Metabolomics and Transcriptomics Provide Insights into Lipid Biosynthesis in the Embryos of Walnut (<i>Juglans regia</i> L.)

Walnut (<i>Juglans regia</i> L.) is an important woody oilseed tree species due to its commercial value. However, the regulation mechanism of walnut oil accumulation is still poorly understood, which restricted the breeding and genetic improvement of high-quality oil-bearing walnuts. In...

Full description

Bibliographic Details
Main Authors: Manman Liang, Xuemei Zhang, Qinglong Dong, Han Li, Suping Guo, Haoan Luan, Peng Jia, Minsheng Yang, Guohui Qi
Format: Article
Language:English
Published: MDPI AG 2023-01-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/12/3/538
_version_ 1797623485915201536
author Manman Liang
Xuemei Zhang
Qinglong Dong
Han Li
Suping Guo
Haoan Luan
Peng Jia
Minsheng Yang
Guohui Qi
author_facet Manman Liang
Xuemei Zhang
Qinglong Dong
Han Li
Suping Guo
Haoan Luan
Peng Jia
Minsheng Yang
Guohui Qi
author_sort Manman Liang
collection DOAJ
description Walnut (<i>Juglans regia</i> L.) is an important woody oilseed tree species due to its commercial value. However, the regulation mechanism of walnut oil accumulation is still poorly understood, which restricted the breeding and genetic improvement of high-quality oil-bearing walnuts. In order to explore the metabolic mechanism that regulates the synthesis of walnut oil, we used transcriptome sequencing technology and metabolome technology to comprehensively analyze the key genes and metabolites involved in oil synthesis of the walnut embryo at 60, 90, and 120 days after pollination (DAP). The results showed that the oil and protein contents increased gradually during fruit development, comprising 69.61% and 18.32% of the fruit, respectively, during ripening. Conversely, the contents of soluble sugar and starch decreased gradually during fruit development, comprising 2.14% and 0.84%, respectively, during ripening. Transcriptome sequencing generated 40,631 unigenes across 9 cDNA libraries. We identified 51 and 25 candidate unigenes related to the biosynthesis of fatty acid and the biosynthesis of triacylglycerol (TAG), respectively. The expression levels of the genes encoding Acetyl-CoA carboxylase (ACCase), long-chain acyl-CoA synthetases (LACS), 3-oxoacyl-ACP synthase II (KASII), and glycerol-3-phosphate acyl transfer (GPAT) were upregulated at 60 DAP relative to the levels at 90 and 120 DAP, while the stearoyl-ACP-desaturase (<i>SAD</i>) and fatty acid desaturase 2 (<i>FAD2</i>) genes were highly abundantly expressed during all walnut developmental periods. We found that ABSCISIC ACID INSENSEITIVE3 (ABI3), WRINKLEDl (WRI1), LEAFY COTYLEDON1 (LEC1), and FUSCA3 (FUS3) may be key transcription factors involved in lipid synthesis. Additionally, the metabolomics analysis detected 706 metabolites derived from 18 samples, among which, 4 are implicated in the TAG synthesis, 2 in the glycolysis pathway, and 5 in the tricarboxylic acid cycle (TCA cycle) pathway. The combined analysis of the related genes and metabolites in TAG synthesis showed that phospholipid:diacylglycerol acyltransferase (<i>PDAT</i>) genes were highly abundantly expressed across walnut fruit developmental periods, and their downstream metabolite TAG gradually accumulated with the progression of fruit development. The <i>FAD2</i> gene showed consistently higher expression during fruit development, and its downstream metabolites 18:2-PC and 18:3-PC gradually accumulated. The <i>ACCase</i>, <i>LACS</i>, <i>SAD</i>, <i>FAD2</i>, and <i>PDAT</i> genes may be crucial genes required for walnut oil synthesis. Our data will enrich public databases and provide new insights into functional genes related to lipid metabolism in walnut.
first_indexed 2024-03-11T09:29:40Z
format Article
id doaj.art-adc81f89b14243c3a39c011626ede3a7
institution Directory Open Access Journal
issn 2223-7747
language English
last_indexed 2024-03-11T09:29:40Z
publishDate 2023-01-01
publisher MDPI AG
record_format Article
series Plants
spelling doaj.art-adc81f89b14243c3a39c011626ede3a72023-11-16T17:43:48ZengMDPI AGPlants2223-77472023-01-0112353810.3390/plants12030538Metabolomics and Transcriptomics Provide Insights into Lipid Biosynthesis in the Embryos of Walnut (<i>Juglans regia</i> L.)Manman Liang0Xuemei Zhang1Qinglong Dong2Han Li3Suping Guo4Haoan Luan5Peng Jia6Minsheng Yang7Guohui Qi8College of Forestry, Hebei Agricultural University, Baoding 071001, ChinaCollege of Forestry, Hebei Agricultural University, Baoding 071001, ChinaCollege of Forestry, Hebei Agricultural University, Baoding 071001, ChinaCollege of Forestry, Hebei Agricultural University, Baoding 071001, ChinaCollege of Forestry, Hebei Agricultural University, Baoding 071001, ChinaCollege of Forestry, Hebei Agricultural University, Baoding 071001, ChinaCollege of Forestry, Hebei Agricultural University, Baoding 071001, ChinaCollege of Forestry, Hebei Agricultural University, Baoding 071001, ChinaCollege of Forestry, Hebei Agricultural University, Baoding 071001, ChinaWalnut (<i>Juglans regia</i> L.) is an important