Rewired meristem regulation drives morphological evolution of the one-leaf developmental system in Monophyllaea glabra

Abstract

Plants have evolved unconventional shoot systems with a "fuzzy" character that blurs organ boundaries, but the developmental programs driving this morphological diversity remain a mystery. One-leaf plants of the genus Monophyllaea are a striking example of this diversity: they develop a single indeterminate cotyledon instead of a conventional shoot system to form a unique structural unit termed a phyllomorph. Here, we integrate tissue-specific and single-nucleus transcriptomics with spatial gene expression analyses to characterize the meristems underlying this developmental system. The Monophyllaea-specific meristem of the phyllomorph retains a conserved shoot apical meristem-like transcriptional core but has a leaf lamina program superimposed. This chimeric transcriptional state integrates normally distinct developmental programs alongside altered phytohormone regulation. The one-leaf morphology emerges through the rewiring of conserved meristem regulatory networks rather than the passive suppression of meristem activity. The findings highlight the remarkable plasticity of developmental modules in plant morphological evolution.