Abstract. Carotenoids are natural isoprenoid pigments that provide leaves, fruits, vegetables and flowers with distinctive yellow, orange and some reddish colours as well as several aromas in plants. Their bright colours serve as attractants for pollination and seed dispersal. Carotenoids comprise a large family of C 40 polyenes and are synthesised by all photosynthetic organisms, aphids, some bacteria and fungi alike. In animals carotenoid derivatives promote health, improve sexual behaviour and are essential for reproduction. As such, carotenoids are commercially important in agriculture, food, health and the cosmetic industries. In plants, carotenoids are essential components required for photosynthesis, photoprotection and the production of carotenoid-derived phytohormones, including ABA and strigolactone. The carotenoid biosynthetic pathway has been extensively studied in a range of organisms providing an almost complete pathway for carotenogenesis. A new wave in carotenoid biology has revealed implications for epigenetic and metabolic feedback control of carotenogenesis. Developmental and environmental signals can regulate carotenoid gene expression thereby affecting carotenoid accumulation. This review highlights mechanisms controlling (1) the first committed step in phytoene biosynthesis, (2) flux through the branch to synthesis of a-and b-carotenes and (3) metabolic feedback signalling within and between the carotenoid, MEP and ABA pathways.
Carotenoid pigments are critical for plant survival, and carotenoid composition is tuned to the developmental stage, tissue, and to environmental stimuli. We report the cloning of the CAROTENOID CHLOROPLAST REGULATORY1 (CCR1) gene. The ccr1 mutant has increased shoot branching and altered carotenoid composition, namely, reduced lutein in leaves and accumulation of cis-carotenes in dark-grown seedlings. The CCR1 gene was previously isolated as EARLY FLOWERING IN SHORT DAYS and encodes a histone methyltransferase (SET DOMAIN GROUP 8) that methylates histone H3 on Lys 4 and/or 36 (H3K4 and H3K36). ccr1 plants show reduced trimethyl-H3K4 and increased dimethyl-H3K4 surrounding the CAROT-ENOID ISOMERASE (CRTISO) translation start site, which correlates with low levels of CRTISO mRNA. Microarrays of ccr1 revealed the downregulation of 85 genes, including CRTISO and genes associated with signaling and development, and upregulation of just 28 genes. The reduction in CRTISO transcript abundance explains the altered carotenoid profile. The changes in shoot branching are additive with more axillary branching mutants, but the altered carotenoid profile may partially affect shoot branching, potentially by perturbed biosynthesis of the carotenoid substrates of strigolactones. These results are consistent with SDG8 regulating shoot meristem activity and carotenoid biosynthesis by modifying the chromatin surrounding key genes, including CRTISO. Thus, the level of lutein, the most abundant carotenoid in higher plants that is critical for photosynthesis and photoprotection, appears to be regulated by a chromatin modifying enzyme in Arabidopsis thaliana.
In addition to acting as photoprotective compounds, carotenoids also serve as precursors in the biosynthesis of several phytohormones and proposed regulatory signals. Here, we report a signaling process derived from carotenoids that regulates early chloroplast and leaf development. Biosynthesis of the signal depends on z-carotene desaturase activity encoded by the z-CAROTENE DESATURASE (ZDS)/CHLOROPLAST BIOGENESIS5 (CLB5) gene in Arabidopsis thaliana. Unlike other carotenoiddeficient plants, zds/clb5 mutant alleles display profound alterations in leaf morphology and cellular differentiation as well as altered expression of many plastid-and nucleus-encoded genes. The leaf developmental phenotypes and gene expression alterations of zds/clb5/spc1/pde181 plants are rescued by inhibitors or mutations of phytoene desaturase, demonstrating that phytofluene and/or z-carotene are substrates for an unidentified signaling molecule. Our work further demonstrates that this signal is an apocarotenoid whose synthesis requires the activity of the carotenoid cleavage dioxygenase CCD4.
Endosperm carotenoid content in wheat is a primary determinant of flour colour and this affects both the nutritional value of the grain and its utility for different applications. Utilising wheat rice synteny two genes, epsilon-cyclase (epsilon-LCY) and phytoene synthase (Psy-A1), were identified as candidate genes for two of the QTL affecting lutein content in wheat endosperm. Analysis of the sequence changes in epsilon-LCY and Psy-A1 revealed possible causal mechanisms for both QTL. A point mutation in epsilon-LCY results in the substitution of a conserved amino acid in the high lutein allele. This substitution has been observed in high lutein-accumulating species from the Gentiales order. In Psy-A1, a sequence duplication at the end of exon 2 creates a new splice site and causes alternative splicing of the transcript and activation of a cryptic exon, resulting in four different transcripts: a wild-type transcript, two transcripts with early terminations and a transcript that would produce an in-frame, albeit longer protein. Only the wild-type splice variant produced an enzymatically active protein and its mRNA abundance was reduced by titration with the other splice variants. This reduction in wild-type mRNA is argued to result in a reduction in PSY protein and thus carotenoid content in wheat.
