KIL transcription factors facilitate embryo growth in maize by promoting endosperm elimination via lytic cell death

The endosperm is a transient nutritive tissue in plant seeds. During maize grain development, two distinct endosperm cell death processes occur. The endosperm adjacent to the embryo scutellum (EAS) is completely dismantled, whereas the starchy endosperm (SE) retains nutrient-packed cell corpses after grain filling. Here, we show that SE cell death selectively degrades some organelles including mitochondria and the endoplasmic reticulum, while preserving protein bodies, starch granules, and chromatin. In contrast, EAS cells undergo lytic cell death to remobilize stored nutrients through a complex corpse clearance process. Using single-cell transcriptome analysis, we identified two NAC transcription factors, KIL1 and KIL2, as specifically upregulated in the EAS. Dominant and recessive loss-of-function studies demonstrate that these genes redundantly promote cell death execution and corpse clearance in the EAS, but are not required for SE cell death. Reduced EAS cell death in KIL loss-of-function lines significantly impeded embryo growth, indicating that EAS elimination is crucial for optimal embryo development. Notably, kil1 and kil2 gene expression is regulated by DOSAGE-EFFECT DEFECTIVE1, an imprinted paternally expressed endosperm transcription factor. Our findings suggest paternal control over EAS cell death and the embryo-endosperm size ratio in maize, providing new leads to modulate this agronomically important trait. Overall design: Single-nucleus RNA-seq experiments were performed on nuclei extracted from endosperm of maize (B73) kernels.