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 (Zea mays) grain development, 2 distinct endosperm cell death processes occur: in 1 process, the endosperm adjacent to the embryo scutellum (EAS) is completely dismantled; in the other, the starchy endosperm (SE) retains nutrient-packed cell corpses after grain filling. Here, we show that SE cell death degrades some organelles including the 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 2 NAC transcription factors, KIRA-LIKE 1 (KIL1) and 2 (KIL2), as specifically upregulated in the EAS. Analyses using dominant and recessive loss-of-function kil mutants demonstrate that these genes redundantly promote cell death and corpse clearance in the EAS, but are not required for SE cell death. Reduced EAS cell death in kil loss-of-function mutants strongly impeded embryo growth, indicating that EAS elimination is crucial for optimal embryo development. Notably, kil1 and kil2 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.

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Publication Details

Journal
The Plant Cell
Published
2025-06-20
DOI
https://doi.org/10.1093/plcell/koaf162
Citations
5
Primary Topic
Plant tissue culture and regeneration
Type
article
Field-Weighted Citation Impact
4.03

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article

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

Thomas Widiez, Geng Sun, Bert De Rybel, Émilie Montes et al.
5 citations
The Plant Cell
Plant tissue culture and regeneration
4.03
article

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

Thomas Widiez, Geng Sun, Bert De Rybel, Émilie Montes, Mohammed Bendahmane, Yemisrach Melkie Abebaw, Thomas Eekhout, Stijn Aesaert, Griet Coussens, Lisa Elias, Yannick Fierlej, Peter Rogowsky, Riet De Rycke, Nicolas M. Doll, Laurens Pauwels, Carolin Seyfferth, Moritz K. Nowack, Clément Bellot, Maria Šimášková, Chloé Plagnard
article en
5 citations

Abstract

The endosperm is a transient nutritive tissue in plant seeds. During maize (Zea mays) grain development, 2 distinct endosperm cell death processes occur: in 1 process, the endosperm adjacent to the embryo scutellum (EAS) is completely dismantled; in the other, the starchy endosperm (SE) retains nutrient-packed cell corpses after grain filling. Here, we show that SE cell death degrades some organelles including the 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 2 NAC transcription factors, KIRA-LIKE 1 (KIL1) and 2 (KIL2), as specifically upregulated in the EAS. Analyses using dominant and recessive loss-of-function kil mutants demonstrate that these genes redundantly promote cell death and corpse clearance in the EAS, but are not required for SE cell death. Reduced EAS cell death in kil loss-of-function mutants strongly impeded embryo growth, indicating that EAS elimination is crucial for optimal embryo development. Notably, kil1 and kil2 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.

The Plant CellVol. 37(7)
Université Claude Bernard Lyon 1 (FR), École Normale Supérieure de Lyon (FR), HOGENT University of Applied Sciences and Arts (BE), Centre National de la Recherche Scientifique (FR), Ghent University Hospital (BE), Ghent University (BE), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), VIB-UGent Center for Plant Systems Biology (BE), Addis Ababa Science and Technology University (ET), VIB-UGent Center for Inflammation Research (BE), Laboratoire Reproduction et Développement des Plantes (FR)
European Molecular Biology Organization, Fonds Wetenschappelijk Onderzoek, Fondation Bettencourt Schueller, European Research Council
Zero hunger
Openalex Percentile: Top 6%
Plant tissue culture and regeneration
4.03
DOIOpen Access PDFOpenAlex
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