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Thousands of specialized, steroidal metabolites are found in a wide spectrum of plants. These include the steroidal glycoalkaloids (SGAs), produced primarily by most species of the genus Solanum, and metabolites belonging to the steroidal saponins class that are widespread throughout the plant kingdom. SGAs play a protective role in plants and have potent activity in mammals, including anti-nutritional effects in humans. The presence or absence of the double bond at the C-5,6 position (unsaturated and saturated, respectively) creates vast structural diversity within this metabolite class and determines the degree of SGA toxicity. For many years, the elimination of the double bond from unsaturated SGAs was presumed to occur through a single hydrogenation step. In contrast to this prior assumption, here, we show that the tomato GLYCOALKALOID METABOLISM25 (GAME25), a short-chain dehydrogenase/reductase, catalyzes the first of three prospective reactions required to reduce the C-5,6 double bond in dehydrotomatidine to form tomatidine. The recombinant GAME25 enzyme displayed 3β-hydroxysteroid dehydrogenase/Δ5,4 isomerase activity not only on diverse steroidal alkaloid aglycone substrates but also on steroidal saponin aglycones. Notably, GAME25 down-regulation rerouted the entire tomato SGA repertoire toward the dehydro-SGAs branch rather than forming the typically abundant saturated α-tomatine derivatives. Overexpressing the tomato GAME25 in the tomato plant resulted in significant accumulation of α-tomatine in ripe fruit, while heterologous expression in cultivated eggplant generated saturated SGAs and atypical saturated steroidal saponin glycosides. This study demonstrates how a single scaffold modification of steroidal metabolites in plants results in extensive structural diversity and modulation of product toxicity.

The glycoalkaloid saponin α-tomatine is a tomato-specific secondary metabolite that accumulates to millimolar levels in vegetative tissues and has antimicrobial and antinutritional activity that kills microbial pathogens and deters herbivorous insects. We describe recent insights into the biosynthetic pathway of α-tomatine synthesis and its regulation. We discuss the mode of action of α-tomatine by physically interacting with sterols, thereby disrupting membranes, and how tomato protects itself from its toxic action. Tomato pathogenic microbes can enzymatically hydrolyze, and thereby inactivate, α-tomatine using either of three distinct types of glycosyl hydrolases. We also describe findings that extend well beyond the simple concept of plants producing toxins and pathogens inactivating them. There are reports that toxicity of α-tomatine is modulated by external pH, that α-tomatine can trigger programmed cell death in fungi, that cellular localization matters for the impact of α-tomatine on invading microbes, and that atomatine breakdown products generated by microbial hydrolytic enzymes can modulate plant immune responses. Finally, we address a number of outstanding questions that deserve attention in the future.

Cultivated potatoes (Solanum tuberosum L.), domesticated from wild Solanum species native to the Andes of southern Peru, possess a diverse gene pool representing more than 100 tuber-bearing relatives (Solanum section Petota). A diversity panel of wild species, landraces, and cultivars was sequenced to assess genetic variation within tuber-bearing Solanum and the impact of domestication on genome diversity and identify key loci selected for cultivation in North and South America. Sequence diversity of diploid and tetraploid S. tuberosum exceeded any crop resequencing study to date, in part due to expanded wild introgressions following polyploidy that captured alleles outside of their geographic origin. We identified 2,622 genes as under selection, with only 14–16% shared by North American and Andean cultivars, showing that a limited gene set drove early improvement of cultivated potato, while adaptation of upland (S. tuberosum group Andigena) and lowland (S. tuberosum groups Chilotanum and Tuberosum) populations targeted distinct loci. Signatures of selection were uncovered in genes controlling carbohydrate metabolism, glycoalkaloid biosynthesis, the shikimate pathway, the cell cycle, and circadian rhythm. Reduced sexual fertility that accompanied the shift to asexual reproduction in cultivars was reflected by signatures of selection in genes regulating pollen development/gametogenesis. Exploration of haplotype diversity at potato’s maturity locus (StCDF1) revealed introgression of truncated alleles from wild species, particularly S. microdontum in long-day–adapted cultivars. This study uncovers a historic role of wild Solanum species in the diversification of long-day–adapted tetraploid potatoes, showing that extant natural populations represent an essential source of untapped adaptive potential.

