Initiation of aboveground organ primordia depends on combined action of auxin, ERECTA family genes, and PINOID

Abstract

Leaves and flowers are produced by the shoot apical meristem (SAM) at a certain distance from its center, a process that requires the hormone auxin. The amount of auxin and the pattern of its distribution in the initiation zone determine the size and spatial arrangement of organ primordia. Auxin gradients in the SAM are formed by PIN-FORMED (PIN) auxin efflux carriers whose polar localization in the plasma membrane depends on the protein kinase PINOID (PID). Previous work determined that ERECTA family genes (ERfs) control initiation of leaves. ERfs are plasma membrane receptors that enable cell-to-cell communications by sensing extracellular small proteins from Epidermal Patterning Factor/EPF-like (EPF/EPFL) family. Here, we investigate whether ERfs regulate initiation of organs by altering auxin distribution or signaling. Genetic and pharmacological data suggest that ERfs do not regulate organogenesis through PINs while transcriptomics data show ERfs do not alter primary transcriptional responses to auxin. Our results indicate that in the absence of ERf signaling, the peripheral zone cells inefficiently initiate leaves in response to auxin signals and that increased accumulation of auxin in the er erl1 erl2 SAM can partially rescue organ initiation defects. We propose that both auxin and ERfs are essential for leaf initiation, and that they have common downstream targets. Genetic data also indicate that the role of PID in initiation of cotyledons and leaves cannot be attributed solely to regulation of PIN polarity, and PID is likely to have other functions in addition to regulation of auxin distribution.