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Transcript profiling of two potato cultivars during glycoalkaloid-inducing treatments shows differential expression of genes in sterol and glycoalkaloid metabolism.

ABSTRACT: Steroidal glycoalkaloids (SGA) are sterol-derived neurotoxic defence substances present in several members of the Solanaceae. In the potato (Solanum tuberosum), high SGA levels may render tubers harmful for consumption. Tuber SGA levels depend on genetic factors, and can increase as a response to certain stresses and environmental conditions. To identify genes underlying the cultivar variation in tuber SGA levels, we investigated two potato cultivars differing in their SGA accumulation during wounding or light exposure; two known SGA-inducing treatments. Using microarray analysis coupled to sterol and SGA quantifications, we identified a small number of differentially expressed genes that were associated with increased SGA levels. Two of these genes, encoding distinct types of sterol ?24-reductases, were by sense/antisense expression in transgenic potato plants shown to have differing roles in sterol and SGA metabolism. The results show that an increased SGA level in potato tubers during both wounding and light exposure is mediated by coordinated expression of a set of key genes in isoprenoid and steroid metabolism, and suggest that differences in this expression underlie cultivar variations in SGA levels. These results may find use within potato breeding and quality assessment.

SUBMITTER: Nahar N

PROVIDER: S-EPMC5335668 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

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Transcript profiling of two potato cultivars during glycoalkaloid-inducing treatments shows differential expression of genes in sterol and glycoalkaloid metabolism.

Nahar Nurun N Westerberg Erik E Arif Usman U Huchelmann Alexandre A Olarte Guasca Alexandra A Beste Lisa L Dalman Kerstin K Dutta Paresh C PC Jonsson Lisbeth L Sitbon Folke F

Scientific reports 20170303

Steroidal glycoalkaloids (SGA) are sterol-derived neurotoxic defence substances present in several members of the Solanaceae. In the potato (Solanum tuberosum), high SGA levels may render tubers harmful for consumption. Tuber SGA levels depend on genetic factors, and can increase as a response to certain stresses and environmental conditions. To identify genes underlying the cultivar variation in tuber SGA levels, we investigated two potato cultivars differing in their SGA accumulation during wo ...[more]

PMID: 28256633

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Project description:Potatoes are the world's most produced non-grain crops and an important food source for billions of people. Potatoes are susceptible to numerous pathogens that reduce yield, including Potato virus Y (PVY). Genetic resistance to PVY is a sustainable way to limit yield and quality losses due to PVY infection. Potato cultivars vary in their susceptibility to PVY and include susceptible varieties such as Russet Burbank, and resistant varieties such as Payette Russet. Although the loci and genes associated with PVY-resistance have been identified, the genes and mechanisms involved in limiting PVY during the development of systemic infections have yet to be fully elucidated. To increase our understanding of PVY infection, potato antiviral responses, and resistance, we utilized RNA sequencing to characterize the transcriptomes of two potato cultivars. Since transcriptional responses associated with the extreme resistance response occur soon after PVY contact, we analyzed the transcriptome and small RNA profile of both the PVY-resistant Payette Russet cultivar and PVY-susceptible Russet Burbank cultivar 24 hours post-inoculation. While hundreds of genes, including terpene synthase and protein kinase encoding genes, exhibited increased expression, the majority, including numerous genes involved in plant pathogen interactions, were downregulated. To gain greater understanding of the transcriptional changes that occur during the development of systemic PVY-infection, we analyzed Russet Burbank leaf samples one week and four weeks post-inoculation and identified similarities and differences, including higher expression of genes involved in chloroplast function, photosynthesis, and secondary metabolite production, and lower expression of defense response genes at those time points. Small RNA sequencing identified different populations of 21- and 24-nucleotide RNAs and revealed that the miRNA profiles in PVY-infected Russet Burbank plants were similar to those observed in other PVY-tolerant cultivars and that during systemic infection ~32% of the NLR-type disease resistance genes were targeted by 21-nt small RNAs. Analysis of alternative splicing in PVY-infected potato plants identified splice variants of several hundred genes, including isoforms that were more dominant in PVY-infected plants. The description of the PVYN-Wi-associated transcriptome and small RNA profiles of two potato cultivars described herein adds to the body of knowledge regarding differential outcomes of infection for specific PVY strain and host cultivar pairs, which will help further understanding of the mechanisms governing genetic resistance and/or virus-limiting responses in potato plants.

