LEUNIG_HOMOLOG Mediates MYC2-Dependent Transcriptional Activation in Cooperation with the Coactivators HAC1 and MED25.

Yanrong You, Qingzhe Zhai, Chunpeng An, Chuanyou Li
Author Information
  1. Yanrong You: State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China. ORCID
  2. Qingzhe Zhai: State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China cyli@genetics.ac.cn qzzhai@genetics.ac.cn. ORCID
  3. Chunpeng An: State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China. ORCID
  4. Chuanyou Li: State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China cyli@genetics.ac.cn qzzhai@genetics.ac.cn. ORCID

Abstract

Groucho/Thymidine uptake 1 (Gro/Tup1) family proteins are evolutionarily conserved transcriptional coregulators in eukaryotic cells. Despite their prominent function in transcriptional repression, little is known about their role in transcriptional activation and the underlying mechanism. Here, we report that the plant Gro/Tup1 family protein LEUNIG_HOMOLOG (LUH) activates MYELOCYTOMATOSIS2 (MYC2)-directed transcription of and via the Mediator complex coactivator and the histone acetyltransferase HAC1. We show that the Mediator subunit MED25 physically recruits LUH to MYC2 target promoters that then links MYC2 with HAC1-dependent acetylation of Lys-9 of histone H3 (H3K9ac) to activate and Moreover, LUH promotes hormone-dependent enhancement of protein interactions between MYC2 and its coactivators MED25 and HAC1. Our results demonstrate that LUH interacts with MED25 and HAC1 through its distinct domains, thus imposing a selective advantage by acting as a scaffold for MYC2 activation. Therefore, the function of LUH in regulating jasmonate signaling is distinct from the function of TOPLESS, another member of the Gro/Tup1 family that represses MYC2-dependent gene expression in the resting stage.

