Dual Function of MIPS1 As a Metabolic Enzyme and Transcriptional Regulator

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2013 Jan 24

PMID 23341037

Citations 21

Authors

David Latrasse

Teddy Jegu

Pin-Hong Meng

Christelle Mazubert

Elodie Hudik

Marianne Delarue

Celine Charon

Martin Crespi

Heribert Hirt

Cecile Raynaud

Catherine Bergounioux

Moussa Benhamed

Affiliations

Soon will be listed here.

Abstract

Because regulation of its activity is instrumental either to support cell proliferation and growth or to promote cell death, the universal myo-inositol phosphate synthase (MIPS), responsible for myo-inositol biosynthesis, is a critical enzyme of primary metabolism. Surprisingly, we found this enzyme to be imported in the nucleus and to interact with the histone methyltransferases ATXR5 and ATXR6, raising the question of whether MIPS1 has a function in transcriptional regulation. Here, we demonstrate that MIPS1 binds directly to its promoter to stimulate its own expression by locally inhibiting the spreading of ATXR5/6-dependent heterochromatin marks coming from a transposable element. Furthermore, on activation of pathogen response, MIPS1 expression is reduced epigenetically, providing evidence for a complex regulatory mechanism acting at the transcriptional level. Thus, in plants, MIPS1 appears to have evolved as a protein that connects cellular metabolism, pathogen response and chromatin remodeling.

Citing Articles

Genome-wide identification, characterization, and expression analysis of MIPS family genes in legume species.

Jacob F, Hamid R, Ghorbanzadeh Z, Valsalan R, Ajinath L, Mathew D BMC Genomics. 2024; 25(1):95.

PMID: 38262915 PMC: 10804463. DOI: 10.1186/s12864-023-09937-7.

A novel transcription factor SIPA1: identification and verification in triple-negative breast cancer.

Guo L, Zhang W, Zhang X, Wang J, Nie J, Jin X Oncogene. 2023; 42(35):2641-2654.

PMID: 37500797 PMC: 10457189. DOI: 10.1038/s41388-023-02787-3.

Myo-inositol phosphate synthase improves heat stress tolerance by ethylene-mediated modulation of chlorophyll content and photosynthetic efficiency.

Sharma N, Shree B, Khurana P Protoplasma. 2023; 260(4):1097-1107.

PMID: 36602620 DOI: 10.1007/s00709-022-01835-1.

Co-culturing experiments reveal the uptake of myo-inositol phosphate synthase (EC 5.5.1.4) in an inositol auxotroph of Saccharomyces cerevisiae.

Steele E, Alebous H, Vickers M, Harris M, Johnson M Microb Cell Fact. 2021; 20(1):138.

PMID: 34281557 PMC: 8287684. DOI: 10.1186/s12934-021-01610-6.

The noncanonical role of the protease cathepsin D as a cofilin phosphatase.

Liu Y, Zhang T, Chen S, Cheng D, Wu C, Wang X Cell Res. 2021; 31(7):801-813.

PMID: 33514914 PMC: 8249557. DOI: 10.1038/s41422-020-00454-w.

References

Tian L, Fong M, Wang J, Wei N, Jiang H, Doerge R . Reversible histone acetylation and deacetylation mediate genome-wide, promoter-dependent and locus-specific changes in gene expression during plant development. Genetics. 2004; 169(1):337-45. PMC: 1448893. DOI: 10.1534/genetics.104.033142. View

Blazquez M . Quantitative GUS Activity Assay in Intact Plant Tissue. CSH Protoc. 2011; 2007:pdb.prot4688. DOI: 10.1101/pdb.prot4688. View

Daxinger L, Hunter B, Sheikh M, Jauvion V, Gasciolli V, Vaucheret H . Unexpected silencing effects from T-DNA tags in Arabidopsis. Trends Plant Sci. 2008; 13(1):4-6. DOI: 10.1016/j.tplants.2007.10.007. View

