A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development

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.

Spatial Nano-Morphology of the Prolamellar Body in Etiolated Arabidopsis thaliana Plants With Disturbed Pigment and Polyprenol Composition

“…Surprisingly, although the carotenoid composition is severely affected in the ccr1-1 plants ( Figure 4 ), the PLB in this mutant is fully developed and regularly arranged ( Figures 5 , 7 ). It was previously established that in the ccr2 plants, the formation of PLB is completely arrested ( Park et al, 2002 ; Cazzonelli et al, 2020 ). Such fact was attributed to the accumulation of cis -carotenes – p-Lyc and pro-neurosporene in particular.…”

“…Carotenoids form another group of molecules that are highly abundant in the PLB membrane fraction. Their structural role in the PLB formation was demonstrated in the PLB-deficient ccr2 mutant, which accumulates particular poly -cis carotenoids and maintains wild type levels of LPOR and Pchlide ( Park et al, 2002 ; Cuttriss et al, 2007 ; Cazzonelli et al, 2020 ). In the ccr2 mutant, restoration of the PLB structure is possible due to further mutations in the ζ-carotene isomerase (ZISO) pointing directly to the role of the cis -carotenoid component in the PLB structure development ( Cazzonelli et al, 2020 ).…”

“…Their structural role in the PLB formation was demonstrated in the PLB-deficient ccr2 mutant, which accumulates particular poly -cis carotenoids and maintains wild type levels of LPOR and Pchlide ( Park et al, 2002 ; Cuttriss et al, 2007 ; Cazzonelli et al, 2020 ). In the ccr2 mutant, restoration of the PLB structure is possible due to further mutations in the ζ-carotene isomerase (ZISO) pointing directly to the role of the cis -carotenoid component in the PLB structure development ( Cazzonelli et al, 2020 ). However, because carotenoids are a large and diverse group of the lipophilic pigments, the role of other molecules from this group in the PLB formation cannot be excluded and remains to be studied.…”

Light‐limited photosynthesis under energy‐saving film decreases eggplant yield

“…Plants respond to light intensity, spectral quality, and photoperiod (Babla et al., 2019; Ballaré & Pierik, 2017; Cazzonelli et al., 2020; Poorter et al., 2019). At the leaf level, blue photons are used less efficiently than orange and red photons in photosynthesis (Bugbee, 2016; Inada, 1976; McCree, 1971).…”

Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells

“…In addition, specific metabolites have been identified that accumulate under stress, such as the dinucleotide 3 0 -phosphoadenosine-5 0 -phosphate (PAP) [36] and the isoprenoid precursor MEcPP [37]. Furthermore, an apocarotenoid-dependent signal was recently identified that is required for proper plastid development [39]. All these metabolites are much more stable than ROS and could be actively transported across the chloroplast envelope, diffuse through the cytosol and induce appropriate responses in the nucleus.…”