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

Abstract

Many solanaceous plants secrete acylsugars, which are branched-chain and straight-chain fatty acids esterified to Glu or Suc. These compounds have important roles in plant defense and potential commercial applications. However, several acylsugar metabolic genes remain unidentified, and little is known about regulation of this pathway. Comparative transcriptomics between low-and high-acylsugar-producing accessions of Solanum pennellii revealed that expression levels of known and novel candidate genes (putatively encoding beta-ketoacyl-(acyl-carrier-protein) synthases, peroxisomal acyl-activating enzymes, ATP binding cassette (ABC) transporters, and central carbon metabolic proteins) were positively correlated with acylsugar accumulation, except two genes previously reported to be involved in acylglucose biosynthesis. Genes putatively encoding oxylipin metabolic proteins, subtilisin-like proteases, and other antimicrobial defense proteins were upregulated in low-acylsugar-producing accessions. Transcriptome analysis after biochemical inhibition of biosynthesis of branched-chain amino acids (precursors to branched-chain fatty acids) by imazapyr showed concentration-dependent downregulation of known and most acylsugar candidate genes, but not defense genes. Weighted gene correlation network analysis identified separate coexpressed gene networks for acylsugar metabolism (including six transcription factor genes and flavonoid metabolic genes) and plant defense (including genes putatively encoding NB-ARC and leucine-rich repeat sequences, protein kinases and defense signaling proteins, and previously mentioned defense proteins). Additionally, virus-induced gene silencing of two trichomes preferentially expressed candidate genes for straight-chain fatty acid biosynthesis confirmed their role in acylsugar metabolism.

An Integrated Analytical Approach Reveals Trichome Acylsugar Metabolite Diversity in the Wild Tomato <em>Solanum Pennellii</em>

“…A group of accessions from the Nazca region, described as S. pennellii var. puberulum, are trichome-deficient and exhibit minimal accumulation of acylsugars and transcripts of genes associated with acylsugar metabolism [26,39]; our pilot experiments confirmed the absence of detectable acylsugars in this group and these accessions were excluded from this study. All extracts were analyzed by UHPLC-HR-MS using positive-mode electrospray ionization.…”

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

“…Together, these steps resulted in a list of 42 candidates. Previously characterized ASATs are expressed and enriched in glandular trichomes relative to non-acylsugar accumulating tissues (Schilmiller et al, 2012a; Ning et al, 2015; Fan et al, 2016; Moghe et al, 2017; Nadakuduti et al, 2017; Leong et al, 2019; Mandal et al, 2020). Thus, the 17 candidates with >500 reads in the trichome samples were selected for further analysis.…”

“…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). Expression of characterized ASATs is enriched in glandular trichomes relative to non-acylsugar producing tissues (Ning et al, 2015; Moghe et al, 2017; Nadakuduti et al, 2017; Leong et al, 2019; Mandal et al, 2020). Phylogenetic and functional analyses revealed that orthologs have similar – but distinct – substrate selectivity in acylsugar biosynthesis across the Solanaceae family (Moghe et al, 2017; Nadakuduti et al, 2017).…”

Genetic and molecular characterization of type-IV glandular trichome development in tomato (>i<Solanum lycopersicum>/i< cv. Micro-Tom) and its participation in arthropod resistance

“…7), we assessed a putative efflux transporter, which may be responsible for acylsugar exudation in type-IV trichome tips. Notably, the ABC transporter previously associated with acylsugar exudation (Mandal et al, 2019) presented a higher expression level in S. galapagense compared to MT-Get, which correlates with the differences in their exudation capacity (Suppl. Fig.…”

“…7d-e) and may sustain the positive feedback responsible for AS production. Recently, a comparative transcriptomic analysis of Solanum pennellii accessions with distinct AS contents found that the expression levels of most AS metabolic genes were positively correlated with AS accumulation (Mandal et al, 2019). Among the differentially expressed genes (DEGs), three genes putatively encoding ATP-binding cassette (ABC) transporters were upregulated in the accessions with high AS content.…”