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

Abstract

Many plants in the Solanaceae family secrete acylsugars, which are branched-chain and straight-chain fatty acids esterified to glucose or sucrose. 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. We used comparative transcriptomic analysis between low- and high-acylsugar-producing accessions of Solanum pennellii and found that expression levels of most acylsugar metabolic genes, including known acylsucrose biosynthetic genes and novel candidate genes (putatively encoding a ketoacyl-ACP synthase IV/II-like enzyme, peroxisomal acyl-activating enzymes, ABC transporters, and central carbon metabolic enzymes), were positively correlated with acylsugar accumulation, except two acylglucose biosynthetic genes. Genes putatively encoding oxylipin metabolic proteins, subtilisin-like proteases, and other antimicrobial defense proteins were upregulated in low-acylsugar-producing accessions, possibly to compensate for diminished defense activities of acylsugars. Gene co-expression network analysis clustered most differentially expressed genes into two separate modules and identified genetic networks associated with acylsugar production and plant defense. Transcriptome analysis after inhibition of biosynthesis of branched-chain amino acids (precursors to branched-chain fatty acids) further supported the coordinated regulation of most acylsugar candidate genes and identified three putative AP2-family transcription factor genes that form a strong co-expression network with many acylsugar metabolic genes.