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.
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.
National Key Laboratory of Plant Molecular Genetics and National Center for Plant Gene Research (Shanghai), Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, People's Republic of China.
Yan-Lei
YL
Fu
Guo-Bin
GB
Zhang
Xin-Fang
XF
Lv
Yuan
Y
Guan
Hong-Ying
HY
Yi
Ji-Ming
JM
Gong
D000040:Abscisic Acid / Q000494:pharmacology; D000222:Adaptation, Physiological / Q000187:drug effects / Q000235:genetics; D017360:Arabidopsis / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism*; D001120:Arginine / Q000378:metabolism; D002118:Calcium / Q000494:pharmacology*; D020013:Calcium Signaling / Q000187:drug effects* / Q000235:genetics; D002135:Calcium-Binding Proteins / Q000235:genetics* / Q000378:metabolism; D003001:Cloning, Molecular; D055864:Droughts; D044127:Epigenesis, Genetic / Q000187:drug effects*; D005110:Extracellular Space / Q000187:drug effects / Q000378:metabolism; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D017343:Genes, Plant / Q000235:genetics; D016153:Genes, Suppressor; D006657:Histones / Q000378:metabolism; D006706:Homeostasis / Q000187:drug effects / Q000235:genetics; D008745:Methylation / Q000187:drug effects; D008954:Models, Biological; D009154:Mutation / Q000235:genetics; D054046:Plant Stomata / Q000166:cytology / Q000187:drug effects / Q000502:physiology*; D011484:Protein-Arginine N-Methyltransferases / Q000378:metabolism*
D029681:Arabidopsis Proteins; C532740:CAS protein, Arabidopsis; D002135:Calcium-Binding Proteins; D006657:Histones; D000040:Abscisic Acid; D001120:Arginine; C524490:PRMT5 protein, Arabidopsis; D011484:Protein-Arginine N-Methyltransferases; D002118:Calcium