Abstract

Exquisitely regulated plastid-to-nucleus communication by retrograde signaling pathways is essential for fine-tuning of responses to the prevailing environmental conditions. The plastidial retrograde signaling metabolite methylerythritol cyclodiphosphate (MEcPP) has emerged as a stress signal transduced into a diverse ensemble of response outputs. Here, we demonstrate enhanced phytochrome B protein abundance in red light-grown MEcPP-accumulating ceh1 mutant Arabidopsis (Arabidopsis thaliana) plants relative to wild-type seedlings. We further establish MEcPP-mediated coordination of phytochrome B with auxin and ethylene signaling pathways and uncover differential hypocotyl growth of red light-grown seedlings in response to these phytohormones. Genetic and pharmacological interference with ethylene and auxin pathways outlines the hierarchy of responses, placing ethylene epistatic to the auxin signaling pathway. Collectively, our findings establish a key role of a plastidial retrograde metabolite in orchestrating the transduction of a repertoire of signaling cascades. This work positions plastids at the zenith of relaying information coordinating external signals and internal regulatory circuitry to secure organismal integrity.

Highlights

  • Dynamic alignment of internal and external cues through activation of corresponding signal transduction pathways is a defining characteristic of organisms essential for fitness and the balancing act of metabolic investment in growth versus adaptive responses

  • Through a forward genetic screen, we identified a bifunctional plastid-produced metabolite methylerythritol cyclodiphosphate (MEcPP) that serves as a precursor of isoprenoids produced by the plastidial methylerythritol phosphate (MEP) pathway and functions as a stress-specific retrograde signaling metabolite (Xiao et al, 2012)

  • Given the stunted hypocotyl phenotype of high MEcPP-accumulating mutant plant, we explored the nature of the photoreceptor involved by examining hypocotyl length of seedlings grown in the dark and under various monochromatic light conditions

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Summary

Introduction

Dynamic alignment of internal and external cues through activation of corresponding signal transduction pathways is a defining characteristic of organisms essential for fitness and the balancing act of metabolic investment in growth versus adaptive responses. The integrity of these responses is achieved through finely controlled communication circuitry, notably retrograde (organelle-to-nucleus) signaling cascades. We established that regulation of growth is in part via MEcPP-mediated modulation of levels and distribution patterns of auxin (IAA) through dual transcriptional and post-translational regulatory inputs (Jiang et al, 2018)

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