An integrated omics analysis reveals the gene expression profiles of rapeseed, castor bean, and maize for seed oil biosynthesis

Abstract Background Seed storage lipids are valuable for human diet and for the sustainable development of mankind. In recent decades, many lipid metabolism genes and pathways have been identified, but the molecular mechanisms that underlie species differences in seed oil biosynthesis are not fully understood. Results To investigate the molecular mechanisms of seed oil accumulation in different species, we performed comparative genome and transcriptome analyses of rapeseed and castor bean, which have high seed oil contents, and maize, which has a low seed oil content. The results uncovered the molecular mechanism of the low and high seed oil content in maize and castor bean, respectively. Transcriptome analyses showed that more than 61% of the lipid- and carbohydrate-related genes were regulated in rapeseed and castor bean, but only 20.1% of the lipid-related genes and 22.5% of the carbohydrate-related genes were regulated in maize. Compared to rapeseed and castor bean, fewer lipid biosynthesis genes but more lipid metabolism genes were regulated in the maize embryo. More importantly, most maize genes encoding lipid-related transcription factors, triacylglycerol (TAG) biosynthetic enzymes, pentose phosphate pathway (PPP) and Calvin Cycle proteins were not regulated during seed oil synthesis, despite the presence of many homologs in the maize genome. These results revealed the molecular underpinnings of the low seed oil content in maize. In castor bean, we observed differential regulation of vital oil biosynthetic enzymes and extremely high expression levels of oil biosynthetic genes, which were consistent with the rapid accumulation of oil in castor bean developing seeds. Conclusions Compared to oil seed (rapeseed and castor bean), less oil biosynthetic genes were regulated during the seed development in non-oil seed (maize). These results shed light on molecular mechanisms of lipid biosynthesis in rapeseed, castor bean, and maize. They can provide information on key target genes that may be useful for future experimental manipulation of oil production in oilseed crops.

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Integrated Transcriptomic and Bioinformatics Analyses Reveal the Molecular Mechanisms for the Differences in Seed Oil and Starch Content Between Glycine max and Cicer arietinum

Frontiers in Plant Science ◽

10.3389/fpls.2021.743680 ◽

2021 ◽

Vol 12 ◽

Author(s):

Kun Cheng ◽

Yi-Fan Pan ◽

Lü-Meng Liu ◽

Han-Qing Zhang ◽

Yuan-Ming Zhang

Keyword(s):

Seed Development ◽

Oil Content ◽

Molecular Mechanisms ◽

Seed Oil ◽

Starch Content ◽

Development Stage ◽

Seed Oil Content ◽

Bioinformatics Analyses ◽

Oil Synthesis ◽

The Common

The seed oil and starch content of soybean are significantly different from that of chickpea. However, there are limited studies on its molecular mechanisms. To address this issue, we conducted integrated transcriptomic and bioinformatics analyses for species-specific genes and acyl-lipid-, starch-, and carbon metabolism-related genes. Among seven expressional patterns of soybean-specific genes, four were highly expressed at the middle- and late oil accumulation stages; these genes significantly enriched fatty acid synthesis and carbon metabolism, and along with common acetyl CoA carboxylase (ACCase) highly expressed at soybean middle seed development stage, common starch-degrading enzyme beta-amylase-5 (BAM5) was highly expressed at soybean early seed development stage and oil synthesis-related genes ACCase, KAS, KAR, ACP, and long-chain acyl-CoA synthetase (LACS) were co-expressed with WRI1, which may result in high seed oil content and low seed starch content in soybean. The common ADP-glucose pyrophosphorylase (AGPase) was highly expressed at chickpea middle seed development stage, along with more starch biosynthesis genes co-expressed with four-transcription-factor homologous genes in chickpea than in soybean, and the common WRI1 was not co-expressed with oil synthesis genes in chickpea, which may result in high seed starch content and low seed oil content in chickpea. The above results may be used to improve chickpea seed oil content in two ways. One is to edit CaWRI1 to co-express with oil synthesis-related genes, which may increase carbon metabolites flowing to oil synthesis, and another is to increase the expression levels of miRNA159 and miRNA319 to inhibit the expression of MYB33, which may downregulate starch synthesis-related genes, making more carbon metabolites flow into oil synthesis. Our study will provide a basis for future breeding efforts to increase the oil content of chickpea seeds.

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Comparative Transcriptome Analysis of Developing Seeds and Silique Wall Reveals Dynamic Transcription Networks for Effective Oil Production in Brassica napus L.

International Journal of Molecular Sciences ◽

10.3390/ijms20081982 ◽

2019 ◽

Vol 20 (8) ◽

pp. 1982 ◽

Cited By ~ 11

Author(s):

Muhammad Shahid ◽

Guangqin Cai ◽

Feng Zu ◽

Qing Zhao ◽

Muhammad Uzair Qasim ◽

...

