Light Controls Cytokinin Signaling via Transcriptional Regulation of Constitutively Active Sensor Histidine Kinase CKI1

Abstract

In plants, the multistep phosphorelay (MSP) pathway mediates a range of regulatory processes, including those activated by cytokinins. The cross talk between cytokinin response and light has been known for a long time. However, the molecular mechanism underlying the interaction between light and cytokinin signaling remains elusive. In the screen for upstream regulators we identified a <i>LONG PALE HYPOCOTYL</i> (<i>LPH</i>) gene whose activity is indispensable for spatiotemporally correct expression of <i>CYTOKININ INDEPENDENT1</i> (<i>CKI1</i>), encoding the constitutively active sensor His kinase that activates MSP signaling. <i>lph</i> is a new allele of <i>HEME OXYGENASE1</i> (<i>HY1</i>) that encodes the key protein in the biosynthesis of phytochromobilin, a cofactor of photoconvertible phytochromes. Our analysis confirmed the light-dependent regulation of the <i>CKI1</i> expression pattern. We show that <i>CKI1</i> expression is under the control of phytochrome A (phyA), functioning as a dual (both positive and negative) regulator of <i>CKI1</i> expression, presumably via the phyA-regulated transcription factors (TF) PHYTOCHROME INTERACTING FACTOR3 and CIRCADIAN CLOCK ASSOCIATED1. Changes in <i>CKI1</i> expression observed in <i>lph</i>/<i>hy1</i>-<i>7</i> and <i>phy</i> mutants correlate with misregulation of MSP signaling, changed cytokinin sensitivity, and developmental aberrations that were previously shown to be associated with cytokinin and/or CKI1 action. Besides that, we demonstrate a novel role of phyA-dependent <i>CKI1</i> expression in the hypocotyl elongation and hook development during skotomorphogenesis. Based on these results, we propose that the light-dependent regulation of <i>CKI1</i> provides a plausible mechanistic link underlying the well-known interaction between light- and cytokinin-controlled plant development.