Loss of StLOX2a confers an optimized semi-dwarf plant architecture without tuber yield penalty under controlled growth conditions in potato

Plant architecture is an important agronomic trait in potato, which is closely related to regional adaptation and cultivation fitness for yield optimization. Here, we identified an optimized semi-dwarf mutant, sd6–23, from a potato T-DNA mutant population, with reduced internode length but increased internode thickness and leaf area without tuber weight penalty under controlled growth conditions. Loss of StLOX2a, which encodes a member of the 13-lipoxygenase family, was identified for sd6–23 by whole-genome resequencing and CRISPR/Cas9 approaches. StLOX2a is predominantly expressed in leaves, and its protein is localized to the chloroplast. The loss of StLOX2a resulted in an increase in the number of leaf epidermal cells and stem pith parenchyma cells, but a decrease in the length of stem epidermal cells. Integrated transcriptome and hormone analyses in leaves and stems revealed that 1) StLOX2a mediates the biosynthesis of jasmonates (JAs), which antagonize cytokinins (CKs) biosynthesis to modulate leaf cell division; 2) alterations in gibberellins (GAs) and CKs biosynthesis, as well as JAs homeostasis, may coordinately regulate stem epidermal cell elongation and pith parenchyma cell division, which could account for the shorter and thicker internodes observed in lox2a mutants. Furthermore, the shortened internode phenotype of lox2a mutants was restored by the exogenous application of GA3. Thus, the loss of StLOX2a achieved plant height reduction while preserving larger leaves, thereby maintaining stable tuber yield. Manipulation of StLOX2a may represent a new strategy to optimize plant architecture for better adaptation to regional environments and cultivation modes in potato breeding.