Defining chromatin state transitions predicts a network that modulates cell wall remodeling in phosphate-starved rice shoots

Abstract

Phosphorus (P) is an essential plant macronutrient vital to fundamental metabolic processes. Plant-available P is low in most soils, making it a frequent limiter of growth. Declining P reserves for fertilizer production exasperates this agricultural challenge. Plants modulate complex responses to fluctuating P levels via global transcriptional regulatory networks. Although chromatin structure plays a substantial role in controlling gene expression, the chromatin dynamics involved in regulating P homeostasis have not been determined. Here we define distinct chromatin states across the rice genome by integrating multiple aspects of chromatin structure, including the H2A.Z histone variant, H3K4me3 modification, and nucleosome positioning. In response to P starvation, 40% of all protein-coding genes exhibit a transition from one chromatin state to another at their transcription start site. Several of these transitions are enriched in subsets of genes differentially expressed by P deficiency. The most prominent subset supports the presence of a coordinated signaling network that targets cell wall structure and is regulated in part via a decrease of H3K4me3 at the transcription start site. The P-starvation induced chromatin dynamics and correlated genes identified here will aid in enhancing P-use efficiency in crop plants, benefitting global agriculture.One sentence summaryCombining data for three components of chromatin structure from control and phosphate-starved rice shoots reveals specific chromatin state transitions that correlate with subsets of functionally distinct differentially-expressed genes.

H3K4 trimethylation dynamics impact diverse developmental and environmental responses in plants

“…Studies in diverse plant species and tissues have investigated genic levels of H3K4me3 in response to a variety of stresses (Foroozani et al, 2019;Jaskiewicz, Conrath, & Peterhänsel, 2011;Kim et al, 2008;Pan et al, 2017;Sokol, Kwiatkowska, Jerzmanowski, & Prymakowska-Bosak, 2007;Tsuji, Saika, Tsutsumi, Hirai, & Nakazono, 2006;van Dijk et al, 2010;Zeng et al, 2019;Zheng et al, 2019). Generally these studies reported positive correlations between H3K4me3 abundance and stress-induced gene expression, further supporting an active role for H3K4me3.…”

“…Because it is enriched in genic regions and correlates with transcript levels, it is considered an active histone mark (Françoise S Howe et al, 2017;Santos-Rosa et al, 2002). However, H3K4me3 dynamics have been associated with not only activation, but also repression of subsets of genes (Clouaire et al, 2012;Foroozani et al, 2019;Françoise S Howe et al, 2017;Lenstra et al, 2011). Unlike its counterpart in yeast, Arabidopsis ATX1 has been shown to play a dual role in transcription (Ding et al, 2011b).…”

“…Studies investigating responses to phosphate (Pi) starvation and high nitrogen have indicated a role for H3K4me3 in plant nutrient homeostasis. A recent report on chromatin dynamics in Pi-starved rice shoots showed that over 40% of protein-coding genes exhibited a low-Pi change in chromatin states (CSs) defined by differing levels of H3K4me3, H2A.Z, and nucleosome occupancy at their TSS (Foroozani et al, 2019). Genes marked by H3K4me3 and H2A.Z that exhibited decreases in both marks in response to Pi starvation were enriched among low-Pi induced genes.…”

“…However, the genome-level studies showed large decreases in 5' localization of H3K4me3 in averaged genic profiles of stressed samples relative to controls (Foroozani et al, 2019;Zeng et al, 2019;Zong, Zhong, You, & Xiong, 2013). Also, in two recent studies in rice, examination of specific subsets of stress-responsive genes revealed negative correlations between H3K4me3 abundance and gene upregulation in response to salt stress (Zheng et al, 2019) or phosphate (Pi) deficiency (Foroozani et al, 2019). These observations support a role for H3K4me3 in not only activation but also repression, consistent with findings in other systems (Clouaire et al, 2012;Françoise S Howe et al, 2017;Lenstra et al, 2011).…”

“…Generally these studies reported positive correlations between H3K4me3 abundance and stress-induced gene expression, further supporting an active role for H3K4me3. However, the genome-level studies showed large decreases in 5' localization of H3K4me3 in averaged genic profiles of stressed samples relative to controls (Foroozani et al, 2019;Zeng et al, 2019;Zong, Zhong, You, & Xiong, 2013). Also, in two recent studies in rice, examination of specific subsets of stress-responsive genes revealed negative correlations between H3K4me3 abundance and gene upregulation in response to salt stress (Zheng et al, 2019) or phosphate (Pi) deficiency (Foroozani et al, 2019).…”