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The interconnected action of cytokinins and ethylene in the control of plant growth was demonstrated. However, the extent of the crosstalk and the underlying molecular mechanisms remained mostly elusive. We and others’ have demonstrated that multistep phosphorelay (MSP) pathway, previously thought mainly to mediate cytokinin signaling, is under control of ethylene through the histidine kinase (HK) activity of ethylene sensor ETR1. Here we show that although ETR1 is an active HK, its receiver domain (ETR1RD) is structurally and functionally unable to accept the phosphate from the phosphorylated His in the ETR1 HK domain (ETR1HK) to initiate the phosphorelay to AHPs, the next downstream link in MSP signaling. Instead, ETR1 interacts with another HK AHK5 and transfers the phosphate from ETR1HK through the receiver domain of AHK5 (AHK5RD), and subsequently to AHP1, AHP2 and AHP3, independently of the HK activity of AHK5. We show that AHK5 is necessary for ethylene-initiated, but not cytokinin-initiated, MSP signaling in planta and is involved in the hormonal control of root growth and architecture in Arabidopsis. Furthermore, we have identified novel mechanism of transcriptional regulation based on the interaction of members of ethylene and MSP signaling pathways in the spatial-specific control of cytokinin-induced ethylene biosynthesis, mediating the cytokinin-induced, ethylene- regulated root growth. We propose that the aforementioned regulatory network represents a molecular basis for the existence of previously proposed morphogenic field combining the properties of both cytokinins and ethylene, controlling, together with auxin, root growth and patterning.