Steroidal glycoalkaloids (SGAs) are cholesterol-derived molecules that contribute to the pathogen defense in tomato but are toxic and considered to be antinutritional compounds to humans. APETALA2/Ethylene Responsive Factor (AP2/ERF) family transcription factors (TFs) play an indispensable role in various biological processes, such as plant growth and development, fruit ripening, biotic and abiotic stresses responses, and SGA biosynthesis. In this study, we identified 176 AP2/ERF genes that were domesticated or improved SlAP2/ERF in the tomato variome ( Solanum lycopersicum ) within either domestication or improvement sweeps, respectively. According to the RNA-sequencing data, 93 of the ERF genes with high transcriptional level (Transcripts Per Million, TPM > 1) belong to six clusters. Weighted gene co-expression network analysis (WGCNA) and metabolite-based genome-wide association study (mGWAS) analyses revealed that the expression level of the Solyc04g071770 ( SlERF.D6 ) gene in the cluster six gradually increased as the fruit matured. Transient transformation verified that the overexpression of SlERF.D6 significantly promoted fruit ripening and regulated the expression of multiple genes in the SGA synthesis pathway, thereby affecting the SGA content of the fruit. Virus-induced gene silencing (VIGS) showed that the silencing of SlERF.D6 delayed fruit ripening and influenced the content of SGAs. Our data provide new insights into AP2/ERF TFs in tomato, offer a candidate TF for fruit development and steroidal glycoalkaloids, and provide new resources for tomato breeding and improvement.

Tomato steroidal glycoalkaloids (tSGAs) are a class of cholesterol-derived metabolites uniquely produced by the tomato clade. These compounds provide protection against biotic stress due to their fungicidal and insecticidal properties. Although commonly reported as being anti-nutritional, both in vitro as well as pre-clinical animal studies have indicated that some tSGAs may have a beneficial impact on human health. However, the paucity of quantitative extraction and analysis methods presents a major obstacle for determining the biological and nutritional functions of tSGAs. To address this problem, we developed and validated the first comprehensive extraction and ultra-high-performance liquid chromatography tandem mass spectrometry (UHPLC-MS/MS) quantification method for tSGAs. Our extraction method allows for up to 16 samples to be extracted simultaneously in 20 min with 93.0 ± 6.8 and 100.8 ± 13.1% recovery rates for tomatidine and alpha-tomatine, respectively. Our UHPLC-MS/MS method was able to chromatographically separate analytes derived from 18 tSGA peaks representing 9 different tSGA masses, as well as two internal standards, in 13 min. Tomato steroidal glycoalkaloids that did not have available standards were annotated using high resolution mass spectrometry as well as product ion scans that provided fragmentation data. Lastly, we utilized our method to survey a variety of commonly consumed tomato-based products. Total tSGA concentrations ranged from 0.2 to 3.4 mg/serving and represent some of the first reported tSGA concentrations in tomato-based products. Our validation studies indicate that our method is sensitive, robust, and able to be used for a variety of applications where concentrations of biologically relevant tSGAs need to be quantified.

Potato, , is one of the most important global crops, but has high levels of waste due to tuber greening under light, which is associated with the accumulation of neurotoxic glycoalkaloids. However, unlike the situation in de-etiolating seedlings, the mechanisms underlying tuber greening are not well understood. Here, we have investigated the effect of monochromatic blue, red, and far-red light on the regulation of chlorophyll and glycoalkaloid accumulation in potato tubers. Blue and red wavelengths were effective for induction and accumulation of chlorophyll, carotenoids and the two major potato glycoalkaloids, α-solanine and α-chaconine, whereas none of these accumulated in darkness or under far-red light. Key genes in chlorophyll biosynthesis ( , encoding the rate-limiting enzyme glutamyl-tRNA reductase, , and and six genes ( , , , , and ) required for glycoalkaloid synthesis were also induced under white, blue, and red light but not in darkness or under far-red light. These data suggest a role for both cryptochrome and phytochrome photoreceptors in chlorophyll and glycoalkaloid accumulation. The contribution of phytochrome was further supported by the observation that far-red light could inhibit white light-induced chlorophyll and glycoalkaloid accumulation and associated gene expression. Transcriptomic analysis of tubers exposed to white, blue, and red light showed that light induction of photosynthesis and tetrapyrrole-related genes grouped into three distinct groups with one group showing a generally progressive induction by light at both 6 h and 24 h, a second group showing induction at 6 h in all light treatments, but induction only by red and white light at 24 h and a third showing just a very moderate light induction at 6 h which was reduced to the dark control level at 24 h. All glycoalkaloid synthesis genes showed a group one profile consistent with what was seen for the most light regulated chlorophyll synthesis genes. Our data provide a molecular framework for developing new approaches to reducing waste due to potato greening.

