Carotenoid cleavage dioxygenases (CCDs) form hormones and signaling molecules. Here we show that a member of an overlooked plant CCD subfamily from rice, that we name Zaxinone Synthase (ZAS), can produce zaxinone, a novel apocarotenoid metabolite in vitro. Loss-of-function mutants (zas) contain less zaxinone, exhibit retarded growth and showed elevated levels of strigolactones (SLs), a hormone that determines plant architecture, mediates mycorrhization and facilitates infestation by root parasitic weeds, such as Striga spp. Application of zaxinone can rescue zas phenotypes, decrease SL content and release and promote root growth in wild-type seedlings. In conclusion, we show that zaxinone is a key regulator of rice development and biotic interactions and has potential for increasing crop growth and combating Striga, a severe threat to global food security.
Summary Carotenoids are isoprenoid compounds synthesized by all photosynthetic and some non‐photosynthetic organisms. They are essential for photosynthesis and contribute to many other aspects of a plant's life. The oxidative breakdown of carotenoids gives rise to the formation of a diverse family of essential metabolites called apocarotenoids. This metabolic process either takes place spontaneously through reactive oxygen species or is catalyzed by enzymes generally belonging to the CAROTENOID CLEAVAGE DIOXYGENASE family. Apocarotenoids include the phytohormones abscisic acid and strigolactones (SLs), signaling molecules and growth regulators. Abscisic acid and SLs are vital in regulating plant growth, development and stress response. SLs are also an essential component in plants’ rhizospheric communication with symbionts and parasites. Other apocarotenoid small molecules, such as blumenols, mycorradicins, zaxinone, anchorene, β‐cyclocitral, β‐cyclogeranic acid, β‐ionone and loliolide, are involved in plant growth and development, and/or contribute to different processes, including arbuscular mycorrhiza symbiosis, abiotic stress response, plant–plant and plant–herbivore interactions and plastid retrograde signaling. There are also indications for the presence of structurally unidentified linear cis‐carotene‐derived apocarotenoids, which are presumed to modulate plastid biogenesis and leaf morphology, among other developmental processes. Here, we provide an overview on the biology of old, recently discovered and supposed plant apocarotenoid signaling molecules, describing their biosynthesis, developmental and physiological functions, and role as a messenger in plant communication.
Natural compounds capable of increasing root depth and branching are desirable tools for enhancing stress tolerance in crops. We devised a sensitized screen to identify natural metabolites capable of regulating root traits in Arabidopsis. β-Cyclocitral, an endogenous root compound, was found to promote cell divisions in root meristems and stimulate lateral root branching. β-Cyclocitral rescued meristematic cell divisions in ccd1ccd4 biosynthesis mutants, and β-cyclocitral–driven root growth was found to be independent of auxin, brassinosteroid, and reactive oxygen species signaling pathways. β-Cyclocitral had a conserved effect on root growth in tomato and rice and generated significantly more compact crown root systems in rice. Moreover, β-cyclocitral treatment enhanced plant vigor in rice plants exposed to salt-contaminated soil. These results indicate that β-cyclocitral is a broadly effective root growth promoter in both monocots and eudicots and could be a valuable tool to enhance crop vigor under environmental stress.
Saffron is the dried stigmas of and is the most expensive spice in the world. Its red color is due to crocins, which are apocarotenoid glycosides that accumulate in the vacuole to a level up to 10% of the stigma dry weight. Previously, we characterized the first dedicated enzyme in the crocin biosynthetic pathway, carotenoid cleavage dioxygenase2 (CsCCD2), which cleaves zeaxanthin to yield crocetin dialdehyde. In this work, we identified six putative () genes expressed in stigmas. Heterologous expression in showed that only one of corresponding proteins (CsALDH3I1) was able to convert crocetin dialdehyde into the crocin precursor crocetin. CsALDH3I1 carries a carboxyl-terminal hydrophobic domain, similar to that of the membrane-associated apocarotenoid dehydrogenase YLO-1. We also characterized the UDP-glycosyltransferase CsUGT74AD1, which converts crocetin to crocins 1 and 2'. In vitro assays revealed high specificity of CsALDH3I1 for crocetin dialdehyde and long-chain apocarotenals and of CsUGT74AD1 for crocetin. Following extract fractionation, CsCCD2, CsALDH3I1, and CsUGT74AD1 were found in the insoluble fraction, suggesting their association with membranes or large insoluble complexes. Analysis of protein localization in both stigmas and following transgene expression in leaves revealed that CsCCD2, CsALDH3I, and CsUGT74AD1 were localized to the plastids, the endoplasmic reticulum, and the cytoplasm, respectively, in association with cytoskeleton-like structures. Based on these findings and current literature, we propose that the endoplasmic reticulum and cytoplasm function as transit centers for metabolites whose biosynthesis starts in the plastid and are accumulated in the vacuole.
