts with HY5. We further demonstrate that BBX21 negatively regulates ABI5 expression by interfering with HY5 binding to the ABI5 promoter. In addition, ABI5 was shown to directly activate its own expression, whereas BBX21 negatively regulates this activity by directly interacting with ABI5. Together, our study indicates that BBX21 coordinates with HY5 and ABI5 on the ABI5 promoter and that these transcriptional regulators work in concert to integrate light and ABA signaling in Arabidopsis thaliana.


Vyšlo v časopise: Convergence of Light and ABA Signaling on the Promoter. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004197
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004197

Souhrn

Light is one of the most important environmental cues regulating multiple aspects of plant growth and development, and abscisic acid (ABA) is a plant hormone that plays important roles during many phases of the plant life cycle and in plants' responses to various environmental stresses. How plants integrate the external light signal with endogenous ABA pathway for better adaptation and survival remains poorly understood. Here, we show that BBX21 (also known as SALT TOLERANCE HOMOLOG 2), a B-box (BBX) protein previously shown to positively regulate seedling photomorphogenesis, is also involved in ABA signaling. Our genetic data show that BBX21 may act upstream of several ABA INSENSITIVE (ABI) genes and ELONGATED HYPOCOTYL 5 (HY5) in ABA control of seed germination. Previous studies showed that HY5 acts as a direct activator of ABI5 expression, and that BBX21 interacts with HY5. We further demonstrate that BBX21 negatively regulates ABI5 expression by interfering with HY5 binding to the ABI5 promoter. In addition, ABI5 was shown to directly activate its own expression, whereas BBX21 negatively regulates this activity by directly interacting with ABI5. Together, our study indicates that BBX21 coordinates with HY5 and ABI5 on the ABI5 promoter and that these transcriptional regulators work in concert to integrate light and ABA signaling in Arabidopsis thaliana.


Zdroje

1. RizziniL, FavoryJJ, CloixC, FaggionatoD, O'HaraA, et al. (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332: 103–106.

2. YiC, DengXW (2005) COP1-from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol 15: 618–625.

3. OsterlundMT, HardtkeCS, WeiN, DengXW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462–466.

4. HolmM, MaLG, QuLJ, DengXW (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev 16: 1247–1259.

5. KoornneefM, RolffE, SpruitCJP (1980) Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.). Heynh Z Pflanzenphysiol 100: 147–160.

6. OyamaT, ShimuraY, OkadaK (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11: 2983–2995.

7. UlmR, BaumannA, OraveczA, MateZ, AdamE, et al. (2004) Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc Natl Acad Sci U S A 101: 1397–1402.

8. LeeJ, HeK, StolcV, LeeH, FigueroaP, et al. (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19: 731–749.

9. ZhangH, HeH, WangX, WangX, YangX, et al. (2011) Genome-wide mapping of the HY5-mediated gene networks in Arabidopsis that involve both transcriptional and post-transcriptional regulation. Plant J 65: 346–358.

10. KhannaR, KronmillerB, MaszleDR, CouplandG, HolmM, et al. (2009) The Arabidopsis B-box zinc finger family. Plant Cell 21: 3416–3420.

11. PutterillJ, RobsonF, LeeK, SimonR, CouplandG (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80: 847–857.

12. SarmientoF (2013) The BBX subfamily IV: Additional cogs and sprockets to fine-tune light-dependent development. Plant Signal Behav 8: e23831.

13. ChangCS, MaloofJN, WuSH (2011) COP1-mediated degradation of BBX22/LZF1 optimizes seedling development in Arabidopsis. Plant Physiol 156: 228–239.

14. ChangCS, LiYH, ChenLT, ChenWC, HsiehWP, et al. (2008) LZF1, a HY5-regulated transcriptional factor, functions in Arabidopsis de-etiolation. Plant J 54: 205–219.

15. DattaS, HettiarachchiC, JohanssonH, HolmM (2007) SALT TOLERANCE HOMOLOG2, a B-box protein in Arabidopsis that activates transcription and positively regulates light-mediated development. Plant Cell 19: 3242–3255.

16. DattaS, JohanssonH, HettiarachchiC, IrigoyenML, DesaiM, et al. (2008) LZF1/SALT TOLERANCE HOMOLOG3, an Arabidopsis B-box protein involved in light-dependent development and gene expression, undergoes COP1-mediated ubiquitination. Plant Cell 20: 2324–2338.

17. GangappaSN, CroccoCD, JohanssonH, DattaS, HettiarachchiC, et al. (2013) The Arabidopsis B-BOX protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell 25: 1243–1257.

18. HolmM, HardtkeCS, GaudetR, DengXW (2001) Identification of a structural motif that confers specific interaction with the WD40 repeat domain of Arabidopsis COP1. EMBO J 20: 118–127.

19. IndorfM, CorderoJ, NeuhausG, Rodriguez-FrancoM (2007) Salt tolerance (STO), a stress-related protein, has a major role in light signalling. Plant J 51: 563–574.

