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

Abstract 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 developin...

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Main Authors: Jian Ding, Chengjiang Ruan, Wei Du, Ying Guan
Format: Article
Language:English
Published: BMC 2019-05-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-019-1815-x
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spelling doaj-729a1f6412a043f29720c0e816f2975e2020-11-25T03:19:20ZengBMCBMC Plant Biology1471-22292019-05-0119111810.1186/s12870-019-1815-xRNA-seq data reveals a coordinated regulation mechanism of multigenes involved in the high accumulation of palmitoleic acid and oil in sea buckthorn berry pulpJian Ding0Chengjiang Ruan1Wei Du2Ying Guan3Key Laboratory of Biotechnology and Bioresources Utilization, Ministry of Education, Institute of Plant Resources, Dalian Minzu UniversityKey Laboratory of Biotechnology and Bioresources Utilization, Ministry of Education, Institute of Plant Resources, Dalian Minzu UniversityKey Laboratory of Biotechnology and Bioresources Utilization, Ministry of Education, Institute of Plant Resources, Dalian Minzu UniversityInstitute of Berries, Heilongjiang Academy of Agricultural SciencesAbstract 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.http://link.springer.com/article/10.1186/s12870-019-1815-xPalmitoleic acidHippophae L.Fatty acid biosynthesisOil accumulationBerry pulp oilNon-seed tissue
collection DOAJ
language English
format Article
sources DOAJ
author Jian Ding
Chengjiang Ruan
Wei Du
Ying Guan
spellingShingle Jian Ding
Chengjiang Ruan
Wei Du
Ying Guan
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
BMC Plant Biology
Palmitoleic acid
Hippophae L.
Fatty acid biosynthesis
Oil accumulation
Berry pulp oil
Non-seed tissue
author_facet Jian Ding
Chengjiang Ruan
Wei Du
Ying Guan
author_sort Jian Ding
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_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_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_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
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2019-05-01
description Abstract 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.
topic Palmitoleic acid
Hippophae L.
Fatty acid biosynthesis
Oil accumulation
Berry pulp oil
Non-seed tissue
url http://link.springer.com/article/10.1186/s12870-019-1815-x
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