Heterometric expression of an LBD gene via LBD-TCP assembly regulates floral organ size and fruit weight in Physalis

Plant LATERAL ORGAN BOUNDARIES DOMAIN (LBD) family is crucial for defining organ boundaries and participates in various developmental processes, but its role in fruit weight has rarely been elucidated. Here, we characterized an LBD gene, <i>Physalis organ size 3</i> (<i>POS3</i>), in <i>Physalis floridana</i>, designated as <i>PfPOS3</i>. This gene exhibited high expression levels in floral meristems, carpels, and developing seeds and fruits when compared to <i>Solanum pimpinellifolium</i> and <i>Solanum lycopersicum</i>. The floral organ size, seed weight, and mature fruit weight were significantly reduced in <i>PfPOS3</i> knockdown and knockout plants. Consistent with overexpression analyses, <i>PfPOS3</i> promoted cell size and inhibited cell division during berry development. Moreover, overexpression of <i>PfPOS3</i> and <i>SlPOS3</i> shared identical phenotypic variation in transgenic Physalis plants. Both PfPOS3 and SlPOS3 interacted with Teosinte branched1/Cycloidea/Proliferating cell factor 15 (TCP15) and TCP18, and the POS3-TCP modules directly regulated the expression of <i>Cyclin D1;1</i> (<i>CYCD1;1</i>) and <i>CYCB1;1</i>. Overall, POS3 may have the capability to orchestrate cell number and cell size, thus regulating fruit weight variation within Solanaceae. However, a significant reduction in the expression of <i>SlPOS3</i> may result in a pronounced weakening or complete loss of this function within <i>Solanum</i>. Our findings shed new light on the reproductive organ size control, the developmental evolution of fruit morphology, and the breeding of Physalis crops.