Local and distal signals drive cell-type-specific leaf responses during shade avoidance

Abstract

Plants reposition and grow their leaves towards optimal light conditions in a canopy. To achieve both horizontal and vertical displacement, plants need to simultaneously elongate their cells unidirectionally and maintain an elongation rate differential between the abaxial and adaxial side of the organ to bend. Exposure to Far-Red (FR) light enrichment can induce both responses, depending on where FR is sensed. Here we studied how plants maintain both growth responses simultaneously within the same organ. To deduce the regulatory mechanisms governing the simultaneous regulation of differential and unidirectional elongation, we performed both organ specific and single cell RNA sequencing experiments on plants exposed to local or whole plant FR enrichment. Single cell transcriptomics resolved that FR light signalling occurs through all cell types, but core components of the shade avoidance pathway are expressed cell type-specifically and require signalling across tissues to control growth plasticity. The upstream photoreceptor targets, including auxin biosynthesis-associated genes, in the leaf lamina are expressed in the epidermis, whilst auxin response gene expression in the petiole occurs also in the deeper tissues layers. We thus identified the remotely triggered differential growth transcriptome acting in the abaxial cortex and show that this is complemented by locally induced second transcriptome signature that is associated with unidirectional petiole elongation. The latter is induced across all cell types. We propose that this spatial distinction of transcriptional regulation of gene clusters could represent how differential and unidirectional growth can occur simultaneously in the same organ under FR light enrichment.