Steroidal glycoalkaloid profiling and structures of glycoalkaloids in wild tomato fruit

Iijima, Yoko; Watanabe, Bunta; Sasaki, Ryosuke; Takenaka, Makiko; Ono, Hiroshi; Sakurai, Nozomu; Umemoto, Naoyuki; Suzuki, Hideyuki; Shibata, Daisuke; Aoki, Koh

doi:10.1016/j.phytochem.2013.07.016

Cited by 87 publications

(100 citation statements)

References 60 publications

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“…Secondary metabolism in S. pennellii is considerably more complex, as evidenced by its glycoalkaloid, acyl sugar, terpene, carotenoid and volatile content. The additional glycoalkaloids in S. pennellii can be toxic, and their abundance is reflected in the relative expression of decorative enzymes of glycoalkaloid biosynthesis in S. pennellii and S. lycopersicum 39 (Supplementary Note), with similar patterns also observed for acyl sugars and terpenes 29,33 . Variants seen in several carotenoid pathway genes, including PSY1 and lyc-B genes, are consistent with the lack of lycopene accumulation in mature S. pennellii fruit (Supplementary Note).…”

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confidence: 66%

The genome of the stress-tolerant wild tomato species Solanum pennellii

et al. 2014

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Solanum pennellii is a wild tomato species endemic to Andean regions in South America, where it has evolved to thrive in arid habitats. Because of its extreme stress tolerance and unusual morphology, it is an important donor of germplasm for the cultivated tomato Solanum lycopersicum 1 . Introgression lines (ILs) in which large genomic regions of S. lycopersicum are replaced with the corresponding segments from S. pennellii can show remarkably superior agronomic performance 2 . Here we describe a high-quality genome assembly of the parents of the IL population. By anchoring the S. pennellii genome to the genetic map, we define candidate genes for stress tolerance and provide evidence that transposable elements had a role in the evolution of these traits. Our work paves a path toward further tomato improvement and for deciphering the mechanisms underlying the myriad other agronomic traits that can be improved with S. pennellii germplasm.Crosses between distantly related plants can lead to substantial improvements in performance. Notably, S. pennellii × S. lycopersicum ILs have been used to define numerous quantitative trait loci (QTLs) for superior yield, chemical composition, morphology, abiotic stress tolerance and extreme heterosis 3,4 . Although genetic studies have proven informative, few genes underlying specific QTLs have been cloned, largely because of the lack of a S. pennellii genome sequence. To support QTL analyses, we sequenced the genome of S. pennellii using Illumina sequencing with ~190-fold coverage ( Fig. 1 and Supplementary Tables 1-5). The initial assembly size was 942 Mb, with a scaffold N50 value of 1.7 Mb and N90 value of 0.43 Mb (Table 1 and Supplementary Tables 6 and 7). We estimated the total genome size to be about 1.2 Gb using a k-mer-based analysis ( Supplementary Fig. 1 and Supplementary Table 8), in accordance with previous estimations 3,4 . We anchored 97.1% of the genome assembly to chromosomes using genetic maps and restriction site-associated DNA sequencing (RAD-seq)-based markers from the IL population 5 (Supplementary Note). Comparison of the assembly to publicly available BAC sequences indicated an accuracy of >99.9%, and a satisfactory accuracy of gap-filled regions was shown by realigning reads (Supplementary Fig. 2 and Supplementary Table 9). Of the 307,350 S. lycopersicum and 7,812 S. pennellii publicly available ESTs, 93% and >96% could be aligned to the genome, respectively (Supplementary Table 10), indicating comprehensive coverage of the gene-rich regions. We predicted 32,273 high-confidence genes and a potential set of 44,966 protein-coding genes and checked these

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confidence: 66%

The genome of the stress-tolerant wild tomato species Solanum pennellii

et al. 2014

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“…It is worth noting, however, that the levels of a-tomatine were much higher in fruit of silenced Solyc10g085230 compared with fruit of silenced Solyc06g062290. Importantly, a delay in fruit ripening was observed following silencing of Solyc10g085230, which may be of importance since it is often reported that green fruit accumulate considerably higher levels of a-tomatine compared with ripe fruit (Itkin et al, 2011(Itkin et al, , 2013Iijima et al, 2013). That said, silencing of either gene resulted in significant changes in the levels of several other glycoalkaloids within the fruit ( Figure 13E).…”

