Ribosome biogenesis is a fundamental and highly orchestrated process that involves hundreds of ribosome biogenesis factors. Despite advances that have been made in yeast, the molecular mechanism of ribosome biogenesis remains largely unknown in plants. We uncovered a WD40 protein, Shrunken and Embryo Defective Kernel 1 (SHREK1), and showed that it plays a crucial role in ribosome biogenesis and kernel development in maize (Zea mays). The shrek1 mutant shows an aborted embryo and underdeveloped endosperm and embryo-lethal in maize. SHREK1 localizes mainly to the nucleolus and accumulates to high levels in the seed. Depleting SHREK1 perturbs pre-rRNA processing and causes imbalanced profiles of mature rRNA and ribosome. The expression pattern of ribosomal-related genes is significantly altered in shrek1. Like its yeast (Saccharomyces cerevisiae) ortholog Periodic tryptophan protein 1 (PWP1), SHREK1 physically interacts with ribosomal protein ZmRPL7a, a transient component of the PWP1-subcomplex involved in pre-rRNA processing in yeast. Additionally, SHREK1 may assist in the A₃ cleavage of the pre-rRNA in maize by interacting with the nucleolar protein ZmPOP4, a maize homolog of the yeast RNase mitochondrial RNA-processing complex subunit. Overall, our work demonstrates a vital role of SHREK1 in pre-60S ribosome maturation, and reveals that impaired ribosome function accounts for the embryo lethality in shrek1.

Serine functions as both a substrate for protein biosynthesis and a signaling molecule for growth and development. However, the mechanism remains poorly understood. Here, we cloned and functionally characterized the maize (Zea mays) gene Dek20, which encodes phosphoglycerate dehydrogenase1 (PGDH1), the rate-limiting enzyme in the phosphorylated pathway of serine biosynthesis (PPSB). The dek20(Ser282Leu) mutation disrupts the interaction between residues Ser282 and His284, leading to the release of His284, which subsequently binds NAD+/NADH to inhibit serine biosynthesis. Consequently, serine content decreases dramatically, and the cellular response to nutrient starvation is enriched in transcriptome analysis. Serine deficiency triggers tRNASer degradation and reduced translation elongation at serine codons. The stalled ribosomes activate General Control Nonderepressible 2 (GCN2) kinase, which affects the phosphorylation of eukaryotic initiation factor 2α (eIF2α) and ribosomal protein S6 kinase (S6 K), furtherly inhibiting translation initiation. Consistent with these findings, polysome profiling and Ribo-seq analysis revealed a marked decrease in translation efficiency in dek20. Notably, proteins essential for storage compound biosynthesis and cell cycle progression exhibit reduced translation in dek20. Collectively, our findings reveal the primary serine biosynthesis pathway and a mechanism for monitoring amino acid levels in maize, the model plant with C4 photosynthesis.