Arabidopsis Histone Methylase CAU1/PRMT5/SKB1 Acts as an Epigenetic Suppressor of the Calcium Signaling Gene CAS to Mediate Stomatal Closure in Response to Extracellular Calcium

Abstract

(J-M.G).Elevations in extracellular calcium ([Ca 2+ ] o ) are known to stimulate cytosolic calcium ([Ca 2+ ] cyt ) oscillations to close stomata. However, the underlying mechanisms regulating this process remain largely to be determined. Here, through the functional characterization of the calcium underaccumulation mutant cau1, we report that the epigenetic regulation of CAS, a putative Ca 2+ binding protein proposed to be an external Ca 2+ sensor, is involved in this process. cau1 mutant plants display increased drought tolerance and stomatal closure. A mutation in CAU1 significantly increased the expression level of the calcium signaling gene CAS, and functional disruption of CAS abolished the enhanced drought tolerance and stomatal [Ca 2+ ] o signaling in cau1. Map-based cloning revealed that CAU1 encodes the H4R3sme2 (for histone H4 Arg 3 with symmetric dimethylation)-type histone methylase protein arginine methytransferase5/Shk1 binding protein1. Chromatin immunoprecipitation assays showed that CAU1 binds to the CAS promoter and modulates the H4R3sme2-type histone methylation of the CAS chromatin. When exposed to elevated [Ca 2+ ] o , the protein levels of CAU1 decreased and less CAU1 bound to the CAS promoter. In addition, the methylation level of H4R3sme2 decreased in the CAS chromatin. Together, these data suggest that in response to increases in [Ca 2+ ] o , fewer CAU1 protein molecules bind to the CAS promoter, leading to decreased H4R3sme2 methylation and consequent derepression of the expression of CAS to mediate stomatal closure and drought tolerance. INTRODUCTIONCytosolic calcium ([Ca 2+ ] cyt ) plays a pivotal role as a second messenger in plant development and interactions with the environment (Helpler and Wayne, 1985;Poovaiah and Reddy, 1993;Bush, 1995). Various signals, including biotic stress, abiotic stress, hormones, and mechanical disturbance, are sensed by plant cells and elicit repetitive oscillation or spiking of [Ca 2+ ] cyt , which are termed Ca 2+ signatures and regulated by Ca 2+ channels, pumps, or carriers localized at the plasma membrane or in the membranes of organelles (Bush, 1995;Thuleau et al., 1998;Rudd and Franklin-Tong, 1999;Sanders et al., 1999;Allen et al., 2000Allen et al., , 2001Harper, 2001). These Ca 2+ signatures vary in frequency and amplitude in response to different stimuli and thus are believed to encode stimulus-specific information that can be transduced and sensed by downstream Ca 2+ sensors, including calmodulins, calcium-dependent proteins, and calcineurin B-like proteins (Zielinski, 1998;Luan et al., 2002;Sanders et al., 2002). These calcium sensors decode Ca 2+ signatures by binding Ca 2+ ions via conserved EF-hand domains and transduce them into specific cellular responses, such as altered phosphorylation and expression of target genes, to bring about physiological responses corresponding to the original stimuli (Luan et al., 2002;Sanders et al., 2002).In contrast with intracellular Ca 2+ , the role of extracellular Ca 2+ ([Ca 2+ ] o ) remains to ...

Quantitative phosphoproteomics of lectin receptor‐like kinase VI.4 dependent abscisic acid response in Arabidopsis thaliana

“…ABA affects the CAU1–CAS interaction and interrupts the suppression of CAS. CAS plays an important role in evoking [Ca 2+ ] cyt by regulating inositol‐1,4,5‐trisphosphate (IP3) biosynthesis (Weinl et al , Fu et al ). Furthermore, CAS is related to optimal photosynthesis (Wang et al ).…”

PARAQUAT TOLERANCE3 Is an E3 Ligase That Switches off Activated Oxidative Response by Targeting Histone-Modifying PROTEIN METHYLTRANSFERASE4b

“…Two different types of PRMTs catalyze asymmetric di-methylation (ADMA) and symmetric di-methylation (SDMA) on the Arg residues, respectively [ 17 , 21 ]. The prmt5 mutant has decreased level of histone H4 Arg3-SDMA, leading to enhanced drought tolerance [ 22 ]. A pair of PROTEIN ARGININE METHYLTRANSFERASE4 (PRMT4) homologs, AtPRMT4a and AtPRMT4b, is required for the asymmetrical di-methylation of Arg-2, Arg-17, and Arg-26 in histone H3 [ 14 ].…”

Phosphoenolpyruvate carboxylase regulation in C4‐PEPC‐expressing transgenic rice during early responses to drought stress

“…The efficiency of Ca 2+ signaling is mediated by Ca 2+ ‐binding proteins (McCormack and Braam ). Additionally, Ca 2+ ‐binding proteins, calmodulin‐like proteins, calcineurin B‐like protein and calcineurin B‐like protein‐interacting kinases mediate plant responses to a variety of external stresses (Tripathi et al , Fu et al ). Previous studies have also concluded that the endogenous Ca 2+ signaling molecule also regulates C4‐PEPC activity under natural or drought conditions in transgenic rice containing the maize C4‐PEPC gene (Li et al , Chen et al , Ren et al ).…”

“…Cell‐specific accumulation of maize PEPC is correlated with demethylation at a specific site located greater than 3 kb upstream of the gene (Langdale et al ). A previous report indicated that the A. thaliana histone methylase CAU1/PRMT5/SKB1 acts as an epigenetic suppressor of the CAS calcium signaling gene to mediate stomatal closure and drought tolerance in response to extracellular calcium (Fu et al ). Whether the methylation of the exogenous promoter of C4‐PEPC influences rice drought responses is unclear and requires further study.…”