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SUMMARY: The apocarotenoid strigolactones (SLs) facilitate pre‐symbiotic communication between arbuscular mycorrhizal (AM) fungi and plants. Related blumenol‐C‐glucosides (blumenols), have also been associated with symbiosis, but the cues that are involved in the regulation of blumenol accumulation during AM symbiosis remain unclear. In rice, our analyses demonstrated a strict correlation between foliar blumenol abundance and intraradical fungal colonisation. More specifically, rice mutants affected at distinct stages of the interaction revealed that fungal cortex invasion was required for foliar blumenol accumulation. Plant phosphate status and D14L hormone signalling had no effect, contrasting their known role in induction of SLs. This a proportion of the SL biosynthetic enzymes, D27 and D17, are equally required for blumenol production. These results importantly clarify that, while there is a partially shared biosynthetic pathway between SL and blumenols, the dedicated induction of the related apocarotenoids occurs in response to cues acting at distinct stages during the root colonisation process. However, we reveal that neither SLs nor blumenols are essential for fungal invasion of rice roots. Significance Statement: The apocarotenoids strigolactone and blumenol are both associated with arbuscular mycorrhizal symbiosis. Servanté et al. report divergent regulation of each compound despite the partially shared biosynthetic pathway, thereby highlighting the involvement of distinct tissues and signalling cues at different stages of the interaction. [ABSTRACT FROM AUTHOR]

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: A level of redundancy and interplay among the transcriptional regulators of floral development safeguards a plant's reproductive success and ensures crop production. In the present study, an additional layer of complexity in the regulation of floral meristem (FM) identity and flower development is elucidated linking carotenoid biosynthesis and metabolism to the regulation of determinate flowering. The accumulation and subsequent cleavage of a diverse array of ζ‐carotenes in the chloroplast biogenesis 5 (clb5) mutant of Arabidopsis results in the reprogramming of meristematic gene regulatory networks establishing FM identity mirroring that of the FM identity master regulator, APETALA1 (AP1). The immediate transition to floral development in clb5 requires long photoperiods in a GIGANTEA‐independent manner, whereas AP1 is essential for the floral organ development of clb5. The elucidation of this link between carotenoid metabolism and floral development translates to tomato exposing a regulation of FM identity redundant to and initiated by AP1 and proposed to be dependent on the E class floral initiation and organ identity regulator, SEPALLATA3 (SEP3). Significance Statement: In the present study, we aimed to explore how regulation of the multi‐enzyme poly‐cis‐transformation of 15 cis‐phytoene to all trans‐lycopene, which evolved from the single enzymatic reaction in bacteria, provides a unique means to regulate various aspects of plant development. As a result, a link between carotenoid biosynthesis and metabolism and the regulation of floral meristem identity and floral organ development in Arabidopsis and tomato is uncovered. [ABSTRACT FROM AUTHOR]

SUMMARY: The Oryza sativa (rice) carotenoid cleavage dioxygenase OsZAS was described to produce zaxinone, a plant growth‐promoting apocarotenoid. A zas mutant line showed reduced arbuscular mycorrhizal (AM) colonization, but the mechanisms underlying this behavior are unknown. Here, we investigated how OsZAS and exogenous zaxinone treatment regulate mycorrhization. Micromolar exogenous supply of zaxinone rescued root growth but not the mycorrhizal defects of the zas mutant, and even reduced mycorrhization in wild‐type and zas genotypes. The zas line did not display the increase in the level of strigolactones (SLs) that was observed in wild‐type plants at 7 days post‐inoculation with AM fungus. Moreover, exogenous treatment with the synthetic SL analog GR24 rescued the zas mutant mycorrhizal phenotype, indicating that the lower AM colonization rate of zas is caused by a deficiency in SLs at the early stages of the interaction, and indicating that during this phase OsZAS activity is required to induce SL production, possibly mediated by the Dwarf14‐Like (D14L) signaling pathway. OsZAS is expressed in arbuscule‐containing cells, and OsPT11prom::OsZAS transgenic lines, where OsZAS expression is driven by the OsPT11 promoter active in arbusculated cells, exhibit increased mycorrhization compared with the wild type. Overall, our results show that the genetic manipulation of OsZAS activity in planta leads to a different effect on AM symbiosis from that of exogenous zaxinone treatment, and demonstrate that OsZAS influences the extent of AM colonization, acting as a component of a regulatory network that involves SLs. Significance Statement: OsZAS was described to produce zaxinone, a plant growth‐promoting apocarotenoid in Oryza sativa (rice). Here we demonstrate the importance of OsZAS to guarantee the correct extent of root colonization by arbuscular mycorrhizal (AM) fungi. We show that OsZAS controls the extent of AM colonization, acting as a component of a regulatory network, possibly mediated by the Dwarf14‐Like (D14L) signaling pathway, that involves SLs. [ABSTRACT FROM AUTHOR]

SUMMARY: 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. Significance Statement: Accumulation of an undefined apocarotenoid, ACS1, derived from cis‐carotenoids leads to important defects in leaf development via a previously unknown molecular mechanism. In this work we show that accumulation of ACS1 initiates a retrograde signal cascade resulting in the transcriptional modulation of diverse genes and define the molecular events involved in ACS1's regulation of leaf development. Our work illustrates how two sequential plastidial retrograde signaling cascades modulate leaf development during a particular developmental window. These results will be instrumental in efforts to biochemically define ACS1. [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]

The Arabidopsis BYPASS1 ( BPS1) gene is required for normal root and shoot development. In bps1 mutants, grafting and root excision experiments have shown that mutant roots produce a transmissible signal that is capable of arresting shoot development. In addition, we previously showed that growth of bps1 mutants on the carotenoid biosynthesis inhibitor fluridone resulted in partial rescue of both leaf and root defects. These observations suggest that a single mobile carotenoid-derived signal affects both root and shoot development. Here, we describe further characterization of the bps1 root-derived signal using genetic and biosynthetic inhibitor approaches. We characterized leaf and root development in double mutants that combined the bps1 mutant with mutants that have known defects in genes encoding carotenoid processing enzymes or defects in responses to carotenoid-derived abscisic acid. Our studies indicate that the mobile signal is neither abscisic acid nor the MAX-dependent hormone that regulates shoot branching, and that production of the signal does not require the activity of any single carotenoid cleavage dioxygenase. In addition, our studies with CPTA, a lycopene cyclase inhibitor, show that signal production requires synthesis of β-carotene and its derivatives. Furthermore, we show a direct requirement for carotenoids as signal precursors, as the GUN plastid-to-nucleus signaling pathway is not required for phenotypic rescue. Together, our results suggest that bps1 roots produce a novel mobile carotenoid-derived signaling compound. [ABSTRACT FROM AUTHOR]