ZmICE1a regulates the defence–storage trade-off in maize endosperm

Abstract

The endosperm of cereal grains feeds the entire world as a major food supply; however, little is known about its defence response during endosperm development. The Inducer of CBF Expression 1 (ICE1) is a well-known regulator of cold tolerance in plants. ICE1 has a monocot-specific homologue that is preferentially expressed in cereal endosperms but with an unclear regulatory function. Here we characterized the function of monocot-specific ZmICE1a, which is expressed in the entire endosperm, with a predominant expression in its peripheral regions, including the aleurone layer, subaleurone layer and basal endosperm transfer layer in maize (Zea mays). Loss of function of ZmICE1a reduced starch content and kernel weight. RNA sequencing and CUT&Tag-seq analyses revealed that ZmICE1a positively regulates genes in starch synthesis while negatively regulating genes in aleurone layer-specific defence and the synthesis of indole-3-acetic acid and jasmonic acid (JA). Exogenous indole-3-acetic acid and JA both induce the expression of numerous defence genes, which show distinct spatial-specific expression in the basal endosperm transfer layer and subaleurone layer, respectively. Moreover, we dissected a JA–ZmJAZ9–ZmICE1a–MPI signalling axis involved in JA-mediated defence regulation. Overall, our study revealed ZmICE1a as a key regulator of endosperm defence response and a coordinator of the defence–storage trade-off in endosperm development. A cereal-specific transcription factor, ZmICE1a, positively regulates storage in the central part of the endosperm while negatively regulating defence in its peripheral region, revealing the molecular mechanism underlying the antagonism between resistance and yield, which is crucial for cereal crop improvement.