Spatiotemporal Transcriptomics of Litchi Fruitlet Abscission Reveals a Compartmentalized Regulatory Network and Identifies LcERF61 as a Key Regulator

Abstract

Organ abscission is a developmental process crucial for both plant life cycles and agricultural productivity, but its spatial restriction to the tiny abscission zone (AZ) has made investigating the underlying molecular mechanisms challenging. Here, we applied spatiotemporal transcriptomics to dissect fruitlet abscission in litchi (Litchi chinensis Sonn.). This approach reveals an unexpected spatial compartmentalization of the gene regulatory landscape within the AZ. Upon attenuation of IAA polar transport, local ET, ABA, and GA pathways within the AZ core may converge to form an abscission initiation center. These signals are subsequently interpreted by spatially defined transcription factors, which translate them into domain-specific outputs and coordinate the spatiotemporal programs of cell wall remodeling. Accordingly, we show that the onset of cell degradation within the AZ begins in the central region and then extends to the outer boundary. Crucially, we functionally established LcERF61, which is strongly induced in the AZ following abscission, as a key positive regulator of fruitlet abscission. Moreover, DNA affinity purification sequencing (DAP-seq) indicated that LcERF61 directly binds to and activates the promoters of LcIDL1 (INFLORESCENCE DEFICIENT IN ABSCISSION-like) and LcIDL3, which encode small signaling peptides essential for abscission. Our findings reveal a spatially compartmentalized regulatory framework for organ abscission and establish the LcERF61-LcIDL1/3 module as a key signaling hub, providing a conceptual advance in understanding how plants execute precise organ abscission.