Two imprinted genes primed by DEMETER in the central cell and activated by WRKY10 in the endosperm

Ke Yang; Yuling Tang; Yue Li; Wenbin Guo; Zhengdao Hu; Xuanpeng Wang; Fr&#233;d&#233;ric Berger; Jing Li

doi:10.1016/j.jgg.2024.04.003

Volume 51 Issue 8

Aug. 2024

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Two imprinted genes primed by DEMETER in the central cell and activated by WRKY10 in the endosperm

doi: 10.1016/j.jgg.2024.04.003

Ke Yang^a,b,c,d,
Yuling Tang^b,c,d,
Yue Li^a,
Wenbin Guo^a,
Zhengdao Hu^a,
Xuanpeng Wang^b,c,d,
Frédéric Berger^e,
Jing Li^b,c,d

a. College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China;
b. Sanya Institute of Breeding and Multiplication, Hainan University, Sanya, Hainan 572025, China;
c. School of Tropical Agriculture and Forestry, Hainan University, Haikou, Hainan 570228, China;
d. Hainan Yazhou Bay Seed Laboratory, Sanya, Hainan 572025, China;
e. Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, 1030 Vienna, Austria

Funds:

This work was supported by the National Natural Science Foundation of China (31570322).

Received Date: 2024-03-28
Accepted Date: 2024-04-02
Rev Recd Date: 2024-04-02

Available Online: 2025-06-06

Publish Date: 2024-04-08

Abstract

Abstract

The early development of the endosperm is crucial for balancing the allocation of maternal nutrients to offspring. This process is believed to be evolutionarily associated with genomic imprinting, resulting in parentally biased allelic gene expression. Beyond Fertilization Independent Seed (FIS) genes, the number of imprinted genes involved in early endosperm development and seed size determination remains limited. This study introduces early endosperm-expressed HAIKU (IKU) downstream Candidate F-box 1 (ICF1) and ICF2 as maternally expressed imprinted genes (MEGs) in Arabidopsis thaliana. Although these genes are also demethylated by DEMETER (DME) in the central cell, their activation differs from the direct DME-mediated activation seen in classical MEGs such as the FIS genes. Instead, ICF maternal alleles carry pre-established hypomethylation in their promoters, priming them for activation by the WRKY10 transcription factor in the endosperm. On the contrary, paternal alleles are predominantly suppressed by CG methylation. Furthermore, we find that ICF genes partially contribute to the small seed size observed in iku mutants. Our discovery reveals a two-step regulatory mechanism that highlights the important role of conventional transcription factors in the activation of imprinted genes, which was previously not fully recognized. Therefore, the mechanism provides a new dimension to understand the transcriptional regulation of imprinting in plant reproduction and development.
- Imprinting,
- Epigenetics,
- DNA methylation,
- Seed size,
- Endosperm

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References(48)

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