ZmICE1a regulates the defence–storage trade-off in maize endosperm [CUT&Tag]
The endosperm of cereal grains feeds the entire world as major food supply, however little is known for its defense responses during endosperm development. Inducer of CBF Expression 1 (ICE1) is a known regulator of cold tolerance in plants. ICE1 has a monocot-specific homologue that is preferentially expressed in cereal grains but with an unclear regulatory function. Here, we characterized the function of monocot-specific ZmICE1 (ZmICE1a) in maize (Zea mays) kernel. mRNA in situ hybridization (ISH) revealed that ZmICE1a is predominantly expressed in the peripheral endosperm (AL, SAL, and BETL). Loss-of-function of ZmICE1a reduced starch content and kernel weight. RNA-seq analysis revealed contradicted expression patterns between starch synthesis genes and genes involved in defense and phytohormone synthesis in zmice1a developing endosperm. Coupled with CUT&Tag-seq analysis, we found that ZmICE1a positively regulates genes in starch synthesis, while negatively regulates genes in AL-specific defense and the synthesis of IAA and JA. Explant assays revealed that exogenous IAA or JA induces the expression of numerous defense genes. mRNA ISH assays revealed that the defense genes induced by IAA and JA, exhibit distinct spatial specific expression in BETL and SAL, respectively. Moreover, we dissected a JA-ZmJAZ9-ZmICE1a-MPI signaling axis involved in JA-mediated defense regulation. Overall, our study revealed ZmICE1a as a key regulatory for endosperm defense responses, and coordinates defense-storage tradeoffs during endosperm development. Overall design: Identification of ZmICE1a regulatory functions using RNA-seq and CUT&Tag-seq during maize endosperm development