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

Abstract

1Many plants in the Solanaceae family secrete acylsugars, which are branched-chain and straight-2 chain fatty acids esterified to glucose or sucrose. These compounds have important roles in plant 3 defense and potential commercial applications. However, several acylsugar metabolic genes 4 remain unidentified, and little is known about regulation of this pathway. We used comparative 5 transcriptomic analysis between low-and high-acylsugar-producing accessions of Solanum 6 pennellii and found that expression levels of most acylsugar metabolic genes, including known 7 acylsucrose biosynthetic genes and novel candidate genes (putatively encoding a ketoacyl-ACP 8 synthase IV/II-like enzyme, peroxisomal acyl-activating enzymes, ABC transporters, and central 9 carbon metabolic enzymes), were positively correlated with acylsugar accumulation, except two 10 acylglucose biosynthetic genes. Genes putatively encoding oxylipin metabolic proteins, 11 subtilisin-like proteases, and other antimicrobial defense proteins were upregulated in low-12 acylsugar-producing accessions, possibly to compensate for diminished defense activities of 13 acylsugars. Gene co-expression network analysis clustered most differentially expressed genes 14 into two separate modules and identified genetic networks associated with acylsugar production 15 and plant defense. Transcriptome analysis after inhibition of biosynthesis of branched-chain 16 amino acids (precursors to branched-chain fatty acids) further supported the coordinated 17 regulation of most acylsugar candidate genes and identified three putative AP2-family 18 transcription factor genes that form a strong co-expression network with many acylsugar 19 metabolic genes. 20 21 22 23 24 25 26 27

An Integrated Analytical Approach Reveals Trichome Acylsugar Metabolite Diversity in the Wild Tomato Solanum pennellii

“…A group of accessions from the Nazca region, described as S. pennellii var. puberulum , are trichome-deficient and exhibit the 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.…”

Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity

“…S. pennellii natural accessions ( Mandal et al, 2020 ), as well as the S. lycopersicum M82 × S. pennellii LA0716 chromosomal substitution introgression lines (ILs) ( Eshed and Zamir, 1995 ), offer convenient resources to investigate interspecific genetic variation that affects acylsugar metabolic diversity ( Mandal et al, 2020 ; Schilmiller et al, 2010 ). In a rescreen of ILs for S. pennellii genetic regions that alter trichome acylsugar profiles ( Schilmiller et al, 2010 ), IL7-4 was found to accumulate increased C10 medium chain containing acylsugars compared with M82 ( Figure 2 , A and B).…”

Specialized Metabolism in a Nonmodel Nightshade: 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 more than 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 cultivated tomato (Solanum lycopersicum), Solanum pennellii, Petunia axillaris, and Salpiglossis sinuata (Schilmiller et al, 2012a(Schilmiller et al, , 2015Fan et al, 2016Fan et al, , 2017Moghe et al, 2017;Nadakuduti et al, 2017). The 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).…”