Project description:BackgroundGlycoalkaloids are bioactive compounds that contribute to the defence response of plants against herbivore attack and during pathogenesis. Solanaceous plants, including cultivated and wild potato species, are sources of steroidal glycoalkaloids. Solanum plants differ in the content and composition of glycoalkaloids in organs. In wild and cultivated potato species, more than 50 steroidal glycoalkaloids were recognized. Steroidal glycoalkaloids are recognized as potential allelopathic/phytotoxic compounds that may modify the growth of target plants. There are limited data on the impact of the composition of glycoalkaloids on their phytotoxic potential.ResultsThe presence of α-solasonine and α-solamargine in potato leaf extracts corresponded to the high phytotoxic potential of the extracts. Among the differentially expressed genes between potato leaf bulks with high and low phytotoxic potential, the most upregulated transcripts in sample of high phytotoxic potential were anthocyanin 5-aromatic acyltransferase-like and subtilisin-like protease SBT1.7-transcript variant X2. The most downregulated genes were carbonic anhydrase chloroplastic-like and miraculin-like. An analysis of differentially expressed proteins revealed that the most abundant group of proteins were those related to stress and defence, including glucan endo-1,3-beta-glucosidase acidic isoform, whose expression level was 47.96× higher in potato leaf extract with low phytotoxic.ConclusionsThe phytotoxic potential of potato leaf extract possessing low glycoalkaloid content is determined by the specific composition of these compounds in leaf extract, where α-solasonine and α-solamargine may play significant roles. Differentially expressed gene and protein profiles did not correspond to the glycoalkaloid biosynthesis pathway in the expression of phytotoxic potential. We cannot exclude the possibility that the phytotoxic potential is influenced by other compounds that act antagonistically or may diminish the glycoalkaloids effect.

Project description:BackgroundGrapevine berries undergo complex biochemical changes during fruit maturation, many of which are dependent upon the variety and its environment. In order to elucidate the varietal dependent developmental regulation of primary and specialized metabolism, berry skins of Cabernet Sauvignon and Shiraz were subjected to gas chromatography-mass spectrometry (GC-MS) and liquid chromatography-mass spectrometry (LC-MS) based metabolite profiling from pre-veraison to harvest. The generated dataset was augmented with transcript profiling using RNAseq.ResultsThe analysis of the metabolite data revealed similar developmental patterns of change in primary metabolites between the two cultivars. Nevertheless, towards maturity the extent of change in the major organic acid and sugars (i.e. sucrose, trehalose, malate) and precursors of aromatic and phenolic compounds such as quinate and shikimate was greater in Shiraz compared to Cabernet Sauvignon. In contrast, distinct directional projections on the PCA plot of the two cultivars samples towards maturation when using the specialized metabolite profiles were apparent, suggesting a cultivar-dependent regulation of the specialized metabolism. Generally, Shiraz displayed greater upregulation of the entire polyphenol pathway and specifically higher accumulation of piceid and coumaroyl anthocyanin forms than Cabernet Sauvignon from veraison onwards. Transcript profiling revealed coordinated increased transcript abundance for genes encoding enzymes of committing steps in the phenylpropanoid pathway. The anthocyanin metabolite profile showed F3'5'H-mediated delphinidin-type anthocyanin enrichment in both varieties towards maturation, consistent with the transcript data, indicating that the F3'5'H-governed branching step dominates the anthocyanin profile at late berry development. Correlation analysis confirmed the tightly coordinated metabolic changes during development, and suggested a source-sink relation between the central and specialized metabolism, stronger in Shiraz than Cabernet Sauvignon. RNAseq analysis also revealed that the two cultivars exhibited distinct pattern of changes in genes related to abscisic acid (ABA) biosynthesis enzymes.ConclusionsCompared with CS, Shiraz showed higher number of significant correlations between metabolites, which together with the relatively higher expression of flavonoid genes supports the evidence of increased accumulation of coumaroyl anthocyanins in that cultivar. Enhanced stress related metabolism, e.g. trehalose, stilbene and ABA in Shiraz berry-skin are consistent with its relatively higher susceptibility to environmental cues.

Project description:Potato, S. tuberosum, 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 (HEMA1, encoding the rate-limiting enzyme glutamyl-tRNA reductase, GSA, CHLH and GUN4) and six genes (HMG1, SQS, CAS1, SSR2, SGT1 and SGT2) 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.

Dataset Information

Transcript profiling of two potato cultivars during glycoalkaloid-inducing treatments shows differential expression of genes in sterol and glycoalkaloid metabolism.

Publications

Transcript profiling of two potato cultivars during glycoalkaloid-inducing treatments shows differential expression of genes in sterol and glycoalkaloid metabolism.

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