Wang C, Gao F, Wu J, Dai J, Wei C, Li Y . Arabidopsis putative deacetylase AtSRT2 regulates basal defense by suppressing PAD4, EDS5 and SID2 expression. Plant Cell Physiol. 2010; 51(8):1291-9. PMC: 2920754. DOI: 10.1093/pcp/pcq087. View

Hall D, Zhu H, Zhu X, Royce T, Gerstein M, Snyder M . Regulation of gene expression by a metabolic enzyme. Science. 2004; 306(5695):482-4. DOI: 10.1126/science.1096773. View

Marion J, Bach L, Bellec Y, Meyer C, Gissot L, Faure J . Systematic analysis of protein subcellular localization and interaction using high-throughput transient transformation of Arabidopsis seedlings. Plant J. 2008; 56(1):169-79. DOI: 10.1111/j.1365-313X.2008.03596.x. View

Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B . Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell. 2001; 103(7):1111-20. DOI: 10.1016/s0092-8674(00)00213-0. View

Roudier F, Ahmed I, Berard C, Sarazin A, Mary-Huard T, Cortijo S . Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 2011; 30(10):1928-38. PMC: 3098477. DOI: 10.1038/emboj.2011.103. View

Arnaud P, Goubely C, Pelissier T, Deragon J . SINE retroposons can be used in vivo as nucleation centers for de novo methylation. Mol Cell Biol. 2000; 20(10):3434-41. PMC: 85636. DOI: 10.1128/MCB.20.10.3434-3441.2000. View

10.

Berr A, Menard R, Heitz T, Shen W . Chromatin modification and remodelling: a regulatory landscape for the control of Arabidopsis defence responses upon pathogen attack. Cell Microbiol. 2012; 14(6):829-39. DOI: 10.1111/j.1462-5822.2012.01785.x. View

11.

Jacob Y, Stroud H, LeBlanc C, Feng S, Zhuo L, Caro E . Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature. 2010; 466(7309):987-91. PMC: 2964344. DOI: 10.1038/nature09290. View

12.

Fukuda H . Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol Biol. 2001; 44(3):245-53. DOI: 10.1023/a:1026532223173. View

13.

Shen X, Xiao H, Ranallo R, Wu W, Wu C . Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science. 2002; 299(5603):112-4. DOI: 10.1126/science.1078068. View

14.

Meng P, Raynaud C, Tcherkez G, Blanchet S, Massoud K, Domenichini S . Crosstalks between myo-inositol metabolism, programmed cell death and basal immunity in Arabidopsis. PLoS One. 2009; 4(10):e7364. PMC: 2754662. DOI: 10.1371/journal.pone.0007364. View

15.

Lam E . Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol. 2004; 5(4):305-15. DOI: 10.1038/nrm1358. View

16.

Moore J, Loake G, Spoel S . Transcription dynamics in plant immunity. Plant Cell. 2011; 23(8):2809-20. PMC: 3180793. DOI: 10.1105/tpc.111.087346. View

17.

Gendrel A, Lippman Z, Martienssen R, Colot V . Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods. 2005; 2(3):213-8. DOI: 10.1038/nmeth0305-213. View

18.

Scott E, Pillus L . Homocitrate synthase connects amino acid metabolism to chromatin functions through Esa1 and DNA damage. Genes Dev. 2010; 24(17):1903-13. PMC: 2932972. DOI: 10.1101/gad.1935910. View

19.

Jacob Y, Feng S, LeBlanc C, Bernatavichute Y, Stroud H, Cokus S . ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat Struct Mol Biol. 2009; 16(7):763-8. PMC: 2754316. DOI: 10.1038/nsmb.1611. View

20.

Wu H, Cheun A . Programmed cell death in plant reproduction. Plant Mol Biol. 2001; 44(3):267-81. DOI: 10.1023/a:1026536324081. View