Epigenetic role for the conserved Fe-S cluster biogenesis protein AtDRE2 in Arabidopsis thaliana

被引:22
作者
Buzas, Diana Mihaela [1 ,2 ,3 ]
Nakamura, Miyuki [1 ,4 ]
Kinoshita, Tetsu [1 ,2 ,3 ]
机构
[1] Nara Inst Sci & Technol, Grad Sch Biol Sci, Nara 6300192, Japan
[2] Nagahama Inst Biosci & Technol, Fac Biosci, Nagahama, Shiga 5260829, Japan
[3] Yokohama City Univ, Kihara Inst Biol Res, Yokohama, Kanagawa 2440813, Japan
[4] Swedish Univ Agr Sci, Dept Plant Biol, SE-75007 Uppsala, Sweden
基金
日本学术振兴会;
关键词
IRON-SULFUR PROTEINS; DNA GLYCOSYLASE; DOMAIN PROTEIN; DEMETHYLATION; EXPRESSION; ENDOSPERM; DEMETER; ACTS; METHYLATION; MATURATION;
D O I
10.1073/pnas.1404058111
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
On fertilization in Arabidopsis thaliana, one maternal gamete, the central cell, forms a placenta-like tissue, the endosperm. The DNA glycosylase DEMETER (DME) excises 5-methylcytosine via the base excision repair pathway in the central cell before fertilization, creating patterns of asymmetric DNA methylation and maternal gene expression across DNA replications in the endosperm lineage (EDL). Active DNA demethylation in the central cell is essential for transcriptional activity in the EDL of a set of genes, including FLOWERING WAGENINGEN (FWA). A DME-binding motif for iron-sulfur (Fe-S) cluster cofactors is indispensable for its catalytic activity. We used an FWA-GFP reporter to find mutants defective in maternal activation of FWA-GFP in the EDL, and isolated an allele of the yeast Dre2/ human antiapoptotic factor CIAPIN1 homolog, encoding an enzyme previously implicated in the cytosolic Fe-S biogenesis pathway (CIA), which we named atdre2-2. We found that AtDRE2 acts in the central cell to regulate genes maternally activated in the EDL by DME. Furthermore, the FWA-GFP expression defect in atdre2-2 was partially suppressed genetically by a mutation in the maintenance DNA methyltransferase MET1; the DNA methylation levels at four DME targets increased in atdre2-2 seeds relative to WT. Although atdre2-2 shares zygotic seed defects with CIA mutants, it also uniquely manifests dme phenotypic hallmarks. These results demonstrate a previously unidentified epigenetic function of AtDRE2 that may be separate from the CIA pathway.
引用
收藏
页码:13565 / 13570
页数:6
相关论文
共 34 条
[1]   The essential WD40 protein Cia1 is involved in a late step of cytosolic and nuclear iron-sulfur protein assembly [J].
Balk, J ;
Netz, DJA ;
Tepper, K ;
Pierik, AJ ;
Lill, R .
MOLECULAR AND CELLULAR BIOLOGY, 2005, 25 (24) :10833-10841
[2]   The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins [J].
Balk, J ;
Pierik, AJ ;
Netz, DJA ;
Mühlenhoff, U ;
Lill, R .
EMBO JOURNAL, 2004, 23 (10) :2105-2115
[3]   Iron Cofactor Assembly in Plants [J].
Balk, Janneke ;
Schaedler, Theresia A. .
ANNUAL REVIEW OF PLANT BIOLOGY, VOL 65, 2014, 65 :125-+
[4]   The MADS domain protein DIANA acts together with AGAMOUS-LIKE80 to specify the central cell in Arabidopsis ovules [J].
Bemer, Marian ;
Wolters-Arts, Mieke ;
Grossniklaus, Ueli ;
Angenent, Gerco C. .
PLANT CELL, 2008, 20 (08) :2088-2101
[5]   Requirements of the cytosolic iron-sulfur cluster assembly pathway in Arabidopsis [J].
Bernard, Delphine G. ;
Netz, Daili J. A. ;
Lagny, Thibaut J. ;
Pierik, Antonio J. ;
Balk, Janneke .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2013, 368 (1622)
[6]   Redox signaling between DNA repair proteins for efficient lesion detection [J].
Boal, Amie K. ;
Genereux, Joseph C. ;
Sontz, Pamela A. ;
Gralnick, Jeffrey A. ;
Newman, Dianne K. ;
Barton, Jacqueline K. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2009, 106 (36) :15237-15242
[7]   The Essential Cytosolic Iron-Sulfur Protein Nbp35 Acts without Cfd1 Partner in the Green Lineage [J].
Bych, Katrine ;
Netz, Daili J. A. ;
Vigani, Gianpiero ;
Bill, Eckhard ;
Lill, Roland ;
Pierik, Antonio J. ;
Balk, Janneke .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2008, 283 (51) :35797-35804
[8]   Characterization of mutations that are synthetic lethal with pol3-13, a mutated allele of DNA polymerase delta in Saccharomyces cerevisiae [J].
Chanet, R ;
Heude, M .
CURRENT GENETICS, 2003, 43 (05) :337-350
[9]   DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis [J].
Choi, YH ;
Gehring, M ;
Johnson, L ;
Hannon, M ;
Harada, JJ ;
Goldberg, RB ;
Jacobsen, SE ;
Fischer, RL .
CELL, 2002, 110 (01) :33-42
[10]   DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation [J].
Gehring, M ;
Huh, JH ;
Hsieh, TF ;
Penterman, J ;
Choi, Y ;
Harada, JJ ;
Goldberg, RB ;
Fischer, RL .
CELL, 2006, 124 (03) :495-506