Single‐nucleus transcriptomic atlas reveals autophagy and hormone signaling in early grapevine ( Vitis vinifera L.) tendril versus inflorescence determination

Understanding the early specification of tendrils versus inflorescences in grapevine is key for developmental biology and agricultural applications. Here, we performed a comparative anatomical and cyto-histological analysis of lateral buds from the tendril-prone cultivar "Pinot Noir" ("PN") and the inflorescence-prone cultivar "Einset Seedless" ("EinS"). Our results show that cytological differences between tendril and inflorescence primordia emerge early during floral initiation, prior to any visible structural divergence. In particular, rib zone (RZ) cells in the uncommitted lateral meristem (UM) of "PN" differentiated into vacuolated pith cells more rapidly than those in "EinS." We subsequently applied single-nucleus RNA sequencing (snRNA-seq) to 50 052 nuclei from lateral buds of both cultivars, generating a cell type-resolved transcriptional atlas. Reconstruction of shoot apical meristem (SAM) and UM developmental trajectories revealed accelerated SAM differentiation in "PN." Together with cyto-histological observations of a less abundant UM mantle zone and lower cell cycle gene activity in UM cells, these findings indicate that both accelerated SAM differentiation and reduced UM proliferative activity restrict complete inflorescence formation in "PN," which is consistent with the anatomical differences observed. Analyzing UM and inflorescence meristem differentiation trajectories distinguished inflorescences- and tendril-specific differentiation trajectories, and revealed the involvement of the autophagy and hormone signal transduction pathway in early tendril versus inflorescence determination. Furthermore, transcription factors from the GRF, B3, S1Fa-like, WRKY, GATA, and C2H2 families showed expression patterns correlated with tendril specification. These results provide key insights into the differentiation of homologous reproductive structures in grapevine, thereby advancing the theoretical framework for early tendril versus inflorescence specification and supporting future applied research.