C2H2 zinc finger-SET histone methyltransferase is a plant-specific chromatin modifier

Abstract

Histone modification represents a universal mechanism for regulation of eukaryotic gene expression underlying diverse biological processes from neuronal gene expression in mammals to control of flowering in plants. In animal cells, these chromatin modifications are effected by well-defined multiprotein complexes containing specific histone-modifying activities. In plants, information about the composition of such co-repressor complexes is just beginning to emerge. Here, we report that two Arabidopsis thaliana factors, a SWIRM domain polyamine oxidase protein, AtSWP1, and a plant-specific C2H2 zinc finger-SET domain protein, AtCZS, interact with each other in plant cells and repress expression of a negative regulator of flowering, FLOWERING LOCUS C (FLC) via an autonomous, vernalization-independent pathway. Loss-of-function of either AtSWP1 or AtCZS results in reduced dimethylation of lysine 9 and lysine 27 of histone H3 and hyperacetylation of histone H4 within the FLC locus, in elevated FLC mRNA levels, and in moderately delayed flowering. Thus, AtSWP1 and AtCZS represent two main components of a co-repressor complex that fine tunes flowering and is unique to plants.

Arabidopsis Co-Repressor Complexes Containing Polyamine Oxidase-Like Proteins and Plant-Specific Histone Methyltransferases

“…To date, we have documented one AtSWP1/AtCZS target gene, the FLC negative regulator of flowering, and the corresponding flower timing delay phenotypes of the Arabidopsis null mutants in AtSWP1 and AtCZS. 6 However, these mutants exhibited other, unrelated to FLC, phenotypic changes, such as altered root length, indicating existence of additional target genes of the AtSWP1/AtCZS complex (Fig. 1).…”

“…2) and are required for generation of the H3K9 and H3K27 methylation marks on heterochromatin. 6 AtCZS contains SET domain diagnostic of HMTs; 35 thus, it presumably represents the actual enzyme that methylates H3K9 and H3K27 whereas the effect of AtSWP1 on these histone methylation marks is indirect, most likely through recruiting AtCZS. Because genetic inactivation of AtSWP1 and/or AtCZS alters not only histone methylation, but also acetylation, 6 the AtSWP1/AtCZS corepressor complex most likely also contains as yet unidentified HDACs (Fig.…”

“…Although conserved between evolutionarily-distant plant species such as monocots and dicots, 6 it is found only in plants. 35 In mammalian PAO-containing complexes, 36 the AtCZS functionality is most closely represented by one of their zinc finger proteins, REST 11,37 or ZNF217, 12 and the PreSET-SET-PostSET HMT G9a protein that Arabidopsis Co-Repressor Complexes methylates H3K9 and/or H3K27.…”

“…While both animal LSD1 and plant AtSWP1 exhibit a common conserved domain structure, i.e., N-proximal SWIRM domain and C-proximal PAO-like domain, 6,16 only LSD1 possesses a detectable demethylase activity when tested in vitro using the purified recombinant proteins. 6,16 A worKinG model of tHe AtSwP1/AtCzS CorePreSSor ComPlex Our working model of the AtSWP1/AtCZS corepressor is based on the notion that it may combine both general and plant-specific activities and components. For example, the presence of a PAO-like protein, SET-domain HMT, zinc finger proteins, and HDACs would represent a general feature, plant and animal.…”

“…Joining these research efforts, we have identified a novel type of transcriptional repressor complex which may act as one of the global regulators of plant gene expression and which combines both general, i.e., conserved between plants and animals, and plant-specific corepressor activities and components. 6 mAmmAliAn PolyAmine oxidASe (PAo)/lySine demetHylASe 1 (lSd1)-ContAininG CorePreSSor ComPlex…”