BpLAZY1A Mediates Transcriptional Polarity and Drives Adaxial Tension Wood Like Tissue Formation in Silver Birch (Betula pendula) Branches

Abstract

A defining feature of most trees is the architectural distinction between a vertically growing main stem and laterally growing branches. This growth habit increases fitness by increasing photosynthetically active surface area and shading competitors. Here, we studied the weeping birch cultivar Betula pendula Youngii to uncover the mechanisms that maintain lateral branch growth. We identified a loss-of-function mutation in BpLAZY1A, a core component of the gravitropic signalling pathway, as the cause of the weeping phenotype. Forward genetic analysis demonstrated that the weeping phenotype is recessive in silver birch. Transgenic BpLAZY1A RNAi lines phenocopied Youngii, confirming the functional role of BpLAZY1A. Reporter analysis revealed that BpLAZY1A is expressed predominantly in gravity-sensing starch sheath cells, with occasional expression in the main stem phloem. Time lapse imaging revealed two distinct gravitropic responses during branch development - an early response associated with establishment of the branch apex gravitropic set-point angle, and a later response associated with polar reinforcement at the branch base. The main stem retained normal gravitropic responses in BpLAZY1A RNAi lines, indicating a branch-specific role for BpLAZY1A. Integrative analyses combining transcriptomics, chemical profiling, and histochemistry indicated that BpLAZY1A establishes adaxial-abaxial polarity during early branch development. In wild-type branches, pectin-rich tension wood-like tissue formed preferentially in the adaxial xylem, accompanied by adaxial expression of pectin- and tension wood-associated genes, including BpRRT1 and BpCOBRA-LIKE4. Auxin-related genes, including BpIAA29 and BpSAURs, were preferentially upregulated in the abaxial side. This transcriptional asymmetry was reduced in BpLAZY1A RNAi line 1, where tension wood-like tissue formed in both adaxial and abaxial sides of the xylem, indicating a loss of polarity. Together, these findings demonstrate that BpLAZY1A functions specifically in branch gravitropism and links spatially asymmetric gene expression with branch growth orientation and biomechanical reinforcement. Our results identify BpLAZY1A as a key regulator coordinating gravitropic signalling, tissue polarity, and the developmental biomechanics underlying lateral branch growth.