PIF4–Mediated Activation of Expression Integrates Temperature into the Auxin Pathway in Regulating Hypocotyl Growth

English version České info

Higher plants adapt their growth to high temperature by a dramatic change in plant architecture. It has been shown that the transcriptional regulator phytochrome-interacting factor 4 (PIF4) and the phytohormone auxin are involved in the regulation of high temperature–induced hypocotyl elongation in Arabidopsis. Here we report that PIF4 regulates high temperature–induced hypocotyl elongation through direct activation of the auxin biosynthetic gene YUCCA8 (YUC8). We show that high temperature co-upregulates the transcript abundance of PIF4 and YUC8. PIF4–dependency of high temperature–mediated induction of YUC8 expression as well as auxin biosynthesis, together with the finding that overexpression of PIF4 leads to increased expression of YUC8 and elevated free IAA levels in planta, suggests a possibility that PIF4 directly activates YUC8 expression. Indeed, gel shift and chromatin immunoprecipitation experiments demonstrate that PIF4 associates with the G-box–containing promoter region of YUC8. Transient expression assay in Nicotiana benthamiana leaves support that PIF4 directly activates YUC8 expression in vivo. Significantly, we show that the yuc8 mutation can largely suppress the long-hypocotyl phenotype of PIF4–overexpression plants and also can reduce high temperature–induced hypocotyl elongation. Genetic analyses reveal that the shy2-2 mutation, which harbors a stabilized mutant form of the IAA3 protein and therefore is defective in high temperature–induced hypocotyl elongation, largely suppresses the long-hypocotyl phenotype of PIF4–overexpression plants. Taken together, our results illuminate a molecular framework by which the PIF4 transcriptional regulator integrates its action into the auxin pathway through activating the expression of specific auxin biosynthetic gene. These studies advance our understanding on the molecular mechanism underlying high temperature–induced adaptation in plant architecture.

Vyšlo v časopise: PIF4–Mediated Activation of Expression Integrates Temperature into the Auxin Pathway in Regulating Hypocotyl Growth. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002594
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002594

Souhrn

Zdroje

1. KoiniMAAlveyLAllenTTilleyCAHarberdNP 2009 High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19 408 413

2. BalasubramanianSSureshkumarSLempeJWeigelD 2006 Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2 e106 doi:10.1371/journal.pgen.0020106

3. GrayWMOstinASandbergGRomanoCPEstelleM 1998 High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci USA 95 7197 7202

4. KumarSVWiggePA 2010 H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140 136 147

5. ZhaoY 2010 Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61 49 64

6. MashiguchiKTanakaKSakaiTSugawaraSKawaideH 2011 The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci USA 108 18512 18517

7. ZhaoYChristensenSKFankhauserCCashmanJRCohenJD 2001 A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291 306 309

8. ChengYDaiXZhaoY 2006 Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20 1790 1799

9. ChengYDaiXZhaoY 2007 Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19 2430 2439

10. TaoYFerrerJLLjungKPojerFHongF 2008 Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133 164 176

11. StepanovaANRobertson-HoytJYunJBenaventeLMXieDY 2008 TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133 177 191

12. WonCShenXMashiguchiKZhengZDaiX 2011 Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci USA 108 18518 18523

13. StepanovaANYunJRoblesLMNovakOHeW 2011 The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23 3961 3973

14. LeivarPQuailPH 2011 PIFs: pivotal components in a cellular signaling hub. Trends Plants Sci 16 19 28

15. LauOSDengXW 2010 Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13 571 577

16. StavangJAGallego-BartolomeJGomezMDYoshidaSAsamiT 2009 Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J 60 589 601

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

18. MoonJZhuLShenHHuqE 2008 PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proc Natl Acad Sci USA 105 9433 9438

19. de LucasMDaviereJMRodriguez-FalconMPontinMIglesias-PedrazJM 2008 A molecular framework for light and gibberellin control of cell elongation. Nature 451 480 484

20. TianQUhlirNJReedJW 2002 Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell 14 301 319

21. FukakiHTamedaSMasudaHTasakaM 2002 Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29 153 168

22. NagpalPWalkerLMYoungJCSonawalaATimpteC 2000 AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123 563 574

23. YangXLeeSSoJHDharmasiriSDharmasiriN 2004 The IAA1 protein is encoded by AXR5 and is a substrate of SCF(TIR1). Plant J 40 772 782

24. RoggLELasswellJBartelB 2001 A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13 465 480

25. PatelDFranklinKA 2009 Temperature-regulation of plant architecture. Plant Signal Behav 4 577 579

26. FranklinKAKnightH 2010 Unravelling plant temperature signalling networks. New Phytol 185 8 10

27. CassonSAFranklinKAGrayJEGriersonCSWhitelamGCHetheringtonAM 2009 Phytochrome B and PIF4 regulate stomatal development in response to light quantity. Curr Biol 19 229 234

28. LucyshynDWiggePA 2009 Plant development: PIF4 integrates diverse environmental signals. Curr Biol 19 R265 266

29. FranklinKALeeSHPatelDKumarSVSpartzAK 2011 PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA 108 20231 20235

30. HallidayKJMartinez-GarciaJFJosseEM 2009 Integration of light and auxin signaling. Cold Spring Harb Perspect Biol 1 a001586

31. FranklinKA 2008 Shade avoidance. New Phytol 179 930 944

32. NozueKHarmerSLMaloofJN 2011 Genomic analysis of circadian clock-, light-, and growth-correlated genes reveals PHYTOCHROME-INTERACTING FACTOR5 as a modulator of auxin signaling in Arabidopsis. Plant Physiol 156 357 372

33. LorrainSAllenTDuekPDWhitelamGCFankhauserC 2008 Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53 312 323

34. HornitschekPLorrainSZoeteVMichielinOFankhauserC 2009 Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J 28 3893 3902

35. PozoJCTimpteCTanSCallisJEstelleM 1998 The ubiquitin-related protein RUB1 and auxin response in Arabidopsis. Science 280 1760 1763

36. ChapmanEJEstelleM 2009 Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43 265 285

37. SunJXuYYeSJiangHChenQ 2009 Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21 1495 1511

38. LincolnCBrittonJHEstelleM 1990 Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2 1071 1080

39. AlonsoJMStepanovaANLeisseTJKimCJChenH 2003 Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 653 657

40. SambrookJRussellD 2001 Molecular cloning, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

41. BechtoldNPelletierG 1998 In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82 259 266

42. GendrelAVLippmanZMartienssenRColotV 2005 Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2 213 218

43. HuqEQuailPH 2002 PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J 21 2441 2450

44. ChenQSunJZhaiQZhouWQiL 2011 The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23 3335 3352

45. NakagawaTKuroseTHinoTTanakaKKawamukaiM 2007 Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104 34 41

46. ZhouWWeiLXuJZhaiQJiangH 2010 Arabidopsis Tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22 3692 3709