Iso‐anchorene is an endogenous metabolite that inhibits primary root growth in Arabidopsis

Abstract

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.

Carotenoid-derived bioactive metabolites shape plant root architecture to adapt to the rhizospheric environments

“…In addition, several newly identified bioactive apocarotenoids were demonstrated as important plant root growth regulators. Retinal, which was previously characterized as key precursor of vitamin A in mammals, is identified as conserved endogenous signal in Arabidopsis to regulate periodic oscillatory lateral root initiation ( Figure 1 ) ( Dickinson et al., 2021 ); anchorene is specifically involved in anchor root formation in Arabidopsis ( Figure 1 ) ( Jia et al., 2019b ); β-cyclocitral and iso-anchorene affect root apical meristem to regulate primary root growth in Arabidopsis ( Figure 1 ) ( Dickinson et al., 2019 ; Jia et al., 2021a ); while zaxinone was shown to affects root biomass and nutrient utilization efficiency in rice ( Wang et al., 2019 ). Obviously, carotenoid-derived bioactive metabolites play essential roles underground to regulate root growth and development.…”

“…Both SLs and ABA are derived from carotenoids, which are a class of isopronoid photosynthesis pigments and act as precursors of a serial of bioactive molecules ( Schwartz et al., 1997 ; Alder et al., 2012 ). Most recently, several endogenous carotenoid-derived metabolites are identified as new regulators of root growth and development in plants, such as β-cyclocitral ( Dickinson et al., 2019 ), anchorene ( Jia et al., 2019b ), iso-anchorene ( Jia et al., 2021a ), zaxinone ( Wang et al., 2019 ) and retinal ( Dickinson et al., 2021 ). Therefore, it seems that carotenoids and carotenoid-derived metabolites play intriguingly essential roles in root development and shaping RSA.…”

Ultrahigh‐Performance Liquid Chromatography–Mass Spectrometry Analysis of Carotenoid‐Derived Hormones and Apocarotenoids in Plants

“…UAE is widely used in the extraction of different subclasses of APOs from biological material owing to its high efficiency and facile operation (Mi et al., 2018; Mi, Jia, Balakrishna, & Al‐Babili, 2020; Mi, Jia, Balakrishna, Feng, & Al‐Babili, 2019; Mi, Jia, Balakrishna, Wang, & Al‐Babili, 2019). SPE is also frequently applied for the purification of APOs, ABA, and SLs to reduce the matrix effect on detection of these metabolites (Jia, Mi, Ali, et al., 2021; Mi, Jia, Balakrishna, Feng, et al., 2019; Wang et al., 2019). At present, hybrid techniques combining different chromatography separation techniques and MS are widely used in the separation and detection of APOs in complex mixtures such as plant extracts.…”

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

“…They are prone to be cleaved by reactive oxygen species (ROS) and/or by CAROTENOID CLEAVAGE DIOXYGENASE (CCD), resulting in a diverse family of important metabolites, apocarotenoids, that include precursors of the phytohormones abscisic acid (ABA; e.g., xanthoxin) and strigolactones (Schwartz et al, 1997;Giuliano et al, 2003;Alder et al, 2012;Nisar et al, 2015;Baz et al, 2018;Jia et al, 2018). In addition, recent findings show that apocarotenoids act as growth regulators (e.g., b-cyclocitral, anchorene, iso-anchorene, and zaxinone) and stress-related signaling molecules (e.g., b-cyclocitral and b-cyclocitric acid) in plants (Ablazov et al, 2020;D'Alessandro et al, 2019;Dickinson et al, 2019;Jia et al, 2019;Jia et al, 2021;Ramel et al, 2012;Wang et al, 2019). ABA was first identified in the 1960s as a growth inhibitor that accumulates in abscising cotton fruits (Ohkuma et al, 1963).…”