Maize rough sheath2 and ItsArabidopsisOrthologue ASYMMETRIC LEAVES1 Interact with HIRA, a Predicted Histone Chaperone, to MaintainknoxGene Silencing and Determinacy during Organogenesis

Abstract

Plant shoots are characterized by indeterminate growth resulting from the action of a population of stem cells in the shoot apical meristem (SAM). Indeterminacy within the SAM is specified in part by the class I knox homeobox genes. The myb domain proteins rough sheath2 (RS2) and ASYMMETRIC LEAVES1 (AS1) from maize (Zea mays) and Arabidopsis thaliana, respectively, are required to establish determinacy during leaf development. These proteins are part of a cellular memory system that in response to a stem cell-derived signal keeps knox genes in an off state during organogenesis. Here, we show that RS2/AS1 can form conserved protein complexes through interaction with the DNA binding factor ASYMMETRIC LEAVES2, a predicted RNA binding protein (RIK, for RS2-Interacting KH protein), and a homologue of the chromatinremodeling protein HIRA. Partial loss of HIRA function in Arabidopsis results in developmental defects comparable to those of as1 and causes reactivation of knox genes in developing leaves, demonstrating a direct role for HIRA in knox gene repression and the establishment of determinacy during leaf formation. Our data suggest that RS2/AS1 and HIRA mediate the epigenetic silencing of knox genes, possibly by modulating chromatin structure. Components of this process are conserved in animals, suggesting the possibility that a similar epigenetic mechanism maintains determinacy during both plant and animal development.

Remodeling of chromatin structure in senescent cells and its potential impact on tumor suppression and aging

“…However, the apparent inconsistency in this idea is merely an extension of an existing paradox. Specifically, HIRA and its orthologs in other species are typically involved in gene silencing and formation of heterochromatin (13,50,64,67,97,116,117,119,123), whereas HIRA's favored deposition substrate, histone H3.3, is linked to transcriptional activation (3,77,80,112,133). However, to our knowledge, histone H3.3 per se has not been shown to directly cause or contribute to transcription activation, and a proportion of histone H3.3 does carry posttranslational marks characteristic of transcriptionally silent chromatin (55,74,77).…”

“…For example, pRB recruits the histone methylase Suv39h1 to chromatin and, as described above, this enzyme is required for oncogene-induced formation of heterochromatin in murine T-cells (16). HIRA and ASF1a are two histone chaperones whose physical interaction is required to form transcriptionally silent heterochromatin from yeast to humans (13,50,64,67,97,116,145). One simple model to describe the cooperation of the pRB and HIRA/ASF1a pathways is that pRB initiates heterochromatin formation at the promoters of E2F target genes, and this heterochromatin acts as a nucleation site for HIRA/ASF1a-mediated large scale chromosome condensation.…”

“…Two chromatin regulators, HIRA and ASF1a, drive chromosome condensation during SAHF assembly in human cells (145). HIRA and ASF1a are the human orthologs of proteins known to create transcriptionally silent heterochromatin in yeast, flies and plants (64,83,97,117,121). Yeast Asf1p is required for heterochromatin-mediated silencing of telomeres and mating loci and has histone deposition activity in vitro (67,116,121,127).…”

Aging by epigenetics—A consequence of chromatin damage?

“…Significantly, at least one of these, the histone chaperone HIRA, has been shown to increase in expression or undergo some level of regulation in aging baboon skin [40,41]. Although the HIRA histone chaperone may have some functions linked to transcription activation [42][43][44][45][46][47][48], this chaperone is known to have an evolutionarily conserved role in heterochromatin formation [49][50][51][52][53][54][55][56].…”

Identical sequences but different expression patterns of Hira gene in gynogenetic and gonochoristic crucian carps

“…They represent a conserved protein family found in various organisms, including Drosophila melanogaster, pufferfish, Xenopus laevis, chicken, mouse, humans, and plants (Kirov et al 1998;Llevadot et al 1998;Ray-Gallet et al 2002;Roberts et al 1997;Scamps et al 1996;Pizzuti et al 1999;Phelps-Durr et al 2005). HIRA proteins are characterized by seven conserved WD repeats in their N-terminal, which are predicted to assemble into a b-propeller structure known to provide interfaces for protein-protein interactions (Komachi et al 1994;Smith et al 1999).…”