woody oilseed tree species due to its commercial value. However, the regulation mechanism of walnut oil accumulation is still poorly understood, which restricted the breeding and genetic improvement of high-quality oil-bearing walnuts. In order to explore the metabolic mechanism that regulates the synthesis of walnut oil, we used transcriptome sequencing technology and metabolome technology to comprehensively analyze the key genes and metabolites involved in oil synthesis of the walnut embryo at 60, 90, and 120 days after pollination (DAP). The results showed that the oil and protein contents increased gradually during fruit development, comprising 69.61% and 18.32% of the fruit, respectively, during ripening. Conversely, the contents of soluble sugar and starch decreased gradually during fruit development, comprising 2.14% and 0.84%, respectively, during ripening. Transcriptome sequencing generated 40,631 unigenes across 9 cDNA libraries. We identified 51 and 25 candidate unigenes related to the biosynthesis of fatty acid and the biosynthesis of triacylglycerol (TAG), respectively. The expression levels of the genes encoding Acetyl-CoA carboxylase (ACCase), long-chain acyl-CoA synthetases (LACS), 3-oxoacyl-ACP synthase II (KASII), and glycerol-3-phosphate acyl transfer (GPAT) were upregulated at 60 DAP relative to the levels at 90 and 120 DAP, while the stearoyl-ACP-desaturase (<i>SAD</i>) and fatty acid desaturase 2 (<i>FAD2</i>) genes were highly abundantly expressed during all walnut developmental periods. We found that ABSCISIC ACID INSENSEITIVE3 (ABI3), WRINKLEDl (WRI1), LEAFY COTYLEDON1 (LEC1), and FUSCA3 (FUS3) may be key transcription factors involved in lipid synthesis. Additionally, the metabolomics analysis detected 706 metabolites derived from 18 samples, among which, 4 are implicated in the TAG synthesis, 2 in the glycolysis pathway, and 5 in the tricarboxylic acid cycle (TCA cycle) pathway. The combined analysis of the related genes and metabolites in TAG synthesis showed that phospholipid:diacylglycerol acyltransferase (<i>PDAT</i>) genes were highly abundantly expressed across walnut fruit developmental periods, and their downstream metabolite TAG gradually accumulated with the progression of fruit development. The <i>FAD2</i> gene showed consistently higher expression during fruit development, and its downstream metabolites 18:2-PC and 18:3-PC gradually accumulated. The <i>ACCase</i>, <i>LACS</i>, <i>SAD</i>, <i>FAD2</i>, and <i>PDAT</i> genes may be crucial genes required for walnut oil synthesis. Our data will enrich public databases and provide new insights into functional genes related to lipid metabolism in walnut.https://www.mdpi.com/2223-7747/12/3/538oil contentlipid biosynthesis<i>SAD</i>FAD2regulatory network
spellingShingle Manman Liang
Xuemei Zhang
Qinglong Dong
Han Li
Suping Guo
Haoan Luan
Peng Jia
Minsheng Yang
Guohui Qi
Metabolomics and Transcriptomics Provide Insights into Lipid Biosynthesis in the Embryos of Walnut (<i>Juglans regia</i> L.)
Plants
oil content
lipid biosynthesis
<i>SAD</i>
FAD2
regulatory network
title Metabolomics and Transcriptomics Provide Insights into Lipid Biosynthesis in the Embryos of Walnut (<i>Juglans regia</i> L.)
title_full Metabolomics and Transcriptomics Provide Insights into Lipid Biosynthesis in the Embryos of Walnut (<i>Juglans regia</i> L.)
title_fullStr Metabolomics and Transcriptomics Provide Insights into Lipid Biosynthesis in the Embryos of Walnut (<i>Juglans regia</i> L.)
title_full_unstemmed Metabolomics and Transcriptomics Provide Insights into Lipid Biosynthesis in the Embryos of Walnut (<i>Juglans regia</i> L.)
title_short Metabolomics and Transcriptomics Provide Insights into Lipid Biosynthesis in the Embryos of Walnut (<i>Juglans regia</i> L.)
title_sort metabolomics and transcriptomics provide insights into lipid biosynthesis in the embryos of walnut i juglans regia i l
topic oil content
lipid biosynthesis
<i>SAD</i>
FAD2
regulatory network
url https://www.mdpi.com/2223-7747/12/3/538
work_keys_str_mv AT manmanliang metabolomicsandtranscriptomicsprovideinsightsintolipidbiosynthesisintheembryosofwalnutijuglansregiail
AT xuemeizhang metabolomicsandtranscriptomicsprovideinsightsintolipidbiosynthesisintheembryosofwalnutijuglansregiail
AT qinglongdong metabolomicsandtranscriptomicsprovideinsightsintolipidbiosynthesisintheembryosofwalnutijuglansregiail
AT hanli metabolomicsandtranscriptomicsprovideinsightsintolipidbiosynthesisintheembryosofwalnutijuglansregiail
AT supingguo metabolomicsandtranscriptomicsprovideinsightsintolipidbiosynthesisintheembryosofwalnutijuglansregiail
AT haoanluan metabolomicsandtranscriptomicsprovideinsightsintolipidbiosynthesisintheembryosofwalnutijuglansregiail
AT pengjia metabolomicsandtranscriptomicsprovideinsightsintolipidbiosynthesisintheembryosofwalnutijuglansregiail
AT minshengyang metabolomicsandtranscriptomicsprovideinsightsintolipidbiosynthesisintheembryosofwalnutijuglansregiail
AT guohuiqi metabolomicsandtranscriptomicsprovideinsightsintolipidbiosynthesisintheembryosofwalnutijuglansregiail