Transcriptional Regulation of Cell Cycle Genes in Response to Abiotic Stresses Correlates with Dynamic Changes in Histone Modifications in Maize

Abstract

The histone modification level has been shown to be related with gene activation and repression in stress-responsive process, but there is little information on the relationship between histone modification and cell cycle gene expression responsive to environmental cues. In this study, the function of histone modifications in mediating the transcriptional regulation of cell cycle genes under various types of stress was investigated in maize (Zea mays L.). Abiotic stresses all inhibit the growth of maize seedlings, and induce total acetylation level increase compared with the control group in maize roots. The positive and negative regulation of the expression of some cell cycle genes leads to perturbation of cell cycle progression in response to abiotic stresses. Chromatin immunoprecipitation analysis reveals that dynamic histone acetylation change in the promoter region of cell cycle genes is involved in the control of gene expression in response to external stress and different cell cycle genes have their own characteristic patterns for histone acetylation. The data also showed that the combinations of hyperacetylation and hypoacetylation states of specific lysine sites on the H3 and H4 tails on the promoter regions of cell cycle genes regulate specific cell cycle gene expression under abiotic stress conditions, thus resulting in prolonged cell cycle duration and an inhibitory effect on growth and development in maize seedlings.

A regulatory module controlling stress-induced cell cycle arrest in Arabidopsis

“…On the other hand, when the Cytrap line was treated with 400 mM mannitol for 24 h, S/G2 phase cells decreased by half, and G1 phase cells, which are represented by the lack of expression of both CYCB1;1 and CDT1a markers, significantly increased (Figure 7-figure supplement 1A and B). These results are consistent with the previous observation in maize (Zhao et al, 2014). We found that the anac044 anac085 mutant exhibited the same sensitivity as WT to mannitol (Figure 7-figure supplement 1C), and that the promoter activity of ANAC044 was not elevated by mannitol treatment (Figure 7-figure supplement 1D).…”

“…The above results indicate that the ANAC044/085-mediated pathway plays a major role in DNA stress-induced cell cycle arrest. To examine whether the same signalling module also functions in other stress responses, we investigated the involvement of ANAC044 and ANAC085 in the response to heat and osmotic stresses, which are known to retard G2 and G1 phase progression, respectively, in maize roots (Zhao et al, 2014). When transgenic Arabidopsis seedlings harbouring the cell cycle marker system Cytrap (Yin et al, 2014) were grown at higher temperature (37 °C) for 24 h, root cells expressing the late G2/M marker CYCB1;1 increased significantly, while those expressing the S/G2 marker CDT1a were dramatically reduced (Figure 7A and B).…”

Nitric Oxide Modulates Histone Acetylation at Stress Genes by Inhibition of Histone Deacetylases

“…Global histone hyperacetylation has been observed after heat, salt, and cold stress in a variety of plant species (Sokol et al, 2007;Zhao et al, 2014;Wang et al, 2015), and these stresses are generally characterized by the extensive production of NO (Zhao et al, 2007(Zhao et al, , 2009Bouchard and Yamasaki, 2008;Cantrel et al, 2011). In general, HDACs are transcriptional repressors of stress responses (Choi et al, 2012;Luo et al, 2012;Zheng et al, 2016).…”

Elucidating the molecular mechanisms mediating plant salt‐stress responses

“…Salt stress enhances FLOWERING LOCUS C (FLC) expression by reducing the association of the floral initiator Shk1 kinase binding protein1 (SKB1) with chromatin and reducing H4R3 symmetric dimethylation (H4R3sme2) levels in Arabidopsis, thereby regulating Arabidopsis flowering time under salt stress (Zhang Z. et al ., 2011). In maize roots, salt stress induces changes in histone acetylation in the promoter region of cell cycle genes (Zhou et al ., ,b). Elevated acetylation levels in H3K9 and H3K27 sites lead to transcriptional activation of a peroxidase (POX)‐encoding genes in Beta vulgaris and Beta maritima under salt‐stress conditions (Yolcu et al ., ).…”