The G-protein β subunit SlGB1 regulates tyramine-derived phenolamide metabolism for shoot apex growth and development in tomato.

Abstract

The shoot apex is a critical determinant of plant growth, development, morphology, and yield. The G-protein β subunit (Gβ) is an essential regulator of apical meristem dynamics, yet its precise mechanism of action remains unclear, with notable interspecific variation. This study reveals that in the dicot tomato (Solanum lycopersicum), Gβ subunit mutants (Slgb1) display abnormal shoot morphogenesis and, in severe cases, shoot apex death. Such a phenotype has also been observed in monocot species, like maize (Zea mays) and rice (Oryza sativa), but not in the model dicot Arabidopsis (Arabidopsis thaliana). Using integrated multiomics and liquid chromatography-mass spectrometry, we identified a significant upregulation in tyramine-derived phenolamides in Slgb1 mutants, particularly N-p-trans-coumaroyltyramine (N-P-CT) and N-trans-feruloyltyramine (N-FT). Biochemical and genetic assays pinpointed tyramine hydroxycinnamoyl transferases (THTs) as the enzymes catalyzing N-P-CT and N-FT biosynthesis, with THT8 overexpression inducing shoot apex death. Comparative genomic analysis revealed the presence of a THT-mediated tyramine-derived phenolamide metabolic pathway in species exhibiting gb1 mutant-associated apex death, which is notably absent in Arabidopsis. Protein interaction assays showed that SlGB1 interacts with bHLH79 at the cell membrane and cytoplasm, thereby attenuating the bHLH79-MYB10 interaction within the nucleus, leading to altered THT expression and phenolamide biosynthesis. This study unravels the molecular mechanisms by which SlGB1 governs tomato shoot apex growth and development, highlighting interspecific differences critical for developing breeding strategies aimed at optimizing shoot apex architecture.