Hunting for carotenoid-derived retrograde signals that regulate plastid development
Creators: name: Hou, Xin
Publisher: name: Canberra, ACT : The Australian National University
Year: 2018
Subjects: Apocarotenoid Signal, cis-Carotenoid, Plastid Development, Prolamellar Body, Photomorphogenesis

description: In plants, carotenoids are essential for photosynthesis and photoprotection. However, carotenoids are not the end-products of the pathway: apocarotenoids are produced by carotenoid cleavage dioxygenases (CCDs) or non-enzymatic processes. Apocarotenoids are more soluble or volatile than carotenoids, but they are not simply breakdown products as there can be modifications post cleavage and functions include hormones, volatiles or signals. Evidence is emerging for a class of apocarotenoids herein referred to as Apocarotenoid Signals (ACSs) that have regulatory roles throughout plant development beyond those ascribed to ABA and strigolactone. In the present study, we provide evidence that ACS2, a cis-carotenoid-derived retrograde signal, regulates plastid development during both skotomorphogenesis and photomorphogenesis. cis-carotenoids produced early in the carotenoid pathway may serve as substrates for the production of novel ACSs that regulate nuclear gene expression, metabolic homeostasis and leaf development. When and where they accumulate and what physiological functions they may serve in higher plants remain unclear. cis-carotenoids are not easily detected in most plant tissues, except in the absence of carotenoid isomerase (CRTISO) activity when photoisomerisation rate-limits the isomerisation of tetra-cis to all-trans-lycopene. The accumulation of cis-carotenoids in Arabidopsis crtiso mutant (carotenoid and chloroplast regulation 2, ccr2) tissues was observed in plant tissues grown under extended darkness (i.e. shorter photoperiod) and coincided with a perturbation in chloroplast development that caused leaf yellowing. A forward genetic screen identified an epistatic interaction between the ζ-carotene isomerase (ziso) and ccr2 which could restore plastid development, and revealed that di-cis-ζ-carotene, tri-cis-neurosporene and tetra-cis-lycopene are likely substrates for the generation of an ACS, named ACS2. Transcriptomics analysis of ccr2 ziso mutant tissues revealed that photosynthesis associated nuclear gene expression (PhANG) was activated through the down-regulation of genes involved in repressing photomorphogenesis. We identified an alternative splice mutant of det1, a repressor of photomorphogenesis, which could restore PLB formation and cotyledon greening following de-etiolation in ccr2. Chemical inhibition of carotenoid cleavage dioxygenase activity provided evidence that ACS2 posttranscriptionally maintains protochlorophyllide oxidoreductase (POR) protein levels acting downstream of DET1 to control PLB formation and plastid development. Phytoene synthase (PSY) is a major rate-controlling enzyme that catalyses the initial step of carotenoid biosynthesis and is hence under multi-level regulation. Alteration of PSY gene expression, protein levels or enzyme activity can exert profound effects on carotenoid composition and plant development. Here we show that four mutants of PSY: psy-4, psy-90, psy-130 and psy-145 reduced cis-carotenoids to levels below a threshold and suppressed ACS2 which negatively regulates plastid development in ccr2. The restoration of plastid development in the four ccr2 psy double mutants was caused by decreased PSY activity and reduced protein levels due to altered PSY-AtOR (ORANGE) interaction, but not by changed localization of PSY. This study reveals a novel role of PSY, modulating carotenoid-derived retrograde signals and regulating plastid development.