A novel hydroxycinnamoyl transferase for synthesis of hydroxycinnamoyl spermine conjugates in plants

Abstract

Background Hydroxycinnamoyl-spermine conjugates (HCSpm) are a class of hydroxycinnamic acid amides (HCAAs), which not only are instrumental in plant development and stress response, but also benefit human health. However, HCSpm are not commonly produced in plants, and the mechanism of their biosynthesis remains unclear. In previous investigations of phenolics in Solanum fruits related to eggplant ( Solanum melongena L.), we discovered that Solanum richardii , an African wild relative of eggplant, was rich in HCSpms in fruits. Results The putative spermine hydroxycinnamoyl transferase (HT) SpmHT was isolated from S. richardii and eggplant. SrSpmHT expression was high in flowers and fruit, and was associated with HCSpm accumulation in S. richardii ; however, SpmHT was hardly detected in eggplant cultivars and other wild relatives. Recombinant SpmHT exclusively selected spermine as the acyl acceptor substrate, while showing donor substrate preference in the following order: caffeoyl-CoA, feruloyl-CoA, and p -coumaroyl-CoA. Molecular docking revealed that substrate binding pockets of SpmHT could properly accommodate spermine but not the shorter, more common spermidine. Conclusion SrSpmHT is a novel spermine hydroxycinnamoyl transferase that uses Spm exclusively as the acyl acceptor substrate to produce HCSpms. Our findings shed light on the HCSpm biosynthetic pathway that may allow an increase of health beneficial metabolites in Solanum crops via methods such as introgression or engineering HCAA metabolism. Electronic supplementary material The online version of this article (10.1186/s12870-019-1846-3) contains supplementary material, which is available to authorized users.

Phenolamides in plants: an update on their function, regulation, and origin of their biosynthetic enzymes

“…These enzymes use diverse amine acceptors. OsAHT1 and OsPHT3 are specific for agmatine like HvACT, whereas HvTHT2, HvTHT7, and HvTHT8 are specific for tryptamine and OsTHT1, OsTHT2, OsTBT1, and OsTBT2 acylate tryptamine, serotonin, and tyramine (Burhenne et al, 2003;Tanabe et al, 2016;Ube et al, 2019b;Peng et al, 2019). The ability of several ACT-like to use tyramine and serotonin as substrates underlines a convergent evolution for tyramine and serotonin derived phenolamide synthesis in both Monocotyledons and Solanaceae using BAHD or GNAT acyltransferases, respectively (Peng et al, 2016).…”

“…ACT-like isoforms are differentially expressed. Some are constitutively expressed in roots, flowers, or seedlings, whereas others are inducible upon pathogen challenge given defensive or developmental roles, depending on the phenolamide produced (Burhenne et al, 2003;Tanabe et al, 2016;Peng et al, 2019;Ube et al, 2019b).…”

“…The three clusters may result from convergent evolution in distinct higher plants (Fig. 5); cluster Os12g27220 is restricted to Poales (Dong et al, 2015), cluster NaDH29 is restricted to Solanales (Onkokesung et al, 2012;Peng et al, 2019), and cluster AtSDT seems more widely distributed among Rosids (Luo et al, 2009). Therefore, mono-and di-hydroxycinnamoyl spermidines/spermines are reported in a lot of plants but seems to originate from multi-convergent evolution, highlighting the importance of these compounds in plants, although their functions are poorly understood.…”

“…Therefore, mono-and di-hydroxycinnamoyl spermidines/spermines are reported in a lot of plants but seems to originate from multi-convergent evolution, highlighting the importance of these compounds in plants, although their functions are poorly understood. Expression profiles of enzymes between and within the three groups are not conserved but widely detected in various tissues, including seedlings, roots, leaves, flowers, fruits, and under herbivory attacks (Luo et al, 2009;Onkokesung et al, 2012;Dong et al, 2015;Peng et al, 2019).…”

A SmelAAT Acyltransferase Variant Causes a Major Difference in Eggplant (Solanum melongena L.) Peel Anthocyanin Composition

“…A blast search of the SmelAAT sequence (from '67/3', GeneBank submission Id 2424224) against the '67/3' eggplant genome in NCBI and Sol Genomics databases allowed us to identify putative acyltransferase amino acid sequences from S. melongena, Solanum lycopersicum, Solanum tuberosum, Capsicum annuum, and Petunia axillaris, which were used to obtain a molecular phylogenetic tree (Figure 2, File S1). Some of the sequences analyzed were identified as corresponding to previously described BAHD acyltransferases [33] with known function: SlAT2 (NP_001266253, Solyc01g10 5580), capable of acyl sucrose acetylation [34], SmSpmHT (SMEL_010g340090) with sper-mine hydroxycinnamoyl transferase activity [35], and SlFdAT1 (NP_00134419, Solyc12g088170), acting as a flavonoid-3-O-rutinoside-4 -O-phenylacyl transferase [36].…”