The Isogene 1-Deoxy-D-Xylulose 5-Phosphate Synthase 2 Controls Isoprenoid Profiles, Precursor Pathway Allocation, and Density of Tomato Trichomes

Abstract

Plant isoprenoids are formed from precursors synthesized by the mevalonate (MVA) pathway in the cytosol or by the methyl-D-erythritol 4-phosphate (MEP) pathway in plastids. Although some exchange of precursors occurs, cytosolic sesquiterpenes are assumed to derive mainly from MVA, while plastidial monoterpenes are produced preferentially from MEP precursors. Additional complexity arises in the first step of the MEP pathway, which is typically catalyzed by two divergent 1-deoxy-D-xylulose 5-phosphate synthase isoforms (DXS1, DXS2). In tomato (Solanum lycopersicum), the SlDXS1 gene is ubiquitously expressed with highest levels during fruit ripening, whereas SlDXS2 transcripts are abundant in only few tissues, including young leaves, petals, and isolated trichomes. Specific down-regulation of SlDXS2 expression was performed by RNA interference in transgenic plants to investigate feedback mechanisms. SlDXS2 down-regulation led to a decrease in the monoterpene β-phellandrene and an increase in two sesquiterpenes in trichomes. Moreover, incorporation of MVA-derived precursors into residual monoterpenes and into sesquiterpenes was elevated as determined by comparison of ¹³C to ¹²C natural isotope ratios. A compensatory up-regulation of SlDXS1 was not observed. Down-regulated lines also exhibited increased trichome density and showed less damage by leaf-feeding Spodoptera littoralis caterpillars. The results reveal novel, non-redundant roles of DXS2 in modulating isoprenoid metabolism and a pronounced plasticity in isoprenoid precursor allocation.

RNA sequencing on Solanum lycopersicum trichomes identifies transcription factors that activate terpene synthase promoters

“…For example 1-deoxy-d-xylulose 5-phosphate synthase (DXS), in contrast with Arabidopsis , which contains a single functional gene, has diversified into two isogenes in other plant species including tomato [48]. Whereas SlDXS1 is ubiquitously expressed, SlDXS2 is expressed only in a few tissues and in leaf trichomes its transcript abundance is much higher than that of SlDXS1 [49], although this is not the case in stem trichomes (Table 4). Furthermore, SlDXS2 is moderately induced by wounding in the cultivar Moneymaker [49], which correlates with the observed moderate induction of SlDXS2 by JA (~1.6-fold, Table 4).…”

“…Whereas SlDXS1 is ubiquitously expressed, SlDXS2 is expressed only in a few tissues and in leaf trichomes its transcript abundance is much higher than that of SlDXS1 [49], although this is not the case in stem trichomes (Table 4). Furthermore, SlDXS2 is moderately induced by wounding in the cultivar Moneymaker [49], which correlates with the observed moderate induction of SlDXS2 by JA (~1.6-fold, Table 4). SlDXS2 expression is also approximately threefold upregulated in the tomato cultivar Castlemart upon feeding by Manduca sexta larvae [50].…”

“…The regulation of precursor genes of the MEP pathway by wounding, hormones or elicitors has been demonstrated in various plant species [49–54]. Similarly, evidence for the regulation of precursor biosynthesis of the mevalonate (MVA) pathway is also abundant [55–60].…”

Plant Glandular Trichomes: Natural Cell Factories of High Biotechnological Interest

“…Mutations of some enzymes involved in secondary metabolism also impact trichome density and/or the metabolic activity of glandular trichomes. For example, in the anthocyaninfree mutant, loss of function of the chalcone isomerase (SlCHI1) triggers a reduction of type VI trichome density and metabolic output (Kang et al, 2014), while down-regulation of DXS2, a methylerythritol 4-phosphate (MEP) enzyme, increases their density (Paetzold et al, 2010). The molecular mechanisms through which these genes affect trichome density are currently unknown.…”

Carotenoid Biosynthesis in Arabidopsis: A Colorful Pathway

“…5:1 mixture of IPP and DMAPP (Figure 1). Unlike Arabidopsis, most plants appear to have small gene families encoding DXS isoforms of at least two classes (Walter et al, 2002;Krushkal et al, 2003;Kim et al, 2005;Cordoba et al, 2009;Paetzold et al, 2010;Cordoba et al, 2011). All classes of DXS isozymes have been found to participate in carotenoid biosynthesis.…”