JUMONJI Family from Maize



Required domains for JUMONJI family:PF02373PF02375






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Jumonji (JMJ) family of proteins are named after the cruciform morphology (resembling cross) of normal and abnormal neural grooves on the neural plates of jmj mutant mice, which were identified by mouse gene trap method. Members of this family are recognized by presence of two conserved domains jmjN and jmjC and AT rich DNA binding domain ARID. ARID domains play a role in DNA binding, chromatin binding or regulation at transcription level (Takeuchi et al., 1995). Only the jmjC domain or both jmjC and jmjN domains are present in more than 100 proteins belonging to bacteria, fungi, animals and plants (Balciunas and Roone., 2000). JMJ was initially identified to play a role in normal cardiogenesis by acting as a transcriptional repressor of cyclin D1 in the embryonic heart (Toyoda et al., 2003). JMJ proteins containing jmjC domain belong to the JHDMs (jmjC domain containing histone demethylases) class of histone demethylases that reversibly removes methyl group from histones reaction through an oxidative reaction requiring Fe and a-ketoglutarate as cofactors. Arabidopsis consist of 21 jmjC domain containing proteins subdivide into five groups namely: JARID1/ KDM5, JHDM3/KDM4, JDHM2/KDM3, JHDM6 and group containing just jmjC domain (Shi et al., 2004). Maize consists of 19 ZmJMJs encoding genes distributed unevenly across 9 of the all 10 maize chromosomes, and divided into three subfamilies: JARID1/ KDM5, JHDM3/KDM4 and JHDM2/KDM3 based on amino acid sequence similarity. Based on quantitative real time PCR results, all 19 ZmJMJs showed differential expression  responsive to heat stress treatment or normal condition (Qian et al., 2019).

AtJMJ14 plays role in RNA silencing, EFL6 (early flowering 6) and its homolog REF6 (relative of early flowering 6) belonging to jmjN/C domain containing proteins play a role in brassinosteroid responses, whereas other members are involved in female gametophyte development and cytosine methylation and (Pagnussat et al., 2005, Saze et al., 2008, Yu et al., 2008, Searle et al., 2010, Deleris et al., 2010) . AtJMJ30 regulates the pace of the circadian clock in Arabidopsis, since based on ChIP assay and confirmed by JMJ30 loss and gain of function mutant, morning phased clock component transcription factors CCA1 and LHY directly regulates AtJMJ30 expression repressing its activity (Lu et al., 2011). In response to heat, AtJMJ30 histone demethylase is recruited to HSP21 (Heat Shock protein 21) locus and mediates the balance between H3K27me3 and H3K4me3 by increasing levels of H3Kme3 and by removal of H3K27me3  (Yamaguchi et al., 2021).AtJMJ24 possessing ubiquitin E3 ligase activity destabilizes heterochromatic  state of silenced region by directing CHG methylation specific DNA methyltransferase CHROMOMETHYLASE 3 (CMT3) for proteasome degradation. Thus AtJMJ24 plays a role in linking histone modification and DNA methylation (Deng et al., 2016). Based on loss of function and overexpression studies,  AtJMJ24 negatively regulates silencing of transposable element (TE) AtMu1c by binding to histone H3 in vivo without demethylase activity and AtJMJ24 activity is anti correlated with H3K9me2 levels at AtMu1c (Kabelitz et al., 2016). AtJMJ27, a JHDM2 (jmjC domain-containing histone demethylase 2) protein play role in both defense and developmental processes in Arabidopsis. It exhibits H3K9me1/2 demethylase activity and is a positive regulator of pathogenesis related gene (PR), induced in response to virulent Pseudomonas syringae and Flowering Locus (FLC) and a negative regulator of defense repressor gene WRKY25 and flowering regulator CONSTANS (CO)  (Dutta et al., 2017). Also, AtJMJ14 is a positive modulator of defense genes involved in salicylic acid and pipecolic acid pathways through pathogen induced H3K4me3 enrichment (Li et al., 2019). Arabidopsis telomeric repeat binding factors (TRBs) recruit Polycomb Repressive Complex2 (PRC2) and AtJMJ14, a histone demethylase in order to repress target gene expression by H3K27me3 enrichment and H3K4me3 removal (Wang et al., 2023). Based on jmj13 mutant studies, AtJMJ13 acts as a flowering repressor in Arabidopsis in both temperature and day light dependent manner (Zheng et al., 2019). Arabidopsis AtJMJ15 plays a role in salt stress response since loss of function mutant increased salt stress sensitivity and knockout mutant affected salt stress responsive gene expression by changing H3K4me3 levels. AtJMJ15 represses WRKY46 and WRKY70, negative regulators of abiotic stress by demethylating H3K4me3 mark in promoter and coding region (Shen et al., 2022).

 Last updated June 2023 by Ankita Abnave

References:

Takeuchi T, Yamazaki Y, Katoh-Fukui Y, Tsuchiya R, Kondo S, Motoyama J, Higashinakagawa T. Gene trap capture of a novel mouse gene, jumonji, required for neural tube formation. Genes Dev. 1995 May 15;9(10):1211-22. doi: 10.1101/gad.9.10.1211. PMID: 7758946.

Balciunas D, Ronne H. Evidence of domain swapping within the jumonji family of transcription factors. Trends Biochem Sci. 2000 Jun;25(6):274-6. doi: 10.1016/s0968-0004(00)01593-0. PMID: 10838566.

