Hypersensitive to Red and Blue 1 and Its Modification by Protein Phosphatase 7 Are Implicated in the Control of Arabidopsis Stomatal Aperture

English version České info

The stomatal pores are located on the plant leaf epidermis and regulate CO₂ uptake for photosynthesis and the loss of water by transpiration. Their stomatal aperture therefore affects photosynthesis, water use efficiency, and agricultural crop yields. Blue light, one of the environmental signals that regulates the plant stomatal aperture, is perceived by the blue/UV-A light-absorbing cryptochromes and phototropins. The signal transduction cascades that link the perception of light to the stomatal opening response are still largely unknown. Here, we report two new players, Hypersensitive to Red and Blue 1 (HRB1) and Protein Phosphatase 7 (PP7), and their genetic and biochemical interactions in the control of stomatal aperture. Mutations in either HRB1 or PP7 lead to the misregulation of the stomatal aperture and reduce water loss under blue light. Both HRB1 and PP7 are expressed in the guard cells in response to a light-to-dark or dark-to-light transition. HRB1 interacts with PP7 through its N-terminal ZZ-type zinc finger motif and requires a functional PP7 for its stomatal opening response. HRB1 is phosphorylated in vivo, and PP7 can dephosphorylate HRB1. HRB1 is mostly dephosphorylated in a protein complex of 193 kDa in the dark, and blue light increases complex size to 285 kDa. In the pp7 mutant, this size shift is impaired, and HRB1 is predominately phosphorylated. We propose that a modification of HRB1 by PP7 under blue light is essential to acquire a proper conformation or to bring in new components for the assembly of a functional HRB1 protein complex. Guard cells control stomatal opening in response to multiple environmental or biotic stimuli. This study may furnish strategies that allow plants to enjoy the advantages of both constitutive and ABA-induced protection under water-limiting conditions.

Vyšlo v časopise: Hypersensitive to Red and Blue 1 and Its Modification by Protein Phosphatase 7 Are Implicated in the Control of Arabidopsis Stomatal Aperture. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002674
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002674

Souhrn

Zdroje

1. KamiCLorrainSHornitschekPFankhauserC 2010 Light-regulated plant growth and development. Curr Top Dev Biol 91 29 66

2. FranklinKAQuailPH 2010 Phytochrome functions in Arabidopsis development. J Exp Bot 61 11 24

3. YuXLiuHKlejnotJLinC 2010 The Cryptochrome Blue Light Receptors. The Arabidopsis Book 8 e0135 doi:10.1199/tab.0135

4. LiuHLiuBZhaoCPepperMLinC 2011 The action mechanisms of plant cryptochromes. Trends in Plant Science 16 684 691

5. HualaEOellerPWLiscumEHanISLarsenE 1997 Arabidopsis NPH1: A Protein kinase with a putative redox-sensing domain. Science 278 2120 2123

6. KagawaTSakiTSuetsuguNOikawaKIshiguroS 2001 Arabidopsis NPL1: A phototropin homolog controlling the chloroplast high-light avoidance response. Science 291 2138 2141

7. KinoshitaTDoiMSuetsuguNKagawaTWadaM 2001 Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414 656 660

8. KimTHBöhmerMHuHNishimuraNSchroederJI 2010 Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61 561 591

9. KlusenerBYoungJJMurataYAllenGJMoriIC 2002 Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130 2152 2163

10. ShimazakiKDoiMAssmannSMKinoshitaT 2007 Light regulation of stomatal movement. Annu Rev Plant Biol 58 219 247

11. TallmanG 2004 Are diurnal patterns of stomatal movement the result of alternating metabolism of endogenous guard cell ABA and accumulation of ABA delivered to the apoplast around guard cells by transpiration? J Exp Bot 55 1963 1976

12. MaoJZhangYCSangYLiQHYangHQ 2005 A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci 102 12270 12275

13. DengXWMatsuiMWeiNWagnerDChuAM 1992 COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 71 791 801

14. WangHMaLGLiJMZhaoHYDengXW 2001 Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294 154 158

15. YangHQTangRHCashmoreAR 2001 The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell 13 2573 2687

16. InadaSOhgishiMMayamaTOkadaKSakaiT 2004 RPT2 is a signal transducer involved in phototropic response and stomatal opening by association with phototropin 1 in Arabidopsis thaliana. Plant Cell 16 887 896

17. CominelliEGalbiatiMVavasseurAContiLSalaTVuylstekeM 2005 A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15 1196 1200

18. WangFFLianHLKangCYYangHQ 2010 Phytochrome B is involved in mediating red light-induced stomatal opening in Arabidopsis thaliana. Mol Plant 3 246 259

19. LiangYKDubosCDoddICHolroydGHHetheringtonAM 2005 AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol 15 1201 1206

