College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Sanya Institute of Breeding and Multiplication, Hainan University, Sanya, Hainan 572025, China; School of Tropical Agriculture and Forestry, Hainan University, Haikou, Hainan 570228, China; Hainan Yazhou Bay Seed Laboratory, Sanya, Hainan 572025, China.
Sanya Institute of Breeding and Multiplication, Hainan University, Sanya, Hainan 572025, China; School of Tropical Agriculture and Forestry, Hainan University, Haikou, Hainan 570228, China; Hainan Yazhou Bay Seed Laboratory, Sanya, Hainan 572025, China.
J Genet Genomics. 2024 Aug;51(8):855-865. doi: 10.1016/j.jgg.2024.04.003. Epub 2024 Apr 8.
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 FertilizationIndependentSeed (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.
胚乳的早期发育对于平衡母体营养物质向后代的分配至关重要。这一过程被认为与基因组印迹进化相关，导致等位基因表达的亲本偏倚。除了独立于受精的种子（FIS）基因外，涉及早期胚乳发育和种子大小决定的印迹基因数量仍然有限。本研究在拟南芥中引入了早期胚乳表达的 HAIKU（IKU）下游候选 F-box1（ICF1）和 ICF2 作为母体表达的印迹基因（MEGs）。尽管这些基因也被中央细胞中的 DEMETER（DME）去甲基化，但它们的激活与经典 MEGs 如 FIS 基因中直接的 DME 介导的激活不同。相反，ICF 母本等位基因在其启动子中携带预先建立的低甲基化，使其能够在胚乳中被 WRKY10 转录因子激活。相反，父本等位基因主要被 CG 甲基化抑制。此外，我们发现 ICF 基因部分导致了 iku 突变体中观察到的小种子大小。我们的发现揭示了一个两步调控机制，强调了常规转录因子在印迹基因激活中的重要作用，这在以前并未得到充分认识。因此，该机制为理解植物生殖和发育中印迹的转录调控提供了一个新的维度。
