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SUMMARY: Carotenoids are isoprenoid pigments indispensable for photosynthesis. Moreover, they are the precursor of apocarotenoids, which include the phytohormones abscisic acid (ABA) and strigolactones (SLs) as well as retrograde signaling molecules and growth regulators, such as β‐cyclocitral and zaxinone. Here, we show that the application of the volatile apocarotenoid β‐ionone (β‐I) to Arabidopsis plants at micromolar concentrations caused a global reprogramming of gene expression, affecting thousands of transcripts involved in stress tolerance, growth, hormone metabolism, pathogen defense, and photosynthesis. This transcriptional reprogramming changes, along with induced changes in the level of the phytohormones ABA, jasmonic acid, and salicylic acid, led to enhanced Arabidopsis resistance to the widespread necrotrophic fungus Botrytis cinerea (B.c.) that causes the gray mold disease in many crop species and spoilage of harvested fruits. Pre‐treatment of tobacco and tomato plants with β‐I followed by inoculation with B.c. confirmed the effect of β‐I in increasing the resistance to this pathogen in crop plants. Moreover, we observed reduced susceptibility to B.c. in fruits of transgenic tomato plants overexpressing LYCOPENE β‐CYCLASE, which contains elevated levels of endogenous β‐I, providing a further evidence for its effect on B.c. infestation. Our work unraveled β‐I as a further carotenoid‐derived regulatory metabolite and indicates the possibility of establishing this natural volatile as an environmentally friendly bio‐fungicide to control B.c. Significance Statement: Plants rely on a wide range of metabolites to coordinate their growth and to respond to environmental stimuli. The family of carotenoid‐cleavage products, apocarotenoids, is emerging as a source of growth‐regulating and signaling molecules conferring protection against abiotic and biotic stresses. We show that the apocarotenoid, β‐ionone, is a regulatory metabolite that reshapes Arabidopsis transcriptome and hormone content, increasing resistance to the necrotrophic fungus Botrytis cinerea (B.c.) in Arabidopsis, tobacco and tomato plants. [ABSTRACT FROM AUTHOR]

SUMMARY: The enzyme DWARF27 (D27) catalyzes the reversible isomerization of all‐trans‐ into 9‐cis‐β‐carotene, initiating strigolactone (SL) biosynthesis. Genomes of higher plants encode two D27‐homologs, D27‐like1 and ‐like2, with unknown functions. Here, we investigated the enzymatic activity and biological function of the Arabidopsis D27‐like1. In vitro enzymatic assays and expression in Synechocystis sp. PCC6803 revealed an unreported 13‐cis/15‐cis/9‐cis‐ and a 9‐cis/all‐trans‐β‐carotene isomerization. Although disruption of AtD27‐like1 did not cause SL deficiency phenotypes, overexpression of AtD27‐like1 in the d27 mutant restored the more‐branching phenotype, indicating a contribution of AtD27‐like1 to SL biosynthesis. Accordingly, generated d27 d27like1 double mutants showed a more pronounced branching phenotype compared to d27. The contribution of AtD27‐like1 to SL biosynthesis is likely a result of its formation of 9‐cis‐β‐carotene that was present at higher levels in AtD27‐like1 overexpressing lines. By contrast, AtD27‐like1 expression correlated negatively with the content of 9‐cis‐violaxanthin, a precursor of ABA, in shoots. Consistently, ABA levels were higher in shoots and also in dry seeds of the d27like1 and d27 d27like1 mutants. Transgenic lines expressing GUS driven by the AtD27LIKE1 promoter and transcript analysis of hormone‐treated Arabidopsis seedlings revealed that AtD27LIKE1 is expressed in different tissues and affects ABA and auxin. Taken together, our work reports a cis/cis‐β‐carotene isomerase that affects the content of both cis‐carotenoid‐derived plant hormones, ABA and SLs. Significance Statement: AtD27LIKE1 is involved in the biosynthesis of the two carotenoid‐derived plant hormones ABA and strigolactones (SLs), by feeding SL biosynthesis at the same time as negatively impacting ABA content. [ABSTRACT FROM AUTHOR]

Summary: Carotenoid‐derived regulatory metabolites and hormones are generally known to arise through the oxidative cleavage of a single double bond in the carotenoid backbone, which yields mono‐carbonyl products called apocarotenoids. However, the extended conjugated double bond system of these pigments predestines them also to repeated cleavage forming dialdehyde products, diapocarotenoids, which have been less investigated due to their instability and low abundance. Recently, we reported on the short diapocarotenoid anchorene as an endogenous Arabidopsis metabolite and specific signaling molecule that promotes anchor root formation. In this work, we investigated the biological activity of a synthetic isomer of anchorene, iso‐anchorene, which can be derived from repeated carotenoid cleavage. We show that iso‐anchorene is a growth inhibitor that specifically inhibits primary root growth by reducing cell division rates in the root apical meristem. Using auxin efflux transporter marker lines, we also show that the effect of iso‐anchorene on primary root growth involves the modulation of auxin homeostasis. Moreover, by using liquid chromatography–mass spectrometry analysis, we demonstrate that iso‐anchorene is a natural Arabidopsis metabolite. Chemical inhibition of carotenoid biosynthesis led to a significant decrease in the iso‐anchorene level, indicating that it originates from this metabolic pathway. Taken together, our results reveal a novel carotenoid‐derived regulatory metabolite with a specific biological function that affects root growth, manifesting the biological importance of diapocarotenoids. [ABSTRACT FROM AUTHOR]

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. Significance Statement: Apocarotenoids are carotenoid‐derived small molecules with regulatory functions, including cellular signaling, growth regulation and communication with surrounding organisms. Owing to these functions, apocarotenoids can influence plant physiology, development and plant–plant/plant–microorganisms interactions, making them a major focus of study in agriculture and fundamental research. [ABSTRACT FROM AUTHOR]

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. Significance Statement: Carotenoids are involved in processes such photosynthesis and photoprotection, and precursors of signaling molecules, including the phytohormones strigolactones and abscisic acid. Gibberellin biosynthesis shares isoprenoid precursors with the carotenoids. Therefore, manipulation of carotenoid biosynthesis could influence hormone content and thus plant development and physiology. Here we show how the expression of carrot lycopene β‐cyclase1 modulates gibberellin and abscisic acid content resulting in altered plant architecture, increased biomass and photosynthetic efficiency. [ABSTRACT FROM AUTHOR]