Evolution of metabolic novelty: A trichome-expressed invertase creates specialized metabolic diversity in wild tomato

Abstract

Plants produce a myriad of taxonomically restricted specialized metabolites. This diversity—and our ability to correlate genotype with phenotype—makes the evolution of these ecologically and medicinally important compounds interesting and experimentally tractable. Trichomes of tomato and other nightshade family plants produce structurally diverse protective compounds termed acylsugars. While cultivated tomato (Solanum lycopersicum) strictly accumulates acylsucroses, the South American wild relative Solanum pennellii produces copious amounts of acylglucoses. Genetic, transgenic, and biochemical dissection of the S. pennellii acylglucose biosynthetic pathway identified a trichome gland cell–expressed invertase-like enzyme that hydrolyzes acylsucroses (Sopen03g040490). This enzyme acts on the pyranose ring–acylated acylsucroses found in the wild tomato but not on the furanose ring–decorated acylsucroses of cultivated tomato. These results show that modification of the core acylsucrose biosynthetic pathway leading to loss of furanose ring acylation set the stage for co-option of a general metabolic enzyme to produce a new class of protective compounds.

Candidate Gene Networks for Acylsugar Metabolism and Plant Defense in Wild Tomato Solanum pennellii

“…Genes encoding ASATs and the recently identified invertase (SpASFF1), which are involved in phase 2 of acylsugar biosynthesis (Schilmiller et al, 2015;Fan et al, 2016Fan et al, , 2017Leong et al, 2019), were upregulated in high-acylsugar-producing accessions (Table 2). ASATs use acyl-CoA molecules as their substrates (Schilmiller et al, 2012(Schilmiller et al, , 2015Fan et al, 2016Fan et al, , 2017, and free SCFAs produced by FAScatalyzed de novo fatty acid biosynthesis must be activated to their acyl-CoA derivatives (SCFA-CoA) before they can be used by ASATs ( Figure 1A).…”

“…Sopen04g001210 (marked with an asterisk) was identified as a carboxylesterase gene related to ASH (Schilmiller et al, 2016). Sopen03g040490 (marked with a double-asterisk) has been recently reported as a trichome-expressed invertase gene that is capable of producing acylglucose from acylsucrose (Leong et al, 2019). AG, acylglucose phase 2 (previous model).…”

“…Three acylsugar acyltransferases (ASATs) are involved in phase 2 of acylsucrose biosynthesis (Schilmiller et al, 2015;Fan et al, 2016Fan et al, , 2017. During the preparation of this article, an invertase (acylsucrose fructo-furanosidase1; ASFF1) was reported to be capable of producing acylglucose from acylsucrose (Leong et al, 2019). Previous biochemical studies reported a UDP-glucose:fatty acid glucosyltransferase (UDP-Glc:FA GT; Ghangas and Steffens, 1993;Kuai et al, 1997) and a serine carboxypeptidase-like glucose acyltransferase (SCPL GAT; Li et al, 1999;Li and Steffens, 2000) that initiate acylglucose biosynthesis in S. pennellii (Supplemental Figure 1).…”

Location, location! cellular relocalization primes specialized metabolic diversification

“…While the sugar core is typically the disaccharide sucrose, some plants accumulate monosaccharide cores including glucose . Cleavage of acylsucroses catalyzed by the cell wall invertase‐like enzyme SpASFF1 ( S. pennellii acylsucrose fructofuranosidase 1) is the final step in S. pennellii acylglucose biosynthesis . While homologous invertase enzymes more typically play key roles in plant energy metabolism , the larger group of invertases and other glycoside hydrolase enzymes use a broad range of sugar substrates beyond sucrose .…”

“…). Although cultivated tomato possesses an apparently functional ASFF1 ortholog, it does not make acylglucoses; this is partly because tomato ASFF1 does not accumulate in the trichomes . The combination of SpASFF1 relocalization and accumulation of pyranose ring‐acylated acylsucroses in the trichomes created a cellular environment that potentiated the evolution of a novel invertase that no longer cleaves sucrose, but instead makes structurally diverse acylglucoses in S. pennellii .…”