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      Plant apocarotenoids: from retrograde signaling to interspecific communication

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          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.

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          Most cited references247

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          Strigolactone inhibition of shoot branching.

          A carotenoid-derived hormonal signal that inhibits shoot branching in plants has long escaped identification. Strigolactones are compounds thought to be derived from carotenoids and are known to trigger the germination of parasitic plant seeds and stimulate symbiotic fungi. Here we present evidence that carotenoid cleavage dioxygenase 8 shoot branching mutants of pea are strigolactone deficient and that strigolactone application restores the wild-type branching phenotype to ccd8 mutants. Moreover, we show that other branching mutants previously characterized as lacking a response to the branching inhibition signal also lack strigolactone response, and are not deficient in strigolactones. These responses are conserved in Arabidopsis. In agreement with the expected properties of the hormonal signal, exogenous strigolactone can be transported in shoots and act at low concentrations. We suggest that endogenous strigolactones or related compounds inhibit shoot branching in plants. Furthermore, ccd8 mutants demonstrate the diverse effects of strigolactones in shoot branching, mycorrhizal symbiosis and parasitic weed interaction.
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            Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi.

            Arbuscular mycorrhizal (AM) fungi form mutualistic, symbiotic associations with the roots of more than 80% of land plants. The fungi are incapable of completing their life cycle in the absence of a host root. Their spores can germinate and grow in the absence of a host, but their hyphal growth is very limited. Little is known about the molecular mechanisms that govern signalling and recognition between AM fungi and their host plants. In one of the first stages of host recognition, the hyphae of AM fungi show extensive branching in the vicinity of host roots before formation of the appressorium, the structure used to penetrate the plant root. Host roots are known to release signalling molecules that trigger hyphal branching, but these branching factors have not been isolated. Here we have isolated a branching factor from the root exudates of Lotus japonicus and used spectroscopic analysis and chemical synthesis to identify it as a strigolactone, 5-deoxy-strigol. Strigolactones are a group of sesquiterpene lactones, previously isolated as seed-germination stimulants for the parasitic weeds Striga and Orobanche. The natural strigolactones 5-deoxy-strigol, sorgolactone and strigol, and a synthetic analogue, GR24, induced extensive hyphal branching in germinating spores of the AM fungus Gigaspora margarita at very low concentrations.
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              Inhibition of shoot branching by new terpenoid plant hormones.

              Shoot branching is a major determinant of plant architecture and is highly regulated by endogenous and environmental cues. Two classes of hormones, auxin and cytokinin, have long been known to have an important involvement in controlling shoot branching. Previous studies using a series of mutants with enhanced shoot branching suggested the existence of a third class of hormone(s) that is derived from carotenoids, but its chemical identity has been unknown. Here we show that levels of strigolactones, a group of terpenoid lactones, are significantly reduced in some of the branching mutants. Furthermore, application of strigolactones inhibits shoot branching in these mutants. Strigolactones were previously found in root exudates acting as communication chemicals with parasitic weeds and symbiotic arbuscular mycorrhizal fungi. Thus, we propose that strigolactones act as a new hormone class-or their biosynthetic precursors-in regulating above-ground plant architecture, and also have a function in underground communication with other neighbouring organisms.
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                Author and article information

                Contributors
                salim.babili@kaust.edu.sa
                Journal
                Plant J
                Plant J
                10.1111/(ISSN)1365-313X
                TPJ
                The Plant Journal
                John Wiley and Sons Inc. (Hoboken )
                0960-7412
                1365-313X
                08 January 2021
                January 2021
                : 105
                : 2 ( doiID: 10.1111/tpj.v105.2 )
                : 351-375
                Affiliations
                [ 1 ] Max Planck Institut für Molekulare Pflanzenphysiologie Am Mühlenberg 1 Potsdam 14476 Germany
                [ 2 ] Division of Biological and Environmental Sciences and Engineering Center for Desert Agriculture the BioActives Lab King Abdullah University of Science and Technology Thuwal 23955‐6900 Kingdom of Saudi Arabia
                [ 3 ] Hawkesbury Institute for the Environment Western Sydney University Locked Bag 1797 Penrith NSW 2751 Australia
                Author notes
                [*] [* ] For correspondence (e‐mail salim.babili@ 123456kaust.edu.sa ).

                Author information
                https://orcid.org/0000-0001-9722-5262
                https://orcid.org/0000-0001-7846-9472
                https://orcid.org/0000-0001-5081-6874
                https://orcid.org/0000-0003-4823-2882
                Article
                TPJ15102
                10.1111/tpj.15102
                7898548
                33258195
                156542bd-d046-4b61-8745-0ff6ded3a242
                © 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 12 August 2020
                : 12 November 2020
                : 19 November 2020
                Page count
                Figures: 7, Tables: 0, Pages: 25, Words: 57265
                Funding
                Funded by: King Abdullah University of Science and Technology , open-funder-registry 10.13039/501100004052;
                Award ID: CRG2017
                Categories
                SI Phytohormones 2021
                Plant Hormone Functions and Interactions in Biological Systems
                Custom metadata
                2.0
                January 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.9.7 mode:remove_FC converted:22.02.2021

                Plant science & Botany
                abscisic acid,anchorene,apocarotenoids,β‐cyclocitral,β‐ionone,lcdas,carotenoids,strigolactones,volatiles,zaxinone

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