CsBRC1 inhibits axillary bud outgrowth by directly repressing the auxin efflux carrier CsPIN3 in cucumber

Significance

Lateral branch suppression has been selected during crop domestication, and axillary branches need to be manually removed during fresh cucumber production. Auxin is a key repressor for shoot branching underlying apical dominance. The TEOSINTE BRANCHED1 ( TB1)/ BRANCHED1 ( BRC1) gene acts as the focal point for multiple signals to inhibit branching. However, the relationship between auxin and BRC1 remains elusive. Here cucumber BRANCHED1 (CsBRC1) is found to inhibit shoot branching by directly repressing the auxin efflux carrier CsPIN3. Compared to its wild ancestor, cultivated cucumber displays reduced branches, higher CsBRC1 expression, reduced CsPIN3 expression, and higher auxin accumulation in buds. In this study, we find a regulatory pathway of CsBRC1–CsPIN3–auxin transport in suppressing shoot branching in cucumber.

Abstract

Shoot branching is an important agronomic trait that directly determines plant architecture and affects crop productivity. To promote crop yield and quality, axillary branches need to be manually removed during cucumber production for fresh market and thus are undesirable. Auxin is well known as the primary signal imposing for apical dominance and acts as a repressor for lateral bud outgrowth indirectly. The TEOSINTE BRANCHED1/ CYCLOIDEA/PCF ( TCP) family gene BRANCHED1 ( BRC1) has been shown to be the central integrator for multiple environmental and developmental factors that functions locally to inhibit shoot branching. However, the direct molecular link between auxin and BRC1 remains elusive. Here we find that cucumber BRANCHED1 ( CsBRC1) is expressed in axillary buds and displays a higher expression level in cultivated cucumber than in its wild ancestor. Knockdown of CsBRC1 by RNAi leads to increased bud outgrowth and reduced auxin accumulation in buds. We further show that CsBRC1 directly binds to the auxin efflux carrier PIN-FORMED ( CsPIN3) and negatively regulates its expression in vitro and in vivo. Elevated expression of CsPIN3 driven by the CsBRC1 promoter results in highly branched cucumber with decreased auxin levels in lateral buds. Therefore, our data suggest that CsBRC1 inhibits lateral bud outgrowth by direct suppression of CsPIN3 functioning and thus auxin accumulation in axillary buds in cucumber, providing a strategy to breed for cultivars with varying degrees of shoot branching grown in different cucumber production systems.