Steroidal alkaloids (SAs) and steroidal glycoalkaloids (SGAs) are common constituents of plant species belonging to the Solanaceae family. However, the molecular mechanism regulating the formation of SAs and SGAs remains unknown. Here, genome-wide association mapping was used to elucidate SA and SGA regulation in tomatoes: a SlGAME5-like glycosyltransferase (Solyc10g085240) and the transcription factor SlDOG1 (Solyc10g085210) were significantly associated with steroidal alkaloid composition. In this study, it was found that rSlGAME5-like can catalyze a variety of substrates for glycosidation and can catalyze SA and flavonol pathways to form O-glucoside and O-galactoside in vitro. The overexpression of SlGAME5-like promoted α-tomatine, hydroxytomatine, and flavonol glycoside accumulation in tomatoes. Furthermore, assessments of natural variation combined with functional analyses identified SlDOG1 as a major determinant of tomato SGA content, which also promoted SA and SGA accumulation via the regulation of GAME gene expression. This study provides new insights into the regulatory mechanisms underlying SGA production in tomatoes.

Tomato is a wonder fruit fortified with health-promoting phytochemicals that are beneficial in preventing important chronic degenerative disorders. Tomato is a good source of phenolic compounds (phenolic acids and flavonoids), carotenoids (lycopene, α, and β carotene), vitamins (ascorbic acid and vitamin A) and glycoalkaloids (tomatine). Bioactive constituents present in tomato have antioxidant, anti-mutagenic, anti-proliferative, anti-inflammatory and anti-atherogenic activities. Health promoting bioactivities of tomatoes make them useful ingredient for the development of functional foods. Protective role of tomato (lycopene as a potent antioxidant) in humans against various degenerative diseases are known throughout the world. Intake of tomato is inversely related to the incidence of cancer, cardiovascular diseases, ageing and many other health problems. Bioavailability of phytoconstituents in tomato is generally not affected by routine cooking processes making it even more beneficial for human consumption. The present review provides collective information of phytochemicals in tomato along with discussing their bioactivities and possible health benefits.

Genome-wide association studies (GWAS) are a useful tool to unravel the genetic architecture of complex traits, but the results can be difficult to interpret. Population structure, genetic heterogeneity, and rare alleles easily result in false positive or false negative associations. This paper describes the analysis of a GWAS panel combined with three bi-parental mapping populations to validate GWAS results, using phenotypic data for steroidal glycoalkaloid (SGA) accumulation and the ratio (SGR) between the two major glycoalkaloids α-solanine and α-chaconine in potato tubers. SGAs are secondary metabolites in the Solanaceae family, functional as a defence against various pests and pathogens and in high quantities toxic for humans. With GWAS, we identified five quantitative trait loci (QTL) of which Sga1.1, Sgr8.1 , and Sga11.1 were validated, but not Sga3.1 and Sgr7.1 . In the bi-parental populations, Sga5.1 and Sga7.1 were mapped, but these were not identified with GWAS. The QTLs Sga1.1 , Sga7.1 , Sgr7.1 , and Sgr8.1 co-localize with genes GAME9, GAME 6/GAME 11 , SGT1 , and SGT2 , respectively. For other genes involved in SGA synthesis, no QTLs were identified. The results of this study illustrate a number of pitfalls in GWAS of which population structure seems the most important. We also show that introgression breeding for disease resistance has introduced new haplotypes to the gene pool involved in higher SGA levels in certain pedigrees. Finally, we show that high SGA levels remain unpredictable in potato but that α-solanine/α-chaconine ratio has a predictable outcome with specific SGT1 and SGT2 haplotypes.

The Colorado potato beetle (CPB) is one of the pest insects that significantly can decrease the production of potato when no control measures are taken. The fast, flexible and diverse life cycle of the CPB, its highly destructive feeding habits, and high adaptability to a variety of environment stresses, have made the control of CPB a difficult task. This paper briefly reviews the information on all aspects of CPB management to come to an integrated pest management approach: the biology of the CPB, management practices including their limitations and drawbacks, as well as the need to incorporate host plant resistance into potato varieties. Several aspects of potato breeding for resistance to CPB are discussed. We evaluate the availability of natural variation present in potato wild relatives, the considerations in choosing a specific wild relative, and constraints in using them from biological, environmental and genetic point of view, in which newly developed technologies play an important role. We also consider recently developed GM approaches. We conclude that varieties resistant to CPB are desperately needed by farmers and demanded by society, and that the means to develop them are available.