The Histone Chaperone HIRA Is a Positive Regulator of Seed Germination

Abstract

Histone chaperones regulate the flow and dynamics of histone variants and ensure their assembly into nucleosomal structures, thereby contributing to the repertoire of histone variants in specialized cells or tissues. To date, not much is known on the distribution of histone variants and their modifications in the dry seed embryo. Here, we bring evidence that genes encoding the replacement histone variant H3.3 are expressed in Arabidopsis dry seeds and that embryo chromatin is characterized by a low H3.1/H3.3 ratio. Loss of HISTONE REGULATOR A (HIRA), a histone chaperone responsible for H3.3 deposition, reduces cellular H3 levels and increases chromatin accessibility in dry seeds. These molecular differences are accompanied by increased seed dormancy in hira-1 mutant seeds. The loss of HIRA negatively affects seed germination even in the absence of HISTONE MONOUBIQUITINATION 1 or TRANSCRIPTION ELONGATION FACTOR II S, known to be required for seed dormancy. Finally, hira-1 mutant seeds show lower germination efficiency when aged under controlled deterioration conditions or when facing unfavorable environmental conditions such as high salinity. Altogether, our results reveal a dependency of dry seed chromatin organization on the replication-independent histone deposition pathway and show that HIRA contributes to modulating seed dormancy and vigor.

Histone H3.3 deposition in seed is essential for the post-embryonic developmental competence in Arabidopsis

“…It is unknown by which mechanism H3.3 is deposited to the 5′ gene ends in seeds but removed during germination and seedling development. This possibly involves the H3.3 deposition chaperone HIRA 63 that plays a moderate function in seed germination 64 , or ATRX involved in the deposition of H3.3 65,66 . In addition, specific chromatin remodelers might recruit H3.3 deposition machinery.…”

Maintenance and dynamic reprogramming of chromatin organization during development

“…In the dry seed, the embryo rests in a quiescent state. Embryonic nuclei are small (Figure 2) with highly condensed chromatin (van Zanten et al, 2011(van Zanten et al, , 2012 that has a peculiar composition, highly enriched in the replacement histone variant H3.3 (Layat et al, 2021;Zhao, Lu, et al, 2022) and a specific H2B variant, H2B.8 (Buttress et al, 2022;Jiang et al, 2020). H2B.8 is characterized by a long N-terminal tail that induces formation of phase-separated chromatin condensates contributing to chromatin compaction (Buttress et al, 2022).…”

Deposition and eviction of histone variants define functional chromatin states in plants

“…Outside S-phase, deposition of H3.3-H4 at regions of high nucleosome turnover or upon chromatin reorganization during DNA-repair and transcription requires HISTONE REGULATOR A (HIRA) [17,18] and the Alpha Thalassemia-mental Retardation X-linked (ATRX) ortholog [19]. The importance of these pathways becomes evident upon their perturbation that leads to reduced nucleosome occupancy or altered cellular H3.1/H3.3 ratios [16,[19][20][21]. H3.1 and H3.3 differing by only 4-5 amino acids are believed to have emerged repeatedly during evolution [22].…”