Keyword(s):

Brassica Napus ◽

Seed Development ◽

Vegetable Oil ◽

Oil Content ◽

Seed Oil ◽

Seed Oil Content ◽

Oil Accumulation ◽

Developing Seeds ◽

Oil Biosynthesis ◽

Oil Crops

Vegetable oil is an essential constituent of the human diet and renewable raw material for industrial applications. Enhancing oil production by increasing seed oil content in oil crops is the most viable, environmentally friendly, and sustainable approach to meet the continuous demand for the supply of vegetable oil globally. An in-depth understanding of the gene networks involved in oil biosynthesis during seed development is a prerequisite for breeding high-oil-content varieties. Rapeseed (Brassica napus) is one of the most important oil crops cultivated on multiple continents, contributing more than 15% of the world’s edible oil supply. To understand the phasic nature of oil biosynthesis and the dynamic regulation of key pathways for effective oil accumulation in B. napus, comparative transcriptomic profiling was performed with developing seeds and silique wall (SW) tissues of two contrasting inbred lines with ~13% difference in seed oil content. Differentially expressed genes (DEGs) between high- and low-oil content lines were identified across six key developmental stages, and gene enrichment analysis revealed that genes related to photosynthesis, metabolism, carbohydrates, lipids, phytohormones, transporters, and triacylglycerol and fatty acid synthesis tended to be upregulated in the high-oil-content line. Differentially regulated DEG patterns were revealed for the control of metabolite and photosynthate production in SW and oil biosynthesis and accumulation in seeds. Quantitative assays of carbohydrates and hormones during seed development together with gene expression profiling of relevant pathways revealed their fundamental effects on effective oil accumulation. Our results thus provide insights into the molecular basis of high seed oil content (SOC) and a new direction for developing high-SOC rapeseed and other oil crops.

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Combining quantitative trait locus and co-expression analysis allowed identification of new candidates for oil accumulation in rapeseed

Journal of Experimental Botany ◽

10.1093/jxb/eraa563 ◽

2020 ◽

Author(s):

Yixin Cui ◽

Xiao Zeng ◽

Qing Xiong ◽

Dayong Wei ◽

Jinghang Liao ◽

...

Keyword(s):

Lipid Metabolism ◽

Carbon Metabolism ◽

Quantitative Trait ◽

Oil Content ◽

Seed Oil ◽

Seed Oil Content ◽

The Core ◽

New Genes ◽

Acyl Lipid ◽

Core Module

Abstract In crops there are quantitative trait loci (QTLs) in which some of the causal quantitative trait genes (QTGs) have not been functionally characterized even in the model plant Arabidopsis. We propose an approach to delineate QTGs in rapeseed by coordinating expression of genes located within QTLs and known orthologs related to traits from Arabidopsis. Using this method in developing siliques 15 d after pollination in 71 lines of rapeseed, we established an acyl-lipid metabolism co-expression network with 21 modules composed of 270 known acyl-lipid genes and 3503 new genes. The core module harbored 76 known genes involved in fatty acid and triacylglycerol biosynthesis and 671 new genes involved in sucrose transport, carbon metabolism, amino acid metabolism, seed storage protein processes, seed maturation, and phytohormone metabolism. Moreover, the core module closely associated with the modules of photosynthesis and carbon metabolism. From the co-expression network, we selected 12 hub genes to identify their putative Arabidopsis orthologs. These putative orthologs were functionally analysed using Arabidopsis knockout and overexpression lines. Four knockout mutants exhibited lower seed oil content, while the seed oil content in 10 overexpression lines was significantly increased. Therefore, combining gene co-expression network analysis and QTL mapping, this study provides new insights into the detection of QTGs and into acyl-lipid metabolism in rapeseed.

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Investigation of the contribution of oil biosynthetic enzymes to seed oil content in Brassica napus and Arabidopsis thaliana

Canadian Journal of Plant Science ◽

10.4141/cjps2013-161 ◽

2014 ◽

Vol 94 (6) ◽

pp. 1109-1112 ◽

Cited By ~ 3

Author(s):

Vesna Katavic ◽

Lin Shi ◽

Yuanyuan Yu ◽

Lifang Zhao ◽

George W. Haughn ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Brassica Napus ◽

Seed Coat ◽

Double Haploid ◽

Oil Content ◽

Seed Oil ◽

Fatty Acyl ◽

Seed Oil Content ◽

Oil Biosynthesis ◽

Tag Biosynthesis

Katavic, V., Shi, L., Yu, Y., Zhao, L., Haughn, G. W. and Kunst, L. 2014. Investigation of the contribution of oil biosynthetic enzymes to seed oil content in Brassica napus and Arabidopsis thaliana. Can. J. Plant Sci. 94: 1109–1112. One of the critical reactions in triacylglycerol (TAG) biosynthesis is activation of fatty acyl chains to fatty acyl CoAs, catalyzed by long-chain acyl CoA synthetases (LACS). In Arabidopsis thaliana there is a family of nine genes that encode LACSs. Studies to determine whether the products of two of these genes, LACS8 and LACS9, function together to contribute acyl-CoAs for storage oil biosynthesis in A. thaliana resulted in discovery that it is not LACS8 but LACS1 that functionally overlaps with LACS9 in TAG biosynthesis (published in Plant Journal). To elucidate regulatory mechanisms of seed oil synthesis, the potential roles of phospholipase D zeta (PLDZ) and rhamnose synthase 2 (RHM2/MUM4) in transcription factor GLABRA2 (GL2)-mediated regulation of seed oil biosynthesis and deposition were investigated. Results demonstrated that PLDZ genes are not involved in GL2-mediated seed oil accumulation and that GL2 regulates seed oil production, at least in part, through its influence on expression of the gene RHM2/MUM4 required for the seed coat mucilage biosynthesis (published in Plant Journal). A novel Arabidopsis mutant with speckled seed coat and reduced seed oil phenotypes resulting from a mutation in a single unknown gene was identified, but attempts to isolate the gene by positional cloning have not been successful to date (unpublished results). Finally, seed oil content in near-isogenic double haploid Brassica napus lines was analyzed, “low oil” and “high oil” lines were identified, and developing seeