Identification of novel canonical strigolactones produced by tomato

Abstract

Canonical strigolactones (SLs), such as orobanchol, consist of a tricyclic lactone ring (ABC-ring) connected to a methylbutenolide (D-ring). Tomato plants have been reported to produce not only orobanchol but also various canonical SLs related to the orobanchol structure, including orobanchyl acetate, 7-hydroxyorobanchol isomers, 7-oxoorobanchol, and solanacol. In addition to these, structurally unidentified SL-like compounds known as didehydroorobanchol isomers (DDHs), whose molecular mass is 2 Da smaller than that of orobanchol, have been found. Although the SL biosynthetic pathway in tomato is partially characterized, structural elucidation of DDHs is required for a better understanding of the entire biosynthetic pathway. In this study, three novel canonical SLs with the same molecular mass as DDHs were identified in tomato root exudates. The first was 6,7-didehydroorobanchol, while the other two were not in the DDH category. These two SLs were designated phelipanchol and epiphelipanchol because they induced the germination of Phelipanche ramosa, a noxious root parasitic weed of tomato. We also proposed a putative biosynthetic pathway incorporating these novel SLs from orobanchol to solanacol.

2-oxoglutarate-dependent dioxygenases and BAHD acyltransferases drive the structural diversification of orobanchol in Fabaceae plants

“…As previously described, SlCYP712G1 has been identified as the enzyme responsible for converting orobanchol to DDHs in tomato. The DDHs catalyzed by SlCYP712G1 likely include 6,7-didehydroorobanchol, phelipanchol, and epiphelipanchol, as indicated by their chromatographic behavior compared to authentic SLs we identified ( Wakabayashi et al., 2022 ; Wang et al., 2022 ). The elimination of the hydroxy group at the C7 position of 7-hydroxyorobanchol is presumed to be the key reaction, supported by the detection of putative 7-hydroxyorobanchol as a reaction product of SlCYP712G1 ( Wakabayashi et al., 2022 ; Wang et al., 2022 ).…”

“…Orobanchol, a major naturally occurring SL, has been detected in the root exudate of numerous plants, including monocots like rice ( Oryza sativa ) ( Zhang et al., 2014 ) and dicots such as Sonalaceae ( Wakabayashi et al., 2022 ), Fabaceae ( Ueno et al., 2011 ), Cucurbitaceae ( Khetkam et al., 2014 ), and Linaceae ( Xie et al., 2009a ). Regarding SL biosynthesis, enzyme reactions catalyzed by DWARF27 (D27), carotenoid cleavage dioxygenase 7 (CCD7), and CCD8 are known to convert all- trans -β-carotene to carlactone ( Alder et al., 2012 ).…”

“…Additionally, putative derivatives of orobanchol have been identified in the root exudates of various plants. For instance, downstream canonical SLs of orobanchol, namely 6,7-didehydroorobanchol and phelipanchols, have been identified in tomato ( Supplementary Figure S1C ) ( Wakabayashi et al., 2022 ). These orobanchol derivatives were collectively termed didehydroorobanchol isomers (DDHs), with CYP712G1 identified as the enzyme responsible for the conversion of orobanchol to DDHs in tomato ( Wang et al., 2022 ).…”

“…These orobanchol derivatives were collectively termed didehydroorobanchol isomers (DDHs), with CYP712G1 identified as the enzyme responsible for the conversion of orobanchol to DDHs in tomato ( Wang et al., 2022 ). The oxidation at the C7 position is suggested to be crucial for the conversion of orobanchol to DDHs in tomato ( Wakabayashi et al., 2022 ). Furthermore, other plants also produce orobanchol derivatives biosynthesized through oxidation at the C7 position, such as 7-α/β-hydroxyorobanchyl acetate and 7-oxoorobanchyl acetate identified in cucumber ( Cucumis sativum ) ( Khetkam et al., 2014 ) and flax ( Linum usitatissimum ) ( Xie et al., 2009a ), respectively ( Supplementary Figure S1C ).…”

Biosynthetic Pathways of Hormones in Plants

“…CLA can be treated as the precursor of strigol and orobanchol-type SL, i.e., 5-deoxystrigol (5DS) and 4-deoxyorobanchol (4DO). Enzymes identified in plants, such as Os900/OsCYP711A2 in rice ( Oryza sativa ), VuCYP722C in cowpea ( Vigna unguiculata ), SlCYP722C in tomato ( Solanum lycopersicum ), and GaCYP722C in cotton ( Gossypium arboreum ), take part in the synthesis of organic compounds 4-deoxyorobanchol, orobanchol, and 5-deoxystrigol, respectively, from CLA [ 189 , 190 , 192 , 193 , 194 ].…”