20. JiangL, WangY, LiQF, BjornLO, HeJX, et al. (2012) Arabidopsis STO/BBX24 negatively regulates UV-B signaling by interacting with COP1 and repressing HY5 transcriptional activity. Cell Res 22: 1046–1057.

21. KumagaiT, ItoS, NakamichiN, NiwaY, MurakamiM, et al. (2008) The common function of a novel subfamily of B-Box zinc finger proteins with reference to circadian-associated events in Arabidopsis thaliana. Biosci Biotechnol Biochem 72: 1539–1549.

22. YanH, MarquardtK, IndorfM, JuttD, KircherS, et al. (2011) Nuclear localization and interaction with COP1 are required for STO/BBX24 function during photomorphogenesis. Plant Physiol 156: 1772–1782.

23. CutlerSR, RodriguezPL, FinkelsteinRR, AbramsSR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61: 651–679.

24. NakashimaK, Yamaguchi-ShinozakiK (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32: 959–970.

25. KobayashiY, MurataM, MinamiH, YamamotoS, KagayaY, et al. (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44: 939–949.

26. 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.

27. FinkelsteinRR, LynchTJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12: 599–609.

28. FinkelsteinRR, WangML, LynchTJ, RaoS, GoodmanHM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10: 1043–1054.

29. ParcyF, ValonC, RaynalM, Gaubier-ComellaP, DelsenyM, et al. (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6: 1567–1582.

30. Lopez-MolinaL, MongrandS, ChuaNH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci U S A 98: 4782–4787.

31. Lopez-MolinaL, MongrandS, McLachlinDT, ChaitBT, ChuaNH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32: 317–328.

32. PiskurewiczU, JikumaruY, KinoshitaN, NambaraE, KamiyaY, et al. (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20: 2729–2745.

33. ChenH, ZhangJ, NeffMM, HongSW, ZhangH, et al. (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci U S A 105: 4495–4500.

34. LeungJ, MerlotS, GiraudatJ (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9: 759–771.

35. ParcyF, ValonC, KoharaA, MiseraS, GiraudatJ (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9: 1265–1277.

36. LabyRJ, KincaidMS, KimD, GibsonSI (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response.. Plant J 23: 587–596.

37. ReevesWM, LynchTJ, MobinR, FinkelsteinRR (2011) Direct targets of the transcription factors ABA-Insensitive(ABI)4 and ABI5 reveal synergistic action by ABI4 and several bZIP ABA response factors. Plant Mol Biol 75: 347–363.

38. AchardP, ChengH, De GrauweL, DecatJ, SchouttetenH, et al. (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311: 91–94.

39. CasalJJ, FankhauserC, CouplandG, BlazquezMA (2004) Signalling for developmental plasticity. Trends Plant Sci 9: 309–314.

40. TangW, JiQ, HuangY, JiangZ, BaoM, et al. (2013) FAR-RED ELONGATED HYPOCOTYL3 and FAR-RED IMPAIRED RESPONSE1 transcription factors integrate light and abscisic acid signaling in Arabidopsis. Plant Physiol 163: 857–866.

41. OhE, KangH, YamaguchiS, ParkJ, LeeD, et al. (2009) Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 21: 403–419.

42. SmalleJ, KurepaJ, YangP, EmborgTJ, BabiychukE, et al. (2003) The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell 15: 965–980.

43. StoneSL, WilliamsLA, FarmerLM, VierstraRD, CallisJ (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18: 3415–3428.

44. MazzellaMA, AranaMV, StaneloniRJ, PerelmanS, Rodriguez BatillerMJ, et al. (2005) Phytochrome control of the Arabidopsis transcriptome anticipates seedling exposure to light. Plant Cell 17: 2507–2516.

45. BossiF, CordobaE, DupréP, MendozaMS, RománCS, et al. (2009) The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2.2 genes during sugar signaling. Plant J 59: 359–374.

46. OhE, KimJ, ParkE, KimJI, KangC, et al. (2004) PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16: 3045–3058.

47. OhE, YamaguchiS, HuJ, YusukeJ, JungB, et al. (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19: 1192–1208.

48. SeoM, HanadaA, KuwaharaA, EndoA, OkamotoM, et al. (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48: 354–366.

49. ParkJ, LeeN, KimW, LimS, ChoiG (2011) ABI3 and PIL5 collaboratively activate the expression of SOMNUS by directly binding to its promoter in imbibed Arabidopsis seeds. Plant Cell 23: 1404–1415.

50. Leon-KloosterzielKM, GilMA, RuijsGJ, JacobsenSE, OlszewskiNE, et al. (1996) Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 10: 655–661.

51. KoornneefJM, Brinkhorst-Van der SwanDLC, KarssenCM (1982) The isolation of abscisic acid (ABA)-deficient mutants by selection of induced revertants in non-germinating gibberellin-sensitive lines of Arabidopsis thaliana. Theor Appl Genet 61: 385–393.

52. RenX, ChenZ, LiuY, ZhangH, ZhangM, et al. (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63: 417–429.

53. PanX, WeltiR, WangX (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5: 986–992.

54. LiJ, LiG, GaoS, MartinezC, HeG, et al. (2010) Plant Cell 22: 3634–3649.

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

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 2
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#