Identification of genes associated with ricinoleic acid accumulation in Hiptage benghalensis via transcriptome analysis

Abstract Background Ricinoleic acid is a high-value hydroxy fatty acid with broad industrial applications. Hiptage benghalensis seed oil contains a high amount of ricinoleic acid (~ 80%) and represents an emerging source of this unusual fatty acid. However, the mechanism of ricinoleic acid accumulat...

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Main Authors: Bo Tian, Tianquan Lu, Yang Xu, Ruling Wang, Guanqun Chen
Format: Article
Language:English
Published: BMC 2019-01-01
Series:Biotechnology for Biofuels
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13068-019-1358-2
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author Bo Tian
Tianquan Lu
Yang Xu
Ruling Wang
Guanqun Chen
author_facet Bo Tian
Tianquan Lu
Yang Xu
Ruling Wang
Guanqun Chen
author_sort Bo Tian
collection DOAJ
description Abstract Background Ricinoleic acid is a high-value hydroxy fatty acid with broad industrial applications. Hiptage benghalensis seed oil contains a high amount of ricinoleic acid (~ 80%) and represents an emerging source of this unusual fatty acid. However, the mechanism of ricinoleic acid accumulation in H. benghalensis is yet to be explored at the molecular level, which hampers the exploration of its potential in ricinoleic acid production. Results To explore the molecular mechanism of ricinoleic acid biosynthesis and regulation, H. benghalensis seeds were harvested at five developing stages (13, 16, 19, 22, and 25 days after pollination) for lipid analysis. The results revealed that the rapid accumulation of ricinoleic acid occurred at the early–mid-seed development stages (16–22 days after pollination). Subsequently, the gene transcription profiles of the developing seeds were characterized via a comprehensive transcriptome analysis with second-generation sequencing and single-molecule real-time sequencing. Differential expression patterns were identified in 12,555 transcripts, including 71 enzymes in lipid metabolic pathways, 246 putative transcription factors (TFs) and 124 long noncoding RNAs (lncRNAs). Twelve genes involved in diverse lipid metabolism pathways, including fatty acid biosynthesis and modification (hydroxylation), lipid traffic, triacylglycerol assembly, acyl editing and oil-body formation, displayed high expression levels and consistent expression patterns with ricinoleic acid accumulation in the developing seeds, suggesting their primary roles in ricinoleic acid production. Subsequent co-expression network analysis identified 57 TFs and 35 lncRNAs, which are putatively involved in the regulation of ricinoleic acid biosynthesis. The transcriptome data were further validated by analyzing the expression profiles of key enzyme-encoding genes, TFs and lncRNAs with quantitative real-time PCR. Finally, a network of genes associated with ricinoleic acid accumulation in H. benghalensis was established. Conclusions This study was the first step toward the understating of the molecular mechanisms of ricinoleic acid biosynthesis and oil accumulation in H. benghalensis seeds and identified a pool of novel genes regulating ricinoleic acid accumulation. The results set a foundation for developing H. benghalensis into a novel ricinoleic acid feedstock at the transcriptomic level and provided valuable candidate genes for improving ricinoleic acid production in other plants.
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spelling doaj.art-520e99939829448cb06b3c78d7e751d82022-12-22T03:22:04ZengBMCBiotechnology for Biofuels1754-68342019-01-0112111610.1186/s13068-019-1358-2Identification of genes associated with ricinoleic acid accumulation in Hiptage benghalensis via transcriptome analysisBo Tian0Tianquan Lu1Yang Xu2Ruling Wang3Guanqun Chen4Key Laboratory of Tropical Plant Resource and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of SciencesKey Laboratory of Tropical Plant Resource and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of SciencesDepartment of Agricultural, Food and Nutritional Science, University of AlbertaKey Laboratory of Tropical Plant Resource and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of SciencesDepartment of Agricultural, Food and Nutritional Science, University of AlbertaAbstract Background Ricinoleic acid is a high-value hydroxy fatty acid with broad industrial applications. Hiptage benghalensis seed oil contains a high amount of ricinoleic acid (~ 80%) and represents an emerging source of this unusual fatty acid. However, the mechanism of ricinoleic acid accumulation in H. benghalensis is yet to be explored at the molecular level, which hampers the exploration of its potential in ricinoleic acid production. Results To explore the molecular mechanism of ricinoleic acid biosynthesis and regulation, H. benghalensis seeds were harvested at five developing stages (13, 16, 19, 22, and 25 days after pollination) for lipid analysis. The results revealed that the rapid accumulation of ricinoleic acid occurred at the early–mid-seed development stages (16–22 days after pollination). Subsequently, the gene transcription profiles of the developing seeds were characterized via a comprehensive transcriptome analysis with second-generation sequencing and single-molecule real-time sequencing. Differential expression patterns were identified in 12,555 transcripts, including 71 enzymes in lipid metabolic pathways, 246 putative transcription factors (TFs) and 124 long noncoding RNAs (lncRNAs). Twelve genes involved in diverse lipid metabolism pathways, including fatty acid biosynthesis and modification (hydroxylation), lipid traffic, triacylglycerol assembly, acyl editing and oil-body formation, displayed high expression levels and consistent expression patterns with ricinoleic acid accumulation in the developing seeds, suggesting their primary roles in ricinoleic acid production. Subsequent co-expression network analysis identified 57 TFs and 35 lncRNAs, which are putatively involved in the regulation of ricinoleic acid biosynthesis. The transcriptome data were further validated by analyzing the expression profiles of key enzyme-encoding genes, TFs and lncRNAs with quantitative real-time PCR. Finally, a network of genes associated with ricinoleic acid accumulation in H. benghalensis was established. Conclusions This study was the first step toward the understating of the molecular mechanisms of ricinoleic acid biosynthesis and oil accumulation in H. benghalensis seeds and identified a pool of novel genes regulating ricinoleic acid accumulation. The results set a foundation for developing H. benghalensis into a novel ricinoleic acid feedstock at the transcriptomic level and provided valuable candidate genes for improving ricinoleic acid production in other plants.http://link.springer.com/article/10.1186/s13068-019-1358-2Co-expression network analysisHiptage benghalensisIndustrial oilsLipid biosynthesisLong noncoding RNAOilseed
spellingShingle Bo Tian
Tianquan Lu
Yang Xu
Ruling Wang
Guanqun Chen
Identification of genes associated with ricinoleic acid accumulation in Hiptage benghalensis via transcriptome analysis
Biotechnology for Biofuels
Co-expression network analysis
Hiptage benghalensis
Industrial oils
Lipid biosynthesis
Long noncoding RNA
Oilseed
title Identification of genes associated with ricinoleic acid accumulation in Hiptage benghalensis via transcriptome analysis
title_full Identification of genes associated with ricinoleic acid accumulation in Hiptage benghalensis via transcriptome analysis
title_fullStr Identification of genes associated with ricinoleic acid accumulation in Hiptage benghalensis via transcriptome analysis
title_full_unstemmed Identification of genes associated with ricinoleic acid accumulation in Hiptage benghalensis via transcriptome analysis
title_short Identification of genes associated with ricinoleic acid accumulation in Hiptage benghalensis via transcriptome analysis
title_sort identification of genes associated with ricinoleic acid accumulation in hiptage benghalensis via transcriptome analysis
topic Co-expression network analysis
Hiptage benghalensis
Industrial oils
Lipid biosynthesis
Long noncoding RNA
Oilseed
url http://link.springer.com/article/10.1186/s13068-019-1358-2
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