Organelle-nuclear retrograde signaling regulates gene expression, but its roles in specialized cells and integration with hormonal signaling remain enigmatic. Here we show that the SAL1-PAP (3′-phosphoadenosine 5′- phosphate) retrograde pathway interacts with abscisic acid (ABA) signaling to regulate stomatal closure and seed germination in Arabidopsis. Genetically or exogenously manipulating PAP bypasses the canonical signaling components ABA Insensitive 1 (ABI1) and Open Stomata 1 (OST1); priming an alternative pathway that restores ABA-responsive gene expression, ROS bursts, ion channel function, stomatal closure and drought tolerance in ost1-2. PAP also inhibits wild type and abi1-1 seed germination by enhancing ABA sensitivity. PAP-XRN signaling interacts with ABA, ROS and Ca2+; up-regulating multiple ABA signaling components, including lowly-expressed Calcium Dependent Protein Kinases (CDPKs) capable of activating the anion channel SLAC1. Thus, PAP exhibits many secondary messenger attributes and exemplifies how retrograde signals can have broader roles in hormone signaling, allowing chloroplasts to fine-tune physiological responses.DOI: http://dx.doi.org/10.7554/eLife.23361.001
In plants, continuous formation of lateral roots (LRs) facilitates efficient exploration of the soil environment. Roots can maximize developmental capacity in variable environmental conditions through establishment of sites competent to form LRs. This LR prepattern is established by a periodic oscillation in gene expression near the root tip. The spatial distribution of competent (prebranch) sites results from the interplay between this periodic process and primary root growth; yet, much about this oscillatory process and the formation of prebranch sites remains unknown. We find that disruption of carotenoid biosynthesis results in seedlings with very few LRs. Carotenoids are further required for the output of the LR clock because inhibition of carotenoid synthesis also results in fewer sites competent to form LRs. Genetic analyses and a carotenoid cleavage inhibitor indicate that an apocarotenoid, distinct from abscisic acid or strigolactone, is specifically required for LR formation. Expression of a key carotenoid biosynthesis gene occurs in a spatially specific pattern along the root's axis, suggesting spatial regulation of carotenoid synthesis. These results indicate that developmental prepatterning of LRs requires an uncharacterized carotenoid-derived molecule. We propose that this molecule functions non-cell-autonomously in establishment of the LR prepattern.root development | patterning | secondary metabolite synthesis A nchorage and uptake of water and soluble nutrients are essential functions of plant root systems and key to plant productivity and survival. The capacity of a root system to carry out these functions can be maximized by iterative root branching. Root branches are formed de novo during primary root growth, which allows for the elaboration of a complex root system that effectively enables the plant to navigate and exploit the resources of diverse, locally variable subterranean environments. Understanding the developmental mechanisms underlying the pattern of root branches has broad significance in both basic and applied research.As with other dicotyledonous plants, formation of a complex root system in the model plant Arabidopsis thaliana (Arabidopsis) occurs through iterative production of branches, or lateral roots (LRs), from the primary root. The simplified root system of Arabidopsis has yielded considerable insight into the cellular events and molecular regulators required for LR formation (recently reviewed in refs.
SUMMARYOne of the most stress-responsive genes encoding a mitochondrial protein in Arabidopsis (At3g50930) has been annotated as AtBCS1 (cytochrome bc1 synthase 1), but was previously functionally uncharacterised. Here, we show that the protein encoded by At3g50930 is present as a homo-multimeric protein complex on the outer mitochondrial membrane and lacks the BCS1 domain present in yeast and mammalian BCS1 proteins, with the sequence similarity restricted to the AAA ATPase domain. Thus we propose to re-annotate this protein as AtOM66 (Outer Mitochondrial membrane protein of 66 kDa). While transgenic plants with reduced AtOM66 expression appear to be phenotypically normal, AtOM66 over-expression lines have a distinct phenotype, showing strong leaf curling and reduced starch content. Analysis of mitochondrial protein content demonstrated no detectable changes in mitochondrial respiratory complex protein abundance. Consistent with the stress inducible expression pattern, over-expression lines of AtOM66 are more tolerant to drought stress but undergo stress-induced senescence earlier than wild type. Genome-wide expression analysis revealed a constitutive induction of salicylic acid-related (SA) pathogen defence and cell death genes in over-expression lines. Conversely, expression of SA marker gene PR-1 was reduced in atom66 plants, while jasmonic acid response genes PDF1.2 and VSP2 have increased transcript abundance. In agreement with the expression profile, AtOM66 over-expression plants show increased SA content, accelerated cell death rates and are more tolerant to the biotrophic pathogen Pseudomonas syringae, but more susceptible to the necrotrophic fungus Botrytis cinerea. In conclusion, our results demonstrate a role for AtOM66 in cell death and amplifying SA signalling.
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