Cargando…

RNA-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulp

BACKGROUND: Sea buckthorn is a woody oil crop in which palmitoleic acid (C16:1n7, an omega-7 fatty acid (FA)) contributes approximately 40% of the total FA content in berry pulp (non-seed tissue). However, the molecular mechanisms contributing to the high accumulation of C16:1n7 in developing sea bu...

Descripción completa

Detalles Bibliográficos
Autores principales: Ding, Jian, Ruan, Chengjiang, Du, Wei, Guan, Ying
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6528223/
https://www.ncbi.nlm.nih.gov/pubmed/31109294
http://dx.doi.org/10.1186/s12870-019-1815-x
_version_ 1783420168848801792
author Ding, Jian
Ruan, Chengjiang
Du, Wei
Guan, Ying
author_facet Ding, Jian
Ruan, Chengjiang
Du, Wei
Guan, Ying
author_sort Ding, Jian
collection PubMed
description BACKGROUND: Sea buckthorn is a woody oil crop in which palmitoleic acid (C16:1n7, an omega-7 fatty acid (FA)) contributes approximately 40% of the total FA content in berry pulp (non-seed tissue). However, the molecular mechanisms contributing to the high accumulation of C16:1n7 in developing sea buckthorn berry pulp (SBP) remain poorly understood. RESULTS: We identified 1737 unigenes associated with lipid metabolism through RNA-sequencing analysis of the four developmental stages of berry pulp in two sea buckthorn lines, ‘Za56’ and ‘TF2–36’; 139 differentially expressed genes were detected between the different berry pulp developmental stages in the two lines. Analyses of the FA composition showed that the C16:1n7 contents were significantly higher in line ‘Za56’ than in line ‘TF2–36’ in the mid-late developmental stages of SBP. Additionally, qRT-PCR analyses of 15 genes involved in FA and triacylglycerol (TAG) biosynthesis in both lines revealed that delta9-ACP-desaturase (ACP-Δ9D) competed with 3-ketoacyl-ACP-synthase II (KASII) for the substrate C16:0-ACP and that ACP-Δ9D and delta9-CoA-desaturase (CoA-Δ9D) gene expression positively correlated with C16:1n7 content; KASII and fatty acid elongation 1 (FAE1) gene expression positively correlated with C18:0 content in developing SBP. Specifically, the abundance of ACP-Δ9D and CoA-Δ9D transcripts in line ‘Za56’, which had a higher C16:1n7 content than line ‘TF2–36’, suggests that these two genes play an important role in C16:1n7 biosynthesis. Furthermore, the high expressions of the glycerol-3-phosphate dehydrogenase (GPD1) gene and the WRINKLED1 (WRI1) transcription factor contributed to increased biosynthesis of TAG precursor and FAs, respectively, in the early developmental stages of SBP, and the high expression of the diacylglycerol O-acyltransferase 1 (DGAT1) gene increased TAG assembly in the later developmental stages of SBP. Overall, we concluded that increased ACP-Δ9D and CoA-Δ9D levels coupled with decreased KASII and FAE1 activity is a critical event for high C16:1n7 accumulation and that the coordinated high expression of WRI1, GPD1, and DGAT1 genes resulted in high oil accumulation in SBP. CONCLUSION: Our results provide a scientific basis for understanding the mechanism of high C16:1n7 accumulation in berry pulp (non-seed tissue) and are valuable to the genetic breeding programme for achieving a high quality and yield of SBP oil. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1815-x) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6528223
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-65282232019-05-28 RNA-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulp Ding, Jian Ruan, Chengjiang Du, Wei Guan, Ying BMC Plant Biol Research Article BACKGROUND: Sea buckthorn is a woody oil crop in which palmitoleic acid (C16:1n7, an omega-7 fatty acid (FA)) contributes approximately 40% of the total FA content in berry pulp (non-seed tissue). However, the molecular mechanisms contributing to the high accumulation of C16:1n7 in developing sea buckthorn berry pulp (SBP) remain poorly understood. RESULTS: We identified 1737 unigenes associated with lipid metabolism through RNA-sequencing analysis of the four developmental stages of berry pulp in two sea buckthorn lines, ‘Za56’ and ‘TF2–36’; 139 differentially expressed genes were detected between the different berry pulp developmental stages in the two lines. Analyses of the FA composition showed that the C16:1n7 contents were significantly higher in line ‘Za56’ than in line ‘TF2–36’ in the mid-late developmental stages of SBP. Additionally, qRT-PCR analyses of 15 genes involved in FA and triacylglycerol (TAG) biosynthesis in both lines revealed that delta9-ACP-desaturase (ACP-Δ9D) competed with 3-ketoacyl-ACP-synthase II (KASII) for the substrate C16:0-ACP and that ACP-Δ9D and delta9-CoA-desaturase (CoA-Δ9D) gene expression positively correlated with C16:1n7 content; KASII and fatty acid elongation 1 (FAE1) gene expression positively correlated with C18:0 content in developing SBP. Specifically, the abundance of ACP-Δ9D and CoA-Δ9D transcripts in line ‘Za56’, which had a higher C16:1n7 content than line ‘TF2–36’, suggests that these two genes play an important role in C16:1n7 biosynthesis. Furthermore, the high expressions of the glycerol-3-phosphate dehydrogenase (GPD1) gene and the WRINKLED1 (WRI1) transcription factor contributed to increased biosynthesis of TAG precursor and FAs, respectively, in the early developmental stages of SBP, and the high expression of the diacylglycerol O-acyltransferase 1 (DGAT1) gene increased TAG assembly in the later developmental stages of SBP. Overall, we concluded that increased ACP-Δ9D and CoA-Δ9D levels coupled with decreased KASII and FAE1 activity is a critical event for high C16:1n7 accumulation and that the coordinated high expression of WRI1, GPD1, and DGAT1 genes resulted in high oil accumulation in SBP. CONCLUSION: Our results provide a scientific basis for understanding the mechanism of high C16:1n7 accumulation in berry pulp (non-seed tissue) and are valuable to the genetic breeding programme for achieving a high quality and yield of SBP oil. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1815-x) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-20 /pmc/articles/PMC6528223/ /pubmed/31109294 http://dx.doi.org/10.1186/s12870-019-1815-x Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Ding, Jian
Ruan, Chengjiang
Du, Wei
Guan, Ying
RNA-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulp
title RNA-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulp
title_full RNA-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulp
title_fullStr RNA-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulp
title_full_unstemmed RNA-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulp
title_short RNA-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulp
title_sort rna-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulp
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6528223/
https://www.ncbi.nlm.nih.gov/pubmed/31109294
http://dx.doi.org/10.1186/s12870-019-1815-x
work_keys_str_mv AT dingjian rnaseqdatarevealsacoordinatedregulationmechanismofmultigenesinvolvedinthehighaccumulationofpalmitoleicacidandoilinseabuckthornberrypulp
AT ruanchengjiang rnaseqdatarevealsacoordinatedregulationmechanismofmultigenesinvolvedinthehighaccumulationofpalmitoleicacidandoilinseabuckthornberrypulp
AT duwei rnaseqdatarevealsacoordinatedregulationmechanismofmultigenesinvolvedinthehighaccumulationofpalmitoleicacidandoilinseabuckthornberrypulp
AT guanying rnaseqdatarevealsacoordinatedregulationmechanismofmultigenesinvolvedinthehighaccumulationofpalmitoleicacidandoilinseabuckthornberrypulp