Anchor roots (ANRs) arise at the root-shoot junction and are the least investigated type of Arabidopsis root. Here, we show that ANRs originate from pericycle cells in an auxin-dependent manner and a carotenogenic signal to emerge. By screening known and assumed carotenoid derivatives, we identified anchorene, a presumed carotenoid-derived dialdehyde (diapocarotenoid), as the specific signal needed for ANR formation. We demonstrate that anchorene is an Arabidopsis metabolite and that its exogenous application rescues the ANR phenotype in carotenoid-deficient plants and promotes the growth of normal seedlings. Nitrogen deficiency resulted in enhanced anchorene content and an increased number of ANRs, suggesting a role of this nutrient in determining anchorene content and ANR formation. Transcriptome analysis and treatment of auxin reporter lines indicate that anchorene triggers ANR formation by modulating auxin homeostasis. Together, our work reveals a growth regulator with potential application to agriculture and a new carotenoid-derived signaling molecule.
Arabidopsis AtD27 catalyzes the reverse isomerization of all-trans-/9-cis-βcarotene and carotenes with unmodified -ionone ring. Using pAtD27:NLS-GUS lines and qRT-PCR assays, we show that AtD27 expression is regulated by auxin, ABA and phosphate availability. We provide evidence for the isomerization activity in planta and for a role of AtD27 in determining shoots ABA content.
SUMMARY Because carotenoids act as accessory pigments in photosynthesis, play a key photoprotective role and are of major nutritional importance, carotenogenesis has been a target for crop improvement. Although carotenoids are important precursors of phytohormones, previous genetic manipulations reported little if any effects on biomass production and plant development, but resulted in specific modifications in carotenoid content. Unexpectedly, the expression of the carrot lycopene β‐cyclase (DcLCYB1) in Nicotiana tabacum cv. Xanthi not only resulted in increased carotenoid accumulation, but also in altered plant architecture characterized by longer internodes, faster plant growth, early flowering and increased biomass. Here, we have challenged these transformants with a range of growth conditions to determine the robustness of their phenotype and analyze the underlying mechanisms. Transgenic DcLCYB1 lines showed increased transcript levels of key genes involved in carotenoid, chlorophyll, gibberellin (GA) and abscisic acid (ABA) biosynthesis, but also in photosynthesis‐related genes. Accordingly, their carotenoid, chlorophyll, ABA and GA contents were increased. Hormone application and inhibitor experiments confirmed the key role of altered GA/ABA contents in the growth phenotype. Because the longer internodes reduce shading of mature leaves, induction of leaf senescence was delayed, and mature leaves maintained a high photosynthetic capacity. This increased total plant assimilation, as reflected in higher plant yields under both fully controlled constant and fluctuating light, and in non‐controlled conditions. Furthermore, our data are a warning that engineering of isoprenoid metabolism can cause complex changes in phytohormone homeostasis and therefore plant development, which have not been sufficiently considered in previous studies.
The emerging field of sphingolipidomics calls for accurate quantitative analyses of sphingolipidome. Existing analytical methods for sphingolipid (SPL) profiling often suffer from isotopic/isomeric interference, leading to the low-abundance, but biologically important SPLs being undetected. In the current study, we have developed an improved sphingolipidomic approach for reliable and sensitive quantification of up to 10 subclasses of cellular SPLs. By integratively utilizing high efficiency chromatographic separation, quadrupole time-of-flight (Q-TOF) and triple quadrupole (QQQ) mass spectrometry (MS), our approach facilitated unambiguous identification of several groups of potentially important but low-abundance SPLs that are usually masked by isotopic/isomeric species and hence largely overlooked in many published methods. The methodology, which featured a modified sample preparation and optimized MS parameters, permitted the measurement of 86 individual SPLs in PC12 cells in a single run, demonstrating great potential for high throughput analysis. The improved characterization, along with increased sensitivity for low-abundance SPL species, resulted in the highest number of SPLs being quantified in a single run in PC12 cells. The improved method was fully validated and applied to a lipidomic study of PC12 cell samples with or without amyloid β peptide (Aβ) treatment, which presents a most precise and genuine sphingolipidomic profile of the PC12 cell line. The adoption of the metabolomics protocol, as described in this study, could avoid misidentification and bias in the measurement of the analytically challenging low-abundance endogenous SPLs, hence achieving informative and reliable sphingolipidomics data relevant to discovery of potential SPL biomarkers for Aβ-induced neurotoxicity and neurodegenerative disease.
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