SAC3B, a central component of the mRNA export complex TREX-2, is required for prevention of epigenetic gene silencing in Arabidopsis.
Epigenetic regulation is important for organismal development and response to the environment. Alteration in epigenetic status has been known mostly from the perspective of enzymatic actions of DNA methylation and/or histone modifications. In a genetic screen for cellular factors involved in preventing epigenetic silencing, we isolated an Arabidopsis mutant defective in SAC3B, a component of the conserved TREX-2 complex that couples mRNA transcription with nuleo-cytoplasmic export. Arabidopsis SAC3B dysfunction causes gene silencing at transgenic and endogenous loci, accompanied by elevation in the repressive histone mark H3K9me2 and by reduction in RNA polymerase Pol II occupancy. SAC3B dysfunction does not alter promoter DNA methylation level of the transgene d35S::LUC, although the DNA demethylase ROS1 is also required for d35S::LUC anti-silencing. THP1 and NUA were identified as SAC3B-associated proteins whose mutations also caused d35S::LUC silencing. RNA-DNA hybrid exists at the repressed loci but is unrelated to gene suppression by the sac3b mutation. Genome-wide analyses demonstrated minor but clear involvement of SAC3B in regulating siRNAs and DNA methylation, particularly at a group of TAS and TAS-like loci. Together our results revealed not only a critical role of mRNA-export factors in transcriptional anti-silencing but also the contribution of SAC3B in shaping plant epigenetic landscapes.
Shanghai Center for Plant Stress Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China.|Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USA.|Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou, Gansu 730000, China.
Yu
Y
Yang
Shanghai Center for Plant Stress Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China.|Department of Biochemistry and Molecular Biology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China.
Honggui
H
La
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USA.
Kai
K
Tang
Shanghai Center for Plant Stress Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China.
Daisuke
D
Miki
Shanghai Center for Plant Stress Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China.
Lan
L
Yang
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USA.
Bangshing
B
Wang
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USA.
Cheng-Guo
CG
Duan
Shanghai Center for Plant Stress Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China.
Wenfeng
W
Nie
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USA.
Xingang
X
Wang
Department of Biochemistry, Purdue University, West Lafayette, IN 47906, USA.
Siwen
S
Wang
Shanghai Center for Plant Stress Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China.
Yufeng
Y
Pan
Department of Biochemistry, Purdue University, West Lafayette, IN 47906, USA.
Elizabeth J
EJ
Tran
Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou, Gansu 730000, China.
Lizhe
L
An
Shanghai Center for Plant Stress Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China hmzhang@sibs.ac.cn.|CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China.
Huiming
H
Zhang
Shanghai Center for Plant Stress Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China hmzhang@sibs.ac.cn.|Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USA.|CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China.
Jian-Kang
JK
Zhu
D021581:Active Transport, Cell Nucleus / Q000235:genetics*; D017360:Arabidopsis / Q000235:genetics* / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D002352:Carrier Proteins / Q000235:genetics* / Q000378:metabolism; D019175:DNA Methylation; D018506:Gene Expression Regulation, Plant; D020868:Gene Silencing; D017930:Genes, Reporter; D056426:Genetic Loci; D008156:Luciferases / Q000235:genetics / Q000378:metabolism; D028861:Nuclear Pore Complex Proteins / Q000235:genetics / Q000378:metabolism; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D012319:RNA Polymerase II / Q000235:genetics / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics* / Q000378:metabolism; D034741:RNA, Small Interfering / Q000235:genetics / Q000378:metabolism; D012261:Ribonucleoproteins / Q000235:genetics* / Q000378:metabolism; D014158:Transcription, Genetic
D029681:Arabidopsis Proteins; D002352:Carrier Proteins; C523535:NUA protein, Arabidopsis; D028861:Nuclear Pore Complex Proteins; D009687:Nuclear Proteins; D012333:RNA, Messenger; D034741:RNA, Small Interfering; C471271:ROS1 protein, Arabidopsis; D012261:Ribonucleoproteins; C000620500:SAC3B protein, Arabidopsis; D008156:Luciferases; D012319:RNA Polymerase II
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