Cytokinins and ethylene control plant development via sensors from the histidine kinase (HK) family. However, downstream signaling pathways for the key phytohormones are distinct. Here we report that not only cytokinin but also ethylene is able to control root apical meristem (RAM) size through activation of the multistep phosphorelay (MSP) pathway. We found that both cytokinin and ethylene-dependent RAM shortening requires ethylene binding to ETR1 and the HK activity of ETR1. The receiver domain of ETR1 interacts with MSP signaling intermediates acting downstream of cytokinin receptors, further substantiating the role of ETR1 in MSP signaling. We revealed that both cytokinin and ethylene induce the MSP in similar and distinct cell types with ETR1-mediated ethylene signaling controlling MSP output specifically in the root transition zone. We identified members of the MSP pathway specific and common to both hormones and showed that ETR1-regulated ARR3 controls RAM size. ETR1-mediated MSP spatially differs from canonical CTR1/EIN2/EIN3 ethylene signaling and is independent of EIN2, indicating that both pathways can be spatially and functionally separated. Furthermore, we demonstrated that canonical ethylene signaling controls MSP responsiveness to cytokinin specifically in the root transition zone, presumably via regulation of ARR10, one of the positive regulators of MSP signaling in Arabidopsis.

Functional Genomics and Proteomics of Plants Central European Institute of Technology and National Centre for Biomolecular Research Masaryk University CETEC MU Kamenice 5 A2 625 00 Brno Czech Republic

Functional Genomics and Proteomics of Plants Central European Institute of Technology and National Centre for Biomolecular Research Masaryk University CETEC MU Kamenice 5 A2 625 00 Brno Czech Republic; Division of Biology and Biological Engineering 156 29 California Institute of Technology 1200 East California Boulevard Pasadena CA 91125 USA

Howard Hughes Medical Institute California Institute of Technology 1200 East California Boulevard Pasadena CA 91125 USA; Division of Biology and Biological Engineering 156 29 California Institute of Technology 1200 East California Boulevard Pasadena CA 91125 USA

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