Time-series transcriptomic analysis reveals novel gene modules that control theanine biosynthesis in tea plant (Camellia sinensis).
Theanine (thea) is a unique non-protein amino acid in tea plant (Camellia sinensis) and one of the most important small molecular compounds for tea quality and health effects. The molecular mechanism that maintains thea biosynthesis is not clear but may be reflected in complicated biological network...
Main Authors: | , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Public Library of Science (PLoS)
2020-01-01
|
Series: | PLoS ONE |
Online Access: | https://doi.org/10.1371/journal.pone.0238175 |
id |
doaj-5ac14c7eaae049e39ab9dbd8d55bfdd2 |
---|---|
record_format |
Article |
spelling |
doaj-5ac14c7eaae049e39ab9dbd8d55bfdd22021-03-03T22:04:55ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01159e023817510.1371/journal.pone.0238175Time-series transcriptomic analysis reveals novel gene modules that control theanine biosynthesis in tea plant (Camellia sinensis).Haisheng CaoXiaolong HeJinke DuRui ZhangYing ChenYong MaQi ChenCongbing FangChi-Tang HoShihua ZhangXiaochun WanTheanine (thea) is a unique non-protein amino acid in tea plant (Camellia sinensis) and one of the most important small molecular compounds for tea quality and health effects. The molecular mechanism that maintains thea biosynthesis is not clear but may be reflected in complicated biological networks as other secondary metabolites in plants. We performed an integrative transcriptomic analysis of tea seedlings bud and leave over the time-course of ethylamine (EA) treatment that activated thea pathway. We identified 54 consistent differentially expressed genes (cDEGs, 25 upregulated and 29 downregulated) during thea activation. Gene Ontology (GO) functional enrichment analysis of upregulated genes and downregulated genes showed that they may function as a cascade of biological events during their cooperative contribution to thea biosynthesis. Among the total cDEGs, a diversity of functional genes (e.g., enzymes, transcription factors, transport and binding proteins) were identified, indicating a hierarchy of gene control network underlying thea biosynthesis. A gene network associated with thea biosynthesis was modeled and three interconnected gene functional modules were identified. Among the gene modules, several topologically important genes (e.g., CsBCS-1, CsRP, CsABC2) were experimentally validated using a combined thea content and gene expression analysis. Collectively, we presented here for the first time a comprehensive landscape of the biosynthetic mechanism of thea controlled by a underling gene network, which might provide a theoretical basis for the identification of key genes that contribute to thea biosynthesis.https://doi.org/10.1371/journal.pone.0238175 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Haisheng Cao Xiaolong He Jinke Du Rui Zhang Ying Chen Yong Ma Qi Chen Congbing Fang Chi-Tang Ho Shihua Zhang Xiaochun Wan |
spellingShingle |
Haisheng Cao Xiaolong He Jinke Du Rui Zhang Ying Chen Yong Ma Qi Chen Congbing Fang Chi-Tang Ho Shihua Zhang Xiaochun Wan Time-series transcriptomic analysis reveals novel gene modules that control theanine biosynthesis in tea plant (Camellia sinensis). PLoS ONE |
author_facet |
Haisheng Cao Xiaolong He Jinke Du Rui Zhang Ying Chen Yong Ma Qi Chen Congbing Fang Chi-Tang Ho Shihua Zhang Xiaochun Wan |
author_sort |
Haisheng Cao |
title |
Time-series transcriptomic analysis reveals novel gene modules that control theanine biosynthesis in tea plant (Camellia sinensis). |
title_short |
Time-series transcriptomic analysis reveals novel gene modules that control theanine biosynthesis in tea plant (Camellia sinensis). |
title_full |
Time-series transcriptomic analysis reveals novel gene modules that control theanine biosynthesis in tea plant (Camellia sinensis). |
title_fullStr |
Time-series transcriptomic analysis reveals novel gene modules that control theanine biosynthesis in tea plant (Camellia sinensis). |
title_full_unstemmed |
Time-series transcriptomic analysis reveals novel gene modules that control theanine biosynthesis in tea plant (Camellia sinensis). |
title_sort |
time-series transcriptomic analysis reveals novel gene modules that control theanine biosynthesis in tea plant (camellia sinensis). |
publisher |
Public Library of Science (PLoS) |
series |
PLoS ONE |
issn |
1932-6203 |
publishDate |
2020-01-01 |
description |
Theanine (thea) is a unique non-protein amino acid in tea plant (Camellia sinensis) and one of the most important small molecular compounds for tea quality and health effects. The molecular mechanism that maintains thea biosynthesis is not clear but may be reflected in complicated biological networks as other secondary metabolites in plants. We performed an integrative transcriptomic analysis of tea seedlings bud and leave over the time-course of ethylamine (EA) treatment that activated thea pathway. We identified 54 consistent differentially expressed genes (cDEGs, 25 upregulated and 29 downregulated) during thea activation. Gene Ontology (GO) functional enrichment analysis of upregulated genes and downregulated genes showed that they may function as a cascade of biological events during their cooperative contribution to thea biosynthesis. Among the total cDEGs, a diversity of functional genes (e.g., enzymes, transcription factors, transport and binding proteins) were identified, indicating a hierarchy of gene control network underlying thea biosynthesis. A gene network associated with thea biosynthesis was modeled and three interconnected gene functional modules were identified. Among the gene modules, several topologically important genes (e.g., CsBCS-1, CsRP, CsABC2) were experimentally validated using a combined thea content and gene expression analysis. Collectively, we presented here for the first time a comprehensive landscape of the biosynthetic mechanism of thea controlled by a underling gene network, which might provide a theoretical basis for the identification of key genes that contribute to thea biosynthesis. |
url |
https://doi.org/10.1371/journal.pone.0238175 |
work_keys_str_mv |
AT haishengcao timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT xiaolonghe timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT jinkedu timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT ruizhang timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT yingchen timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT yongma timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT qichen timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT congbingfang timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT chitangho timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT shihuazhang timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis AT xiaochunwan timeseriestranscriptomicanalysisrevealsnovelgenemodulesthatcontroltheaninebiosynthesisinteaplantcamelliasinensis |
_version_ |
1714813459463405568 |