Hybrid seed failure arising from wide crosses between plant species is a recurring obstacle in plant breeding, impeding the transfer of desirable traits. This postzygotic reproductive barrier primarily occurs in the endosperm, a tissue that nourishes the embryo and functions similarly to the placenta in mammals. We found that incompatible seeds show a loss of DNA methylation and chromatin condensation in the endosperm, similar to seeds lacking maternal RNA polymerase IV activity. This similarity is linked to a decrease in small interfering RNAs in the endosperm (sirenRNAs), maternal RNA polymerase IV-dependent short interfering RNAs that regulate DNA methylation. Several AGAMOUS-like MADS-box transcription factor genes (AGLs), key regulators of endosperm development, are targeted by sirenRNAs in cis and in trans. This finding aligns with the enrichment of AGL target genes among deregulated genes. We propose that hybrid seed failure results from reduced maternal sirenRNAs combined with increased AGL expression, leading to abnormal gene regulation in the endosperm.

植物物种之间的广泛杂交引起的杂交种子失败是植物育种中反复出现的障碍，阻碍了理想性状的转移。这种合子后生殖屏障主要发生在胚乳中，胚乳是一种滋养胚胎的组织，其功能类似于哺乳动物的胎盘。我们发现，不相容的种子在胚乳中显示出 DNA 甲基化和染色质浓缩的丢失，类似于缺乏母体 RNA 聚合酶 IV 活性的种子。这种相似性与胚乳中小干扰 RNA （sirenRNA） 的减少有关，SirenRNA 是调节 DNA 甲基化的母体 RNA 聚合酶 IV 依赖性短干扰 RNA。几个 AGAMOUS 样 MADS-box 转录因子基因 （AGLs） 是胚乳发育的关键调节因子，是 sirenRNA 在顺式和反式中靶向的。这一发现与失调基因中 AGL 靶基因的富集一致。我们提出杂交种子失败是由于母体 sirenRNA 减少加上 AGL 表达增加，导致胚乳基因调控异常。