20. KangXChongJNiM 2005 HYPERSENSITIVE TO RED AND BLUE 1, a ZZ-type zinc finger protein, regulates phytochrome B-mediated red and cryptochrome-mediated blue light responses. Plant Cell 17 822 835

21. KangXZhouYSunXNiM 2007 HYPERSENSITIVE TO RED AND BLUE 1 and its C-terminal regulatory function control FLOWERING LOCUS T expression. Plant J 52 937 948

22. HniaKZouitenDCantelSChazaletteDHugonG 2007 ZZ domain of dystrophin and utrophin: topology and mapping of a beta-dystroglycan interaction site. Biochem J 401 667 677

23. MøllerSGKimYSKunkelTChuaNH 2003 PP7 is a positive regulator of blue light signaling in Arabidopsis. Plant Cell 15 1111 1119

24. GenoudTTreviño Santa CruzMKulisicTSparlaFFankhauserCMétrauxJP 2008 The protein phosphatase 7 regulates phytochrome signaling in Arabidopsis. PLoS ONE 3 e2699 doi:10.1371/journal.pone.0002699

25. KutuzovMAEvansDEAndreevaAV 1998 Expression and characterization of PP7, a novel plant protein Ser/Thr phosphatase distantly related to RdgC/PPEF and PP5. FEBS Lett 440 147 152

26. MillaMATownsendJChangIFCushmanJC 2006a The Arabidopsis AtDi19 gene family encodes a novel type of Cys2/His2 zinc-finger protein implicated in ABA-independent dehydration, high-salinity stress and light signaling pathways. Plant Mol Biol 61 13 30

27. HuangHBHoriuchiAGoldbergJGreengardPNairnAC 1997 Site-directed mutagenesis of amino acid residues of protein phosphatase 1 involved in catalysis and inhibitor binding. Proc Natl Acad Sci U S A 94 3530 3535

28. WinterDVinegarBNahalHAmmarRWilsonGV 2007 An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2 e718 doi:10.1371/journal.pone.0000718

29. AndreevaAVKearnsAHawesCREvansDEKutuzovMA 1999 PP7, a gene encoding a novel protein Ser/Thr phosphatase, is expressed primarily in a subset of guard cells in Arabidopsis thaliana. Physiologia Plantarum 106 219 223

30. KinoshitaTOnoNHayashiYMorimotoSNakamuraS 2011 FLOWERING LOCUS T regulates stomatal opening. Cur Biol 21 1232 1238

31. LiuXLCovingtonMFFankhauserCChoryJWagnerDR 2001 ELF3 encodes a circadian clock–regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13 1293 1304

32. FarkasIDombrádiVMiskeiMSzabadosLKonczC 2007 Arabidopsis PPP family of serine/threonine phosphatases. Trends Plant Sci 12 169 176

33. TakemiyaAKinoshitaTAsanumaMShimazakiK 2006 Protein phosphatase 1 positively regulates stomatal opening in response to blue light in Vicia faba. Proc Natl Acad Sci 103 13549 13554

34. TangWYuanMWangRYangYWangC 2011 PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13 124 131

35. MillaMAUnoYChangIFTownsendJMaherEA 2006b A novel yeast two-hybrid approach to identify CDPK substrates: characterization of the interaction between AtCPK11 and AtDi19, a nuclear zinc finger protein. FEBS Lett 580 904 911

36. ZhuSYYuXCWangXJZhaoRLiY 2007 Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19 3019 3036

37. BlomNGammeltoftSBrunakS 1999 Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294 1351 1362

38. YuMSummersJ 1994 Phosphorylation of the duck hepatitis B virus capsid protein associated with conformational changes in the C terminus. J Virol 68 2965 2969

39. KozukaTKongSGDoiMShimazakiKNagataniA 2011 Tissue-autonomous promotion of palisade cell development by phototropin 2 in Arabidopsis. Plant Cell 23 3684 3695

40. NiMTeppermanJMQuailPH 1998 PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95 657 667

41. CurtisMDGrossniklausU 2003 A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133 462 469

42. VoinnetORivasSMestrePBaulcombeD 2003 An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33 949 956

43. WydroMKozubekELehmannP 2006 Optimization of transient Agrobacterium-mediated gene expression system in leaves of Nicotiana benthamiana. Acta Biochim Pol 53 289 298

44. EarleyKWHaagJRPontesOOpperKJuehneT 2006 Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45 616 629

45. BentAFKunkelBNDahlbeckDBrownKLSchmidtR 1994 RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265 1856 1860

46. LeungJMerlotSGiraudatJ 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

47. HilsonPAllemeerschJAltmannTAubourgSAvonA 2004 Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Research 14 2176 2189

48. GordonJ 1991 Use of vanadate as protein-phosphotyrosine phosphatase inhibitor. Methods Enzymol 201 477 482

49. ZhouYNiM 2010 SHB1 truncations and mutations alter its association with a signaling protein complex. Plant Cell 22 703 715