The domestication-associated WHP10 tandem cluster of amino-acid transporter genes enhances whole-plant protein accumulation in maize.

Abstract

Improving protein accumulation in maize is essential for sustainable agriculture, yet the regulatory mechanisms governing the intermediate "flow" of organic nitrogen remain elusive. Here, we reveal that the maize stem acts as a critical regulatory node for nitrogen allocation. By integrating spatial transcriptomics and metabolomics with quantitative genetics, we demonstrate that the high-protein phenotype of the wild maize accession Ames21814 is orchestrated by a transport-oriented stem program. We identified a major locus, Whole-plant High Protein 10 (WHP10), which encodes a tandemly duplicated cluster of amino-acid transporter genes. WHP10 exhibits strong vascular-biased expression, driven by promoter divergence that enhances the wild allele's activity. Functional assays and genetic validation support a model in which the WHP10 cluster facilitates the transport of multiple key nitrogen-rich amino acids, thereby contributing to vascular-associated amino-acid transport and post-uptake organic-nitrogen partitioning. Our findings establish stem flow as a pivotal regulatory layer for protein accumulation and identify WHP10 as a high-value target for precision breeding to enhance whole-plant protein accumulation without compromising grain yield.