Toyoda M, Kojima M, Takeuchi T. Jumonji is a nuclear protein that participates in the negative regulation of cell growth. Biochem Biophys Res Commun. 2000 Aug 2;274(2):332-6. doi: 10.1006/bbrc.2000.3138. PMID: 10913339.

Lu SX, Knowles SM, Webb CJ, Celaya RB, Cha C, Siu JP, Tobin EM. The Jumonji C domain-containing protein JMJ30 regulates period length in the Arabidopsis circadian clock. Plant Physiol. 2011 Feb;155(2):906-15. doi: 10.1104/pp.110.167015. Epub 2010 Dec 7. PMID: 21139085; PMCID: PMC3032475.

Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V. Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development. 2005 Feb;132(3):603-14. doi: 10.1242/dev.01595. Epub 2005 Jan 5. Erratum in: Development. 2005 Mar;132(5):1161. PMID: 15634699.

Saze H, Shiraishi A, Miura A, Kakutani T. Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science. 2008 Jan 25;319(5862):462-5. doi: 10.1126/science.1150987. PMID: 18218897.

Yu X, Li L, Li L, Guo M, Chory J, Yin Y. Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci U S A. 2008 May 27;105(21):7618-23. doi: 10.1073/pnas.0802254105. Epub 2008 May 8. PMID: 18467490; PMCID: PMC2396691.

Searle IR, Pontes O, Melnyk CW, Smith LM, Baulcombe DC. JMJ14, a JmjC domain protein, is required for RNA silencing and cell-to-cell movement of an RNA silencing signal in Arabidopsis. Genes Dev. 2010 May 15;24(10):986-91. doi: 10.1101/gad.579910. PMID: 20478993; PMCID: PMC2867213.

Deleris A, Greenberg MV, Ausin I, Law RW, Moissiard G, Schubert D, Jacobsen SE. Involvement of a Jumonji-C domain-containing histone demethylase in DRM2-mediated maintenance of DNA methylation. EMBO Rep. 2010 Dec;11(12):950-5. doi: 10.1038/embor.2010.158. Epub 2010 Nov 5. PMID: 21052090; PMCID: PMC2999860.

Deng S, Jang IC, Su L, Xu J, Chua NH. JMJ24 targets CHROMOMETHYLASE3 for proteasomal degradation in Arabidopsis. Genes Dev. 2016 Feb 1;30(3):251-6. doi: 10.1101/gad.274647.115. Epub 2016 Jan 21. PMID: 26798133; PMCID: PMC4743055.

Kabelitz T, Brzezinka K, Friedrich T, Górka M, Graf A, Kappel C, Bäurle I. A JUMONJI Protein with E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis. Plant Physiol. 2016 May;171(1):344-58. doi: 10.1104/pp.15.01688. Epub 2016 Mar 15. PMID: 26979329; PMCID: PMC4854677.

Dutta A, Choudhary P, Caruana J, Raina R. JMJ27, an Arabidopsis H3K9 histone demethylase, modulates defense against Pseudomonas syringae and flowering time. Plant J. 2017 Sep;91(6):1015-1028. doi: 10.1111/tpj.13623. Epub 2017 Aug 7. PMID: 28650521

Zheng S, Hu H, Ren H, Yang Z, Qiu Q, Qi W, Liu X, Chen X, Cui X, Li S, Zhou B, Sun D, Cao X, Du J. The Arabidopsis H3K27me3 demethylase JUMONJI 13 is a temperature and photoperiod dependent flowering repressor. Nat Commun. 2019 Mar 21;10(1):1303. doi: 10.1038/s41467-019-09310-x. PMID: 30899015; PMCID: PMC6428840.

Li D, Liu R, Singh D, Yuan X, Kachroo P, Raina R. JMJ14 encoded H3K4 demethylase modulates immune responses by regulating defence gene expression and pipecolic acid levels. New Phytol. 2020 Mar;225(5):2108-2121. doi: 10.1111/nph.16270. Epub 2019 Nov 11. PMID: 31622519

Wang M, Zhong Z, Gallego-Bartolomé J, Feng S, Shih YH, Liu M, Zhou J, Richey JC, Ng C, Jami-Alahmadi Y, Wohlschlegel J, Wu K, Jacobsen SE. Arabidopsis TRB proteins function in H3K4me3 demethylation by recruiting JMJ14. Nat Commun. 2023 Mar 28;14(1):1736. doi: 10.1038/s41467-023-37263-9. PMID: 36977663; PMCID: PMC10049986.

Shen Y, Chi Y, Lu S, Lu H, Shi L. Involvement of JMJ15 in the dynamic change of genome-wide H3K4me3 in response to salt stress. Front Plant Sci. 2022 Sep 26;13:1009723. doi: 10.3389/fpls.2022.1009723. PMID: 36226276; PMCID: PMC9549339.

Yamaguchi N, Ito T. JMJ Histone Demethylases Balance H3K27me3 and H3K4me3 Levels at the HSP21 Locus during Heat Acclimation in Arabidopsis. Biomolecules. 2021 Jun 7;11(6):852. doi: 10.3390/biom11060852. PMID: 34200465; PMCID: PMC8227549.

Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 2004 Dec 29;119(7):941-53. doi: 10.1016/j.cell.2004.12.012. PMID: 15620353.

Qian Y, Chen C, Jiang L, Zhang J, Ren Q. Genome-wide identification, classification and expression analysis of the JmjC domain-containing histone demethylase gene family in maize. BMC Genomics. 2019 Apr 1;20(1):256. doi: 10.1186/s12864-019-5633-1. PMID: 30935385; PMCID: PMC6444447

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