An alternative, zeaxanthin epoxidase-independent abscisic acid biosynthetic pathway in plants

TitleAn alternative, zeaxanthin epoxidase-independent abscisic acid biosynthetic pathway in plants
Publication TypeArticolo su Rivista peer-reviewed
Year of Publication2022
AuthorsJia, Kun-Peng, Mi Jianing, Ali Shawkat, Ohyanagi Hajime, Moreno Juan C., Ablazov Abdugaffor, Balakrishna Aparna, Berqdar Lamis, Fiore Alessia, Diretto Gianfranco, Martínez Claudio, de Lera Angel R., Gojobori Takashi, and Al-Babili Salim
JournalMolecular Plant
Volume15
Issue1
Pagination151 - 166
Date PublishedJan-01-2022
ISSN16742052
Keywordsabscisic acid, Arabidopsis, biosynthesis, Biosynthetic Pathways, comparative study, drug effect, gene expression regulation, Genes, Genetic Variation, genetics, genotype, metabolism, oxidoreductase, Oxidoreductases, Plant, plant gene
Abstract

Abscisic acid (ABA) is an important carotenoid-derived phytohormone that plays essential roles in plant response to biotic and abiotic stresses as well as in various physiological and developmental processes. In Arabidopsis, ABA biosynthesis starts with the epoxidation of zeaxanthin by the ABA DEFICIENT 1 (ABA1) enzyme, leading to epoxycarotenoids; e.g., violaxanthin. The oxidative cleavage of 9-cis-epoxycarotenoids, a key regulatory step catalyzed by 9-CIS-EPOXYCAROTENOID DIOXYGENASE, forms xanthoxin, which is converted in further reactions mediated by ABA DEFICIENT 2 (ABA2), ABA DEFICIENT 3 (ABA3), and ABSCISIC ALDEHYDE OXIDASE 3 (AAO3) into ABA. By combining genetic and biochemical approaches, we unravel here an ABA1-independent ABA biosynthetic pathway starting upstream of zeaxanthin. We identified the carotenoid cleavage products (i.e., apocarotenoids, β-apo-11-carotenal, 9-cis-β-apo-11-carotenal, 3-OH-β-apo-11-carotenal, and 9-cis-3-OH-β-apo-11-carotenal) as intermediates of this ABA1-independent ABA biosynthetic pathway. Using labeled compounds, we showed that β-apo-11-carotenal, 9-cis-β-apo-11-carotenal, and 3-OH-β-apo-11-carotenal are successively converted into 9-cis-3-OH-β-apo-11-carotenal, xanthoxin, and finally into ABA in both Arabidopsis and rice. When applied to Arabidopsis, these β-apo-11-carotenoids exert ABA biological functions, such as maintaining seed dormancy and inducing the expression of ABA-responsive genes. Moreover, the transcriptomic analysis revealed a high overlap of differentially expressed genes regulated by β-apo-11-carotenoids and ABA, suggesting that β-apo-11-carotenoids exert ABA-independent regulatory activities. Taken together, our study identifies a biological function for the common plant metabolites, β-apo-11-carotenoids, extends our knowledge about ABA biosynthesis, and provides new insights into plant apocarotenoid metabolic networks. © 2021 The Authors

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DOI10.1016/j.molp.2021.09.008
Short TitleMolecular Plant