Deconvoluting apocarotenoid‐mediated retrograde signaling networks regulating plastid translation and leaf development

Abstract

Signals originating within plastids modulate organelle differentiation by transcriptionally regulating nuclear-encoded genes. These retrograde signals are also integral regulators of plant development, including leaf morphology. The clb5 mutant displays severe leaf morphology defects due to Apocarotenoid Signal 1 (ACS1) accumulation in the developmentally arrested plastid. Transcriptomic analysis of clb5 validates that ACS1 accumulation deregulates hundreds of nuclear genes, including the suppression of most genes encoding plastid ribosomal proteins. Herein, we order the molecular events causing the leaf phenotype associated with the accumulation of ACS1, which includes two consecutive retrograde signaling cascades. Firstly, ACS1 originating in the plastid drives inhibition of plastid translation (IPT) via nuclear transcriptome remodeling of chlororibosomal proteins, requiring light as an essential component. Subsequently, IPT results in leaf morphological defects via a GUN1-dependent pathway shared with seedlings undergoing chemical IPT treatments and is restricted to an early window of the leaf development. Collectively, this work advances our understanding of the complexity within plastid retrograde signaling exemplified by sequential signal exchange and consequences that in a particular temporal and spatial context contribute to the modulation of leaf development.

Molecular changes of Arabidopsis thaliana plastoglobules facilitate thylakoid membrane remodeling under high light stress

“…It is unclear what may be the subsequent fate of the released carotenoids in PGs; however, studies of substrate preference of CCD4 indicate this PG‐localized enzyme can accommodate a range of carotene and xanthophyll compounds (Auldridge et al ., 2006; Bruno et al ., 2016; Ma et al ., 2013a,b; Rottet et al ., 2016; Rubio et al ., 2008). It is tempting to speculate that CCD4 turnover of carotenoids at the PG may generate apocarotenoid signaling compounds that propagate the leaf senescence process during thylakoid turnover, in light of the recent discoveries of apocarotenoid compounds with developmental signaling roles (Avendaño‐Vázquez et al ., 2014; Cazzonelli et al ., 2020; Escobar‐Tovar et al ., 2020).…”

A Foliar Pigment-Based Bioassay for Interrogating Chloroplast Signalling Reveals that Chlorophyll Biosynthesis Requires Carotenoid Isomerisation.

“…cis-carotenes have been recently proposed to act as substrates in generating an ACS that controls plastid development (e.g. etioplast, chromoplast, and chloroplast) (Avendano-Vazquez et al, 2014, Escobar-Tovar et al, 2021. Phytoene and phyto uene accumulation in response to NFZ treatment are unlikely to be signals themselves, although a burst in their production was shown to elicit arti cial chloroplast-to-chromoplast differentiation in leaves (Llorente et al, 2020).…”

“…An unidenti ed apocarotenoid signal (ACS) generated during acyclic cis-carotene biosynthesis has been shown to regulate nuclear gene expression and chloroplast biogenesis in Arabidopsis tissues (Cazzonelli et al, 2020, Avendano-Vazquez et al, 2014, Escobar-Tovar et al, 2021. The loss of ZETA-CAROTENE DESATURATE (ZDS) function causes lethality following photomorphogenesis, yet the albino seedlings accumulate cis-carotenes that were linked to the control of plastid development and formation of needlelike leaf phenotype (Dong et al, 2007, Avendano-Vazquez et al, 2014, Escobar-Tovar et al, 2021. The loss-of-function in ΖΕΤΑ−CAROTENE ISOMERASE (Z-ISO) causes cis-carotenes to accumulate in etiolated tissues and can delay chlorophyll biosynthesis during seedling photomorphogenesis (Chen et al, 2010, Beltran et al, 2015.…”

A foliar pigment-based bioassay for interrogating chloroplast signalling revealed that carotenoid isomerisation regulates chlorophyll abundance

“…An unidentified apocarotenoid signal (ACS) generated during acyclic cis -carotene biosynthesis has been shown to regulate nuclear gene expression and chloroplast biogenesis in Arabidopsis tissues [ 5 , 14 , 26 ]. The loss of ZETA-CAROTENE DESATURATE (ZDS) function causes lethality following photomorphogenesis, yet the albino seedlings accumulate cis -carotenes that were linked to the control of plastid development and formation of needle-like leaf phenotype [ 5 , 24 , 26 ]. The loss-of-function in ZETA-CAROTENE ISOMERASE (Z-ISO) causes cis -carotenes to accumulate in etiolated tissues and can delay chlorophyll biosynthesis during seedling photomorphogenesis [ 9 , 18 ].…”