Tip of the trichome: evolution of acylsugar metabolic diversity in Solanaceae

Abstract

Acylsugars are insecticidal plant specialized metabolites produced in the Solanaceae (nightshade family). Despite having simple constituents, these compounds are unusually structurally diverse. Their structural variations in phylogenetically closely related species enable comparative biochemical approaches to understand acylsugar biosynthesis and pathway diversification. Thus far, varied enzyme classes contributing to their synthesis were characterized in cultivated and wild tomatoes, including from core metabolism-isopropylmalate synthase (Leu) and invertase (carbon)-and a group of evolutionarily related BAHD acyltransferases known as acylsucrose acyltransferases. Gene duplication and neofunctionalization of these enzymes drove acylsugar diversification both within and beyond tomato. The broad set of evolutionary mechanisms underlying acylsugar diversity in Solanaceae make this metabolic network an exemplar for detailed understanding of the evolution of metabolic form and function.

Solanaceae specialized metabolism in a non-model plant: trichome acylinositol biosynthesis

“…Acylsugars constitute a diverse group of specialized metabolites produced across the Solanaceae family (Moghe et al, 2017). Variation in acyl chain length, branching pattern or occasionally other constituents such as malonyl groups all contribute to this diversity (Fan et al, 2019). Other factors include differences in acylation position, acyl-CoA specificity, and sugar core diversity (Fan et al, 2016; Fan et al, 2017; Moghe et al, 2017; Fan et al, 2019).…”

“…Plants are master chemists and collectively produce an array of structurally diverse specialized metabolites (traditionally called secondary metabolites) from common building blocks (Bennett and Wallsgrove, 1994; Verpoorte and Alfermann, 2000; Wink, 2010). Examples include alkaloids derived from amino acids (Ziegler and Facchini, 2008), terpenes made from isoprenoids (Chappell, 1995; Pichersky and Raguso, 2018; Zhou and Pichersky, 2020) and acylsugars synthesized from acyl-CoAs and sugars (Fan et al, 2019). Most specialized metabolites are restricted in cell- or tissue-specific accumulation and found in phylogenetically restricted groups of plants (Pichersky and Lewinsohn, 2011).…”

“…Acylsugars are specialized metabolites made from sugars and acyl-CoAs in species across the Solanaceae family (King et al, 1986; King and Calhoun, 1988; Matsuzaki et al, 1991; Maldonado et al, 2006; Ghosh et al, 2014; Liu et al, 2017; Moghe et al, 2017). These compounds serve as microbial and herbivory defense agents (Goffreda et al, 1989; Leckie et al, 2016; Luu et al, 2017; Smeda et al, 2018) and contain a sugar core esterified to multiple acyl chains (Fan et al, 2019). The acyl chains are branched or straight and are proposed to be derived from amino acid or fatty acid metabolism, respectively (Walters and Steffens, 1990; Kroumova and Wagner, 2009; Ning et al, 2015).…”

“…Acylsugar acyltransferases (ASATs) are clade III BAHD (BEAT, AHCT, HCT, and DAT) acyltransferase family enzymes (D’Auria, 2006; Moghe et al, 2017), which catalyze the core acylation reactions of characterized acylsugar biosynthetic pathways (Schilmiller et al, 2012a; Schilmiller et al, 2015; Fan et al, 2016; Moghe et al, 2017; Nadakuduti et al, 2017; Fan et al, 2019). ASATs sequentially transfer acyl chains from acyl-CoAs to generate acylsucroses in plants as phylogenetically divergent as Solanum lycopersicum, Solanum pennellii, Petunia axillaris , and Salpiglossis sinuata (Schilmiller et al, 2012a; Schilmiller et al, 2015; Fan et al, 2016; Fan et al, 2017; Moghe et al, 2017; Nadakuduti et al, 2017).…”

Within and cross species predictions of plant specialized metabolism genes using transfer learning

“…Tomato is a model crop species that has emerged as a system for investigating SM pathways. For example, the production of acylsugars, a specialized metabolite, in tomato and its wild relatives is important for repelling herbivores (19)(20)(21). Some specialized metabolites found in the tomato fruit also confer health benefits by, for example, reducing risk of cancers and coronary heart diseases (4,22,23).…”