Hunting for carotenoid-derived retrograde signals that regulate plastid development
Date
2018
Authors
Hou, Xin
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Canberra, ACT : The Australian National University
Abstract
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.
Description
Keywords
Apocarotenoid Signal, cis-Carotenoid, Plastid Development, Prolamellar Body, Photomorphogenesis
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DOI
10.25911/5d5143c2d6275