Deconvoluting apocarotenoid‐mediated retrograde signaling networks regulating plastid translation and leaf development

SUMMARY Signals originating within plastids modulate organelle differentiation by transcriptionally regulating nuclear‐encoded genes. These retrograde signals are also integral regulators of plant development, including leaf morphology. The clb5 mutant displays severe leaf morphology defects due to Apocarotenoid Signal 1 (ACS1) accumulation in the developmentally arrested plastid. Transcriptomic analysis of clb5 validates that ACS1 accumulation deregulates hundreds of nuclear genes, including the suppression of most genes encoding plastid ribosomal proteins. Herein, we order the molecular events causing the leaf phenotype associated with the accumulation of ACS1, which includes two consecutive retrograde signaling cascades. Firstly, ACS1 originating in the plastid drives inhibition of plastid translation (IPT) via nuclear transcriptome remodeling of chlororibosomal proteins, requiring light as an essential component. Subsequently, IPT results in leaf morphological defects via a GUN1‐dependent pathway shared with seedlings undergoing chemical IPT treatments and is restricted to an early window of the leaf development. Collectively, this work advances our understanding of the complexity within plastid retrograde signaling exemplified by sequential signal exchange and consequences that in a particular temporal and spatial context contribute to the modulation of leaf development. Significance Statement Accumulation of an undefined apocarotenoid, ACS1, derived from cis‐carotenoids leads to important defects in leaf development via a previously unknown molecular mechanism. In this work we show that accumulation of ACS1 initiates a retrograde signal cascade resulting in the transcriptional modulation of diverse genes and define the molecular events involved in ACS1’s regulation of leaf development. Our work illustrates how two sequential plastidial retrograde signaling cascades modulate leaf development during a particular developmental window. These results will be instrumental in efforts to biochemically define ACS1.