References

  1. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  2. Methods Mol Biol. 2013;1011:35-49 [PMID: 23615986]
  3. Ann Bot. 2013 Jun;111(6):1021-58 [PMID: 23558912]
  4. PLoS Genet. 2013;9(7):e1003653 [PMID: 23935516]
  5. Genome Biol. 2008 Jan 31;9(1):205 [PMID: 18254933]
  6. Dev Cell. 2010 Dec 14;19(6):884-94 [PMID: 21145503]
  7. Essays Biochem. 2015;58:83-100 [PMID: 26374889]
  8. Plant Cell. 2007 Jul;19(7):2225-45 [PMID: 17616737]
  9. Bioinformatics. 2012 Aug 15;28(16):2184-5 [PMID: 22743226]
  10. Plant Cell. 2004 Aug;16(8):2117-27 [PMID: 15258265]
  11. PLoS Genet. 2013 Apr;9(4):e1003422 [PMID: 23593022]
  12. Plant Cell. 2015 Jun;27(6):1634-49 [PMID: 26071420]
  13. Nature. 2010 Nov 18;468(7322):400-5 [PMID: 20927106]
  14. Plant J. 2007 Nov;52(4):615-26 [PMID: 17877703]
  15. Plant Cell. 2009 Aug;21(8):2237-52 [PMID: 19671879]
  16. Trends Plant Sci. 2008 Mar;13(3):137-44 [PMID: 18314376]
  17. Plant Cell. 2011 Feb;23(2):701-15 [PMID: 21335373]
  18. Plant Cell Physiol. 2012 Feb;53(2):330-43 [PMID: 22173100]
  19. Plant J. 1998 Dec;16(6):735-43 [PMID: 10069079]
  20. Proc Natl Acad Sci U S A. 2013 Jan 8;110(2):761-6 [PMID: 23267111]
  21. Proc Natl Acad Sci U S A. 2017 Feb 14;114(7):1720-1725 [PMID: 28137867]
  22. Crit Rev Biochem Mol Biol. 2013 Nov-Dec;48(6):575-608 [PMID: 24088064]
  23. Science. 1998 May 15;280(5366):1091-4 [PMID: 9582125]
  24. Nature. 2010 Apr 1;464(7289):788-91 [PMID: 20360743]
  25. Mol Plant. 2013 May;6(3):686-703 [PMID: 23142764]
  26. Proc Natl Acad Sci U S A. 2000 Nov 7;97(23):12902-7 [PMID: 11058164]
  27. Mol Cell. 2007 Jun 8;26(5):717-29 [PMID: 17560376]
  28. OMICS. 2012 May;16(5):284-7 [PMID: 22455463]
  29. Sci Adv. 2015 Jul 24;1(6):e1500107 [PMID: 26601214]
  30. Plant Physiol. 2011 May;156(1):46-60 [PMID: 21402796]
  31. Development. 1995 Apr;121(4):975-91 [PMID: 7743940]
  32. Nature. 2007 Aug 9;448(7154):661-5 [PMID: 17637677]
  33. Plant Physiol. 2012 Jan;158(1):423-38 [PMID: 22065421]
  34. Mol Cell Biol. 2007 Aug;27(15):5306-15 [PMID: 17526732]
  35. Nat Protoc. 2007;2(7):1565-72 [PMID: 17585298]
  36. Plant Cell. 2009 Oct;21(10):3105-18 [PMID: 19837869]
  37. Plant Methods. 2005 Dec 18;1:13 [PMID: 16359558]
  38. Science. 2011 Mar 18;331(6023):1451-4 [PMID: 21415355]
  39. Dev Cell. 2015 Jun 8;33(5):576-88 [PMID: 26028217]
  40. Plant Cell. 2011 Sep;23(9):3335-52 [PMID: 21954460]
  41. Proc Natl Acad Sci U S A. 2017 Oct 17;114(42):E8930-E8939 [PMID: 28973940]
  42. Plant Cell. 2009 Aug;21(8):2220-36 [PMID: 19717617]
  43. Plant Cell. 2004 Jan;16(1):126-43 [PMID: 14688297]
  44. Plant Cell. 2015 Aug;27(8):2301-13 [PMID: 26276832]
  45. Plant Mol Biol. 1995 Mar;27(5):933-42 [PMID: 7766883]
  46. Plant Cell. 1996 Dec;8(12):2309-23 [PMID: 8989885]
  47. Plant Cell. 2004 Jul;16(7):1938-50 [PMID: 15208388]
  48. Proc Natl Acad Sci U S A. 2007 Aug 7;104(32):12955-61 [PMID: 17670940]
  49. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8675-9 [PMID: 7567995]
  50. Biochim Biophys Acta. 2013 Jul;1830(7):3867-75 [PMID: 22402254]
  51. Plant Cell. 2017 Aug;29(8):1883-1906 [PMID: 28733419]
  52. Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11494-9 [PMID: 15277686]
  53. Nucleic Acids Res. 2019 Jan 8;47(D1):D8-D14 [PMID: 30365034]
  54. Genomics Proteomics Bioinformatics. 2017 Feb;15(1):14-18 [PMID: 28387199]
  55. Plant Cell Physiol. 2017 Oct 1;58(10):1752-1763 [PMID: 29017003]
  56. Nat Rev Genet. 2010 Nov;11(11):761-72 [PMID: 20940737]
  57. Plant Physiol. 2011 Jun;156(2):491-502 [PMID: 21518777]
  58. Plant Physiol. 1995 May;108(1):47-57 [PMID: 12228453]
  59. Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12990-5 [PMID: 16123135]
  60. Proc Natl Acad Sci U S A. 2011 Jul 26;108(30):12539-44 [PMID: 21737749]
  61. Development. 2011 Jun;138(12):2451-6 [PMID: 21610026]
  62. Mol Cell. 2013 May 23;50(4):504-15 [PMID: 23706819]
  63. Plant Cell. 2011 May;23(5):1795-814 [PMID: 21551388]
  64. Nat Commun. 2014 Jun 18;5:4140 [PMID: 24938363]
  65. Nature. 2015 Sep 10;525(7568):269-73 [PMID: 26258305]
  66. Plant Cell. 2002 Aug;14(8):1919-35 [PMID: 12172031]
  67. Plant Signal Behav. 2018;13(5):e1403709 [PMID: 29125388]
  68. Plant Signal Behav. 2012 Jan;7(1):86-92 [PMID: 22301974]
  69. Plant Cell. 2012 Jul;24(7):2898-916 [PMID: 22822206]
  70. J Biosci Bioeng. 2007 Jul;104(1):34-41 [PMID: 17697981]
  71. Nature. 2007 Aug 9;448(7154):666-71 [PMID: 17637675]
  72. Development. 2012 Nov;139(22):4180-90 [PMID: 23034631]
  73. Annu Rev Plant Biol. 2008;59:41-66 [PMID: 18031220]
  74. Nat Rev Mol Cell Biol. 2015 Mar;16(3):155-66 [PMID: 25693131]
  75. Science. 2006 Jun 9;312(5779):1520-3 [PMID: 16763149]
  76. Plant Physiol. 2008 Jun;147(2):672-81 [PMID: 18390806]
  77. Science. 2008 Mar 7;319(5868):1384-6 [PMID: 18258861]
  78. Gene. 2000 May 16;249(1-2):1-16 [PMID: 10831834]
  79. Development. 2014 Mar;141(5):977-87 [PMID: 24550107]
  80. Nat Chem Biol. 2009 May;5(5):344-50 [PMID: 19349968]
  81. Annu Rev Plant Biol. 2009;60:183-205 [PMID: 19025383]
  82. Genes Dev. 2004 Jul 1;18(13):1577-91 [PMID: 15231736]
  83. Plant Physiol. 2010 Nov;154(3):1403-14 [PMID: 20810545]
  84. Nature. 2013 Dec 19;504(7480):401-5 [PMID: 24336200]
  85. Plant Physiol. 2012 Sep;160(1):541-55 [PMID: 22822211]
  86. Plant Cell. 2013 Feb;25(2):421-37 [PMID: 23444332]

MeSH Term

Acetylation
Arabidopsis
Arabidopsis Proteins
Arsenate Reductases
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
DNA-Binding Proteins
Gene Expression Regulation, Plant
Histones
Lipoxygenases
Plants, Genetically Modified
Promoter Regions, Genetic
Repressor Proteins
Signal Transduction
Transcription Factors
Transcription, Genetic
Transcriptional Activation

Chemicals

Arabidopsis Proteins
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
DNA-Binding Proteins
Histones
JAZ2 protein, Arabidopsis
LUH protein, Arabidopsis
MYC2 protein, Arabidopsis
PFT1 protein, Arabidopsis
Repressor Proteins
Transcription Factors
Lipoxygenases
lipoxygenase 2, Arabidopsis
Arsenate Reductases
HAC1 protein, Arabidopsis