The Path from β-Carotene to Carlactone, a Strigolactone-Like Plant Hormone

Abstract

Strigolactones, phytohormones with diverse signaling activities, have a common structure consisting of two lactones connected by an enol-ether bridge. Strigolactones derive from carotenoids via a pathway involving the carotenoid cleavage dioxygenases 7 and 8 (CCD7 and CCD8) and the iron-binding protein D27. We show that D27 is a β-carotene isomerase that converts all-trans-β-carotene into 9-cis-β-carotene, which is cleaved by CCD7 into a 9-cis-configured aldehyde. CCD8 incorporates three oxygens into 9-cis-β-apo-10'-carotenal and performs molecular rearrangement, linking carotenoids with strigolactones and producing carlactone, a compound with strigolactone-like biological activities. Knowledge of the structure of carlactone will be crucial for understanding the biology of strigolactones and may have applications in combating parasitic weeds.

Nitro-Phenlactone, a Carlactone Analog with Pleiotropic Strigolactone Activities

“…Canonical SLs are divided into strigol-and orobanchol-like subfamilies with a typical structure consisting of a tricyclic (ABC-ring) and a monocyclic lactone (D-ring), which are connected by an enol ether bridge ( Figure 1A and Supplemental Figure 1). SLs are synthesized from carotenoids via carlactone, which lacks the B/C-ring (Alder et al, 2012). In Arabidopsis, carlactone ( Figure 1A) is converted by MAX1, a member of CYP711 family, into carlactonoic acid that can, after methylation, bind to SL receptor (Abe et al, 2014).…”

“…Previously, we showed that carlactone exerts activities of canonical SLs by suppressing the high-tillering phenotype of the SL-deficient rice mutant d10 and inducing seed germination in Striga seeds (Alder et al, 2012). Herein, we describe the design of a new compound, Nitro-Phenlactone (N-PL) ( Figure 1A), which is based on the relatively simple structure of carlactone, and that was synthesized in four steps yielding a racemic mixture consisting of a 5'R-and a 5'S-configured stereoisomers (Supplemental Figure 1, 2).…”

Strigolactones fine-tune the root system

“…Next, plastidic carotenoid cleavage dioxygenases 7 and 8 (CCD7 and CCD8 encoded, respectively, by MAX3 and MAX4 in Arabidopsis; Fig. 1) produce carlactone (Alder et al 2012). Carlactone (or another derived intermediate) is then transported to the cytosol where it is possibly converted to strigolactones by MAX1 that encodes a cytoplasmic cytochrome P450 enzyme (Booker et al 2005;Waters et al 2012).…”

On the substrate‐ and stereospecificity of the plant carotenoid cleavage dioxygenase 7

“…Plant carotenoids also differ in their stereo-configuration and occur all-trans configured as well as in different cis-isomeric forms like 9-cis-violaxanthin and 9-cis-b-carotene, the precursors of abscisic acid and SLs, respectively [15,16,24]. Like with other apocarotenoids, the synthesis of these hormones is initiated by oxidative cleavage of double bonds in carotenoid backbones, a reaction that is generally catalyzed by carotenoid cleavage oxygenases.…”

“…Considering that the E. coli strains used mainly accumulate all-trans-configured carotenoids, these results indicated that SLs are synthesized via the intermediate b-apo-13-carotenone produced by CCD7 and CCD8 from all-trans-b-carotene. However, a recent in vitro study suggested a new path to SLs via carlactone [24], a SLs-like compound that has been very recently also identified in planta [41]. This pathway starts with the D27-catalyzed isomerization of all-trans-into 9-cis-b-carotene that is cleaved by CCD7 to yield b-ionone and 9-cis-b-apo-10 0 -carotenal used by CCD8 to form carlactone, supposedly by catalyzing a combination of different reactions [24].…”