Section: Validation Of Candidate Genes: a Case Study For Genes Associmentioning

confidence: 81%

“…In some cases, the observed considerable variation in the contents of these chemical constituents has been related to the growth habit to which the wild species of tomato have adapted (Schauer et al, 2005;Yeats et al, 2012;Ichihashi and Sinha, 2014). Furthermore, these studies were able to elucidate the biosynthetic pathways of the volatiles phenylethanol and phenylacetaldehyde (Tieman et al, 2006), as well as specific glycoalkaloids (Itkin et al, 2011;Iijima et al, 2013;Itkin et al, 2013). Such research thus contributes considerably to the enhancement of our understanding of fruit specialized metabolism .…”

Section: Introductionmentioning

confidence: 98%

Identification and Mode of Inheritance of Quantitative Trait Loci for Secondary Metabolite Abundance in Tomato

et al. 2015

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A large-scale metabolic quantitative trait loci (mQTL) analysis was performed on the well-characterized Solanum pennellii introgression lines to investigate the genomic regions associated with secondary metabolism in tomato fruit pericarp. In total, 679 mQTLs were detected across the 76 introgression lines. Heritability analyses revealed that mQTLs of secondary metabolism were less affected by environment than mQTLs of primary metabolism. Network analysis allowed us to assess the interconnectivity of primary and secondary metabolism as well as to compare and contrast their respective associations with morphological traits. Additionally, we applied a recently established real-time quantitative PCR platform to gain insight into transcriptional control mechanisms of a subset of the mQTLs, including those for hydroxycinnamates, acyl-sugar, naringenin chalcone, and a range of glycoalkaloids. Intriguingly, many of these compounds displayed a dominant-negative mode of inheritance, which is contrary to the conventional wisdom that secondary metabolite contents decreased on domestication. We additionally performed an exemplary evaluation of two candidate genes for glycolalkaloid mQTLs via the use of virus-induced gene silencing. The combined data of this study were compared with previous results on primary metabolism obtained from the same material and to other studies of natural variance of secondary metabolism.

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“…Thus, tomatine was lower during the ripening process. In contrast, a putative tomatine-glycosylated metabolite, esculeoside A ( m / z = 1270.60 [M + H] + ) [25], was observed in P, but there was no accumulation in MG (Fig. 5b, c).…”

Section: Resultsmentioning

confidence: 99%

Spatially resolved metabolic distribution for unraveling the physiological change and responses in tomato fruit using matrix-assisted laser desorption/ionization–mass spectrometry imaging (MALDI–MSI)

et al. 2016

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Information on spatiotemporal metabolic behavior is indispensable for a precise understanding of physiological changes and responses, including those of ripening processes and wounding stress, in fruit, but such information is still limited. Here, we visualized the spatial distribution of metabolites within tissue sections of tomato (Solanum lycopersicum L.) fruit using a matrix-assisted laser desorption/ionization–mass spectrometry imaging (MALDI–MSI) technique combined with a matrix sublimation/recrystallization method. This technique elucidated the unique distribution patterns of more than 30 metabolite-derived ions, including primary and secondary metabolites, simultaneously. To investigate spatiotemporal metabolic alterations during physiological changes at the whole-tissue level, MALDI–MSI was performed using the different ripening phenotypes of mature green and mature red tomato fruits. Although apparent alterations in the localization and intensity of many detected metabolites were not observed between the two tomatoes, the amounts of glutamate and adenosine monophosphate, umami compounds, increased in both mesocarp and locule regions during the ripening process. In contrast, malate, a sour compound, decreased in both regions. MALDI–MSI was also applied to evaluate more local metabolic responses to wounding stress. Accumulations of a glycoalkaloid, tomatine, and a low level of its glycosylated metabolite, esculeoside A, were found in the wound region where cell death had been induced. Their inverse levels were observed in non-wounded regions. Furthermore, the amounts of both compounds differed in the developmental stages. Thus, our MALDI–MSI technique increased the understanding of the physiological changes and responses of tomato fruit through the determination of spatiotemporally resolved metabolic alterations. Graphical abstractᅟ Electronic supplementary materialThe online version of this article (doi:10.1007/s00216-016-0118-4) contains supplementary material, which is available to authorized users.

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Steroidal glycoalkaloid profiling and structures of glycoalkaloids in wild tomato fruit

Cited by 87 publications

References 60 publications

The genome of the stress-tolerant wild tomato species Solanum pennellii

The genome of the stress-tolerant wild tomato species Solanum pennellii

Identification and Mode of Inheritance of Quantitative Trait Loci for Secondary Metabolite Abundance in Tomato

Spatially resolved metabolic distribution for unraveling the physiological change and responses in tomato fruit using matrix-assisted laser desorption/ionization–mass spectrometry imaging (MALDI–MSI)

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