Subclass-III-SnRK2s orchestrates concurrent starch and storage proteins accumulation during kernel filling in maize

Enhancing both starch and protein accumulation is a key strategy for improving maize yield and quality. Achieving this goal requires an in-depth understanding of the regulatory mechanisms that integrate these pathways. Here, we demonstrate that functionally-redundant subclass III SNF1-related protein kinase2s (SnRK2s) act as central regulators that orchestrate starch synthesis and storage proteins accumulation in maize kernels, with ZmSnRK2.10 playing a predominant role. High-order SnRK2s mutants lacking ZmSnRK2.10 exhibit defective kernel development, with drastically reduced starch and storage proteins content. Mechanistically, ZmSnRK2.10 directly phosphorylates starch synthesis-related enzymes, such as BT1, enhancing their activities and thereby boosting endosperm starch synthesis. In contrast, it indirectly promotes storage proteins synthesis in both endosperm and embryo through modulating the phosphorylation status of downstream transcription factors including Opaque-2 and ZmbZIP75. Interestingly, our study reveals that ZmSnRK2.10 undergoes sequential activation: initially by sucrose in the endosperm during early kernel filling and subsequently by abscisic acid (ABA) in the embryo during later developmental stages. This spatiotemporal regulation suggests a mechanism facilitating coordinated control of these temporally linked processes. Notably, overexpression of ZmSnRK2.10 leads to significant increases in both starch and protein content, as well as a higher vitreous endosperm ratio, thereby simultaneously enhancing maize yield and quality. Our study thus uncovers a previously unknown regulatory mechanism involving subclass III SnRK2s that governs storage functions in maize kernel and provides potential genetic resources for yield and quality improvement.