The WD40 Domain Protein MSI1 Functions in a Histone Deacetylase Complex to Fine-Tune Abscisic Acid Signaling

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2015 Dec 26

PMID 26704384

Citations 69

Authors

Saher Mehdi

Maria Derkacheva

Margareta Ramstrom

Lejon Kralemann

Jonas Bergquist

Lars Hennig

Affiliations

Soon will be listed here.

Abstract

MSI1 belongs to a family of histone binding WD40-repeat proteins. Arabidopsis thaliana contains five genes encoding MSI1-like proteins, but their functions in diverse chromatin-associated complexes are poorly understood. Here, we show that MSI1 is part of a histone deacetylase complex. We copurified HISTONE DEACETYLASE19 (HDA19) with MSI1 and transcriptional regulatory SIN3-like proteins and provide evidence that MSI1 and HDA19 associate into the same complex in vivo. These data suggest that MSI1, HDA19, and HISTONE DEACETYLATION COMPLEX1 protein form a core complex that can integrate various SIN3-like proteins. We found that reduction of MSI1 or HDA19 causes upregulation of abscisic acid (ABA) receptor genes and hypersensitivity of ABA-responsive genes. The MSI1-HDA19 complex fine-tunes ABA signaling by binding to the chromatin of ABA receptor genes and by maintaining low levels of acetylation of histone H3 at lysine 9, thereby affecting the expression levels of ABA receptor genes. Reduced MSI1 or HDA19 levels led to increased tolerance to salt stress corresponding to the increased ABA sensitivity of gene expression. Together, our results reveal the presence of an MSI1-HDA19 complex that fine-tunes ABA signaling in Arabidopsis.

Citing Articles

Epigenetic regulation of lignin biosynthesis in wood formation.

Ma H, Su L, Zhang W, Sun Y, Li D, Li S New Phytol. 2024; 245(4):1589-1607.

PMID: 39639540 PMC: 11754936. DOI: 10.1111/nph.20328.

Nucleo-cytoplasmic distribution of SAP18 reveals its dual function in splicing regulation and heat-stress response in Arabidopsis.

Larran A, Ge J, Martin G, Carlos De La Concepcion J, Dagdas Y, Questa J Plant Commun. 2024; 6(1):101180.

PMID: 39482883 PMC: 11784288. DOI: 10.1016/j.xplc.2024.101180.

Investigating the Role of OsHDT701 and Other Blast-Associated Negative Regulatory Genes in Indica Rice Cultivar Ranjit Using Combined Wet Lab and Computational Approaches.

Sarki Y, Singh H, Keot A, Marwein R, Singha D, Dehury B Mol Biotechnol. 2024; .

PMID: 39476286 DOI: 10.1007/s12033-024-01310-7.

Transcriptome-wide Identification of Nine Tandem Repeat Protein Families in Roselle ( L.).

Yong C, Atheeqah-Hamzah N Trop Life Sci Res. 2024; 35(3):121-148.

PMID: 39464663 PMC: 11507979. DOI: 10.21315/tlsr2024.35.3.6.

Epigenetics Regulation in Responses to Abiotic Factors in Plant Species: A Systematic Review.

da Costa G, Cerqueira A, de Brito C, Mielke M, Gaiotto F Plants (Basel). 2024; 13(15).

PMID: 39124200 PMC: 11314046. DOI: 10.3390/plants13152082.

References

Grzenda A, Lomberk G, Zhang J, Urrutia R . Sin3: master scaffold and transcriptional corepressor. Biochim Biophys Acta. 2009; 1789(6-8):443-50. PMC: 3686104. DOI: 10.1016/j.bbagrm.2009.05.007. View

Park S, Fung P, Nishimura N, Jensen D, Fujii H, Zhao Y . Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science. 2009; 324(5930):1068-71. PMC: 2827199. DOI: 10.1126/science.1173041. View

Moran R, Porath D . Chlorophyll determination in intact tissues using n,n-dimethylformamide. Plant Physiol. 1980; 65(3):478-9. PMC: 440358. DOI: 10.1104/pp.65.3.478. View

Keogh M, Kurdistani S, Morris S, Ahn S, Podolny V, Collins S . Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell. 2005; 123(4):593-605. DOI: 10.1016/j.cell.2005.10.025. View

Tian L, Wang J, Fong M, Chen M, Cao H, Gelvin S . Genetic control of developmental changes induced by disruption of Arabidopsis histone deacetylase 1 (AtHD1) expression. Genetics. 2003; 165(1):399-409. PMC: 1462737. DOI: 10.1093/genetics/165.1.399. View

Carrozza M, Li B, Florens L, Suganuma T, Swanson S, Lee K . Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell. 2005; 123(4):581-92. DOI: 10.1016/j.cell.2005.10.023. View

Chen L, Luo M, Wang Y, Wu K . Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot. 2010; 61(12):3345-53. PMC: 2905197. DOI: 10.1093/jxb/erq154. View

Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T . ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol. 2005; 140(1):115-26. PMC: 1326036. DOI: 10.1104/pp.105.070128. View

van der Vlag J, Otte A . Transcriptional repression mediated by the human polycomb-group protein EED involves histone deacetylation. Nat Genet. 1999; 23(4):474-8. DOI: 10.1038/70602. View

10.

Tie F, Furuyama T, Jane E, Harte P . The Drosophila Polycomb Group proteins ESC and E(Z) are present in a complex containing the histone-binding protein p55 and the histone deacetylase RPD3. Development. 2000; 128(2):275-86. DOI: 10.1242/dev.128.2.275. View

11.

Exner V, Gruissem W, Hennig L . Control of trichome branching by chromatin assembly factor-1. BMC Plant Biol. 2008; 8:54. PMC: 2413220. DOI: 10.1186/1471-2229-8-54. View

12.

Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T . 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. 2005; 44(6):939-49. DOI: 10.1111/j.1365-313X.2005.02583.x. View

13.

Simon P . Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics. 2003; 19(11):1439-40. DOI: 10.1093/bioinformatics/btg157. View

14.

Kaya H, Shibahara K, Taoka K, Iwabuchi M, Stillman B, Araki T . FASCIATA genes for chromatin assembly factor-1 in arabidopsis maintain the cellular organization of apical meristems. Cell. 2001; 104(1):131-42. DOI: 10.1016/s0092-8674(01)00197-0. View

15.

Luo M, Tai R, Yu C, Yang S, Chen C, Lin W . Regulation of flowering time by the histone deacetylase HDA5 in Arabidopsis. Plant J. 2015; 82(6):925-936. DOI: 10.1111/tpj.12868. View

16.

Kenzior A, Folk W . AtMSI4 and RbAp48 WD-40 repeat proteins bind metal ions. FEBS Lett. 1999; 440(3):425-9. DOI: 10.1016/s0014-5793(98)01500-2. View

17.

Hennig L, Bouveret R, Gruissem W . MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol. 2005; 15(6):295-302. DOI: 10.1016/j.tcb.2005.04.004. View

18.

Kohler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W . Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J. 2003; 22(18):4804-14. PMC: 212713. DOI: 10.1093/emboj/cdg444. View

19.

Ausin I, Alonso-Blanco C, Jarillo J, Ruiz-Garcia L, Martinez-Zapater J . Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet. 2004; 36(2):162-6. DOI: 10.1038/ng1295. View

20.

Shevchenko A, Wilm M, Vorm O, Mann M . Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem. 1996; 68(5):850-8. DOI: 10.1021/ac950914h. View