Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed

Abstract Background Duckweed is considered a promising source of energy due to its high starch content and rapid growth rate. Starch accumulation in duckweed involves complex processes that depend on the balanced expression of genes controlled by various environmental and endogenous factors. Previou...

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Main Authors: Changjiang Yu, Xiaowen Zhao, Guang Qi, Zetao Bai, Yu Wang, Shumin Wang, Yubin Ma, Qian Liu, Ruibo Hu, Gongke Zhou
Format: Article
Language:English
Published: BMC 2017-06-01
Series:Biotechnology for Biofuels
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13068-017-0851-8
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record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Changjiang Yu
Xiaowen Zhao
Guang Qi
Zetao Bai
Yu Wang
Shumin Wang
Yubin Ma
Qian Liu
Ruibo Hu
Gongke Zhou
spellingShingle Changjiang Yu
Xiaowen Zhao
Guang Qi
Zetao Bai
Yu Wang
Shumin Wang
Yubin Ma
Qian Liu
Ruibo Hu
Gongke Zhou
Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed
Biotechnology for Biofuels
Duckweed
Transcriptome sequencing
Nitrogen stress
Metabolic flux
Starch accumulation
author_facet Changjiang Yu
Xiaowen Zhao
Guang Qi
Zetao Bai
Yu Wang
Shumin Wang
Yubin Ma
Qian Liu
Ruibo Hu
Gongke Zhou
author_sort Changjiang Yu
title Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed
title_short Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed
title_full Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed
title_fullStr Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed
title_full_unstemmed Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed
title_sort integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed
publisher BMC
series Biotechnology for Biofuels
issn 1754-6834
publishDate 2017-06-01
description Abstract Background Duckweed is considered a promising source of energy due to its high starch content and rapid growth rate. Starch accumulation in duckweed involves complex processes that depend on the balanced expression of genes controlled by various environmental and endogenous factors. Previous studies showed that nitrogen starvation induces a global stress response and results in the accumulation of starch in duckweed. However, relatively little is known about the mechanisms underlying the regulation of starch accumulation under conditions of nitrogen starvation. Results In this study, we used next-generation sequencing technology to examine the transcriptome responses of Lemna aequinoctialis 6000 at three stages (0, 3, and 7 days) during nitrogen starvation in the presence of exogenously applied sucrose. Overall, 2522, 628, and 1832 differentially expressed unigenes (DEGs) were discovered for the treated and control samples. Clustering and enrichment analysis of DEGs revealed several biological processes occurring under nitrogen starvation. Genes involved in nitrogen metabolism showed the earliest responses to nitrogen starvation, whereas genes involved in carbohydrate biosynthesis were responded subsequently. The expression of genes encoding nitrate reductase, glutamine synthetase, and glutamate synthase was down-regulated under nitrogen starvation. The expression of unigenes encoding enzymes involved in gluconeogenesis was up-regulated, while the majority of unigenes involved in glycolysis were down-regulated. The metabolite results showed that more ADP-Glc was accumulated and lower levels of UDP-Glc were accumulated under nitrogen starvation, the activity of AGPase was significantly increased while the activity of UGPase was dramatically decreased. These changes in metabolite levels under nitrogen starvation are roughly consistent with the gene expression changes in the transcriptome. Conclusions Based on these results, it can be concluded that the increase of ADP-glucose and starch contents under nitrogen starvation is a consequence of increased output from the gluconeogenesis and TCA pathways, accompanied with the reduction of lipids and pectin biosynthesis. The results provide novel insights into the underlying mechanisms of starch accumulation during nitrogen starvation, which provide a foundation for the improvement of advanced bioethanol production in duckweed.
topic Duckweed
Transcriptome sequencing
Nitrogen stress
Metabolic flux
Starch accumulation
url http://link.springer.com/article/10.1186/s13068-017-0851-8
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spelling doaj-4be736b0ee4248d886c804815fa289b42020-11-24T20:58:32ZengBMCBiotechnology for Biofuels1754-68342017-06-0110111410.1186/s13068-017-0851-8Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweedChangjiang Yu0Xiaowen Zhao1Guang Qi2Zetao Bai3Yu Wang4Shumin Wang5Yubin Ma6Qian Liu7Ruibo Hu8Gongke Zhou9Shandong Provincial Key Laboratory of Energy Genetics, Qingdao Engineering Research Center of Biomass Resources and Environment, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of SciencesCollege of Life Sciences, China Agricultural UniversityShandong Provincial Key Laboratory of Energy Genetics, Qingdao Engineering Research Center of Biomass Resources and Environment, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of SciencesShandong Provincial Key Laboratory of Energy Genetics, Qingdao Engineering Research Center of Biomass Resources and Environment, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of SciencesShandong Provincial Key Laboratory of Energy Genetics, Qingdao Engineering Research Center of Biomass Resources and Environment, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of SciencesShandong Provincial Key Laboratory of Energy Genetics, Qingdao Engineering Research Center of Biomass Resources and Environment, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of SciencesShandong Provincial Key Laboratory of Energy Genetics, Qingdao Engineering Research Center of Biomass Resources and Environment, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of SciencesGuangzhou Genedenovo Biotechnology Co., LtdShandong Provincial Key Laboratory of Energy Genetics, Qingdao Engineering Research Center of Biomass Resources and Environment, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of SciencesShandong Provincial Key Laboratory of Energy Genetics, Qingdao Engineering Research Center of Biomass Resources and Environment, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of SciencesAbstract Background Duckweed is considered a promising source of energy due to its high starch content and rapid growth rate. Starch accumulation in duckweed involves complex processes that depend on the balanced expression of genes controlled by various environmental and endogenous factors. Previous studies showed that nitrogen starvation induces a global stress response and results in the accumulation of starch in duckweed. However, relatively little is known about the mechanisms underlying the regulation of starch accumulation under conditions of nitrogen starvation. Results In this study, we used next-generation sequencing technology to examine the transcriptome responses of Lemna aequinoctialis 6000 at three stages (0, 3, and 7 days) during nitrogen starvation in the presence of exogenously applied sucrose. Overall, 2522, 628, and 1832 differentially expressed unigenes (DEGs) were discovered for the treated and control samples. Clustering and enrichment analysis of DEGs revealed several biological processes occurring under nitrogen starvation. Genes involved in nitrogen metabolism showed the earliest responses to nitrogen starvation, whereas genes involved in carbohydrate biosynthesis were responded subsequently. The expression of genes encoding nitrate reductase, glutamine synthetase, and glutamate synthase was down-regulated under nitrogen starvation. The expression of unigenes encoding enzymes involved in gluconeogenesis was up-regulated, while the majority of unigenes involved in glycolysis were down-regulated. The metabolite results showed that more ADP-Glc was accumulated and lower levels of UDP-Glc were accumulated under nitrogen starvation, the activity of AGPase was significantly increased while the activity of UGPase was dramatically decreased. These changes in metabolite levels under nitrogen starvation are roughly consistent with the gene expression changes in the transcriptome. Conclusions Based on these results, it can be concluded that the increase of ADP-glucose and starch contents under nitrogen starvation is a consequence of increased output from the gluconeogenesis and TCA pathways, accompanied with the reduction of lipids and pectin biosynthesis. The results provide novel insights into the underlying mechanisms of starch accumulation during nitrogen starvation, which provide a foundation for the improvement of advanced bioethanol production in duckweed.http://link.springer.com/article/10.1186/s13068-017-0851-8DuckweedTranscriptome sequencingNitrogen stressMetabolic fluxStarch accumulation