Multimodal single cell analysis reveals a link between flowering and leaf initiation
TL;DR
Surprisingly, id1- te1- plants exhibited a synergistic floral delay, producing ∼90 leaves before inflorescence production, raising the hypothesis that meristem leaf primordia cessation underpins maize flowering.
Abstract
Zea mays (maize) flowering time is genetically determined and a critical yield determinant. Yet mechanistic understanding of maize flowering remains poor. Indeterminate1 (Id1), a zinc-finger transcription factor (TF), is a monocot-conserved master regulator of maize flowering. Epistasis between Id1 and the ZeaCentroradialis-Delayed Flowering1 (Zcn-Dlf1) inductive pathway partly explains ID1 floral control; however, the strong mutant id1- floral delay is not explained by this pathway alone. To better characterize Id1 actions, we performed single-cell assay for transposase-accessible chromatin and single nucleus RNA sequencing (scATAC-seq and snRNA-seq) comparing Id1+ and id1- developing leaves. These analyses reveal id1- chromatin remodeling via TEOSINTE BRANCHED1 CYCLOIDEA PROLIFERATING CELL FACTOR (TCP) and APETALA2/ETHYLENE RESPONSEFACTOR (AP2/ERF) transcription factors and provide candidate direct targets that include AP2/ERF genes. These candidate direct targets include the family of β-glucosidase genes that lose expression in id1-. Unexpectedly, CRISPR/Cas9 β-glucosidase edits produced plants that phenocopied terminal ear1- (te1-) mutants. This phenocopy prompted an investigation into the genetic relationship between id1-, te1- and flowering. Surprisingly, id1- te1- plants exhibited a synergistic floral delay, producing ∼90 leaves before inflorescence production. Beyond highlighting hitherto unappreciated Te1 autonomous flowering roles, this genetic synergy raises the hypothesis that meristem leaf primordia cessation underpins maize flowering.
