A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development.

Christopher I Cazzonelli,John Rivers,Namraj Dhami,Yagiz Alagoz,Xin Hou,Jiwon Lee,Barry J Pogson,Shashikanth Marri

doi:10.7554/elife.45310

Christopher I Cazzonelli, John Rivers + Show 6 more

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https://doi.org/10.7554/elife.45310

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Journal: eLife	Publication Date: Jan 31, 2020
Citations: 50	License type: CC BY 4.0

Affiliation: Australian National University, Western Sydney University

Abstract

Carotenoids are a core plastid component and yet their regulatory function during plastid biogenesis remains enigmatic. A unique carotenoid biosynthesis mutant, carotenoid chloroplast regulation 2 (ccr2), that has no prolamellar body (PLB) and normal PROTOCHLOROPHYLLIDE OXIDOREDUCTASE (POR) levels, was used to demonstrate a regulatory function for carotenoids and their derivatives under varied dark-light regimes. A forward genetics approach revealed how an epistatic interaction between a ζ-carotene isomerase mutant (ziso-155) and ccr2 blocked the biosynthesis of specific cis-carotenes and restored PLB formation in etioplasts. We attributed this to a novel apocarotenoid retrograde signal, as chemical inhibition of carotenoid cleavage dioxygenase activity restored PLB formation in ccr2 etioplasts during skotomorphogenesis. The apocarotenoid acted in parallel to the repressor of photomorphogenesis, DEETIOLATED1 (DET1), to transcriptionally regulate PROTOCHLOROPHYLLIDE OXIDOREDUCTASE (POR), PHYTOCHROME INTERACTING FACTOR3 (PIF3) and ELONGATED HYPOCOTYL5 (HY5). The unknown apocarotenoid signal restored POR protein levels and PLB formation in det1, thereby controlling plastid development.

Highlights

Carotenoids are a diverse group of hydrophobic isoprenoid pigments required for numerous biological processes in photosynthetic organisms and are essential for human health (Cazzonelli, 2011; Baranski and Cazzonelli, 2016)
We demonstrate how an unidentified apocarotenoid signal acted in parallel to DET1 to control prolamellar body (PLB) formation as well as PROTOCHLOROPHYLLIDE OXIDOREDUCTASE (POR), PHYTOCHROME INTERACTING FACTOR3 (PIF3) and HY5 transcript levels, thereby fine-tuning plastid development in tissues exposed to extended periods of darkness
Far red light treatment of etiolated seedlings represses PORA activity, while the synthesis of Pchlide continues without conversion into chlorophyllide

Summary

Introduction

Carotenoids are a diverse group of hydrophobic isoprenoid pigments required for numerous biological processes in photosynthetic organisms and are essential for human health (Cazzonelli, 2011; Baranski and Cazzonelli, 2016). In addition to providing plant flowers, fruits and seeds with distinct colours, carotenoids have accessory roles in facilitating the assembly of the light harvesting complex, light capture during photosynthesis and photoprotection during high light and/or temperature stress (Nisar et al, 2015; Baranski and Cazzonelli, 2016). The current frontiers are to discover the regulators of carotenoid biosynthesis, storage, and catabolism and apocarotenoids that in turn regulate plant development and photosynthesis (Cazzonelli and Pogson, 2010; Havaux, 2014; Baranski and Cazzonelli, 2016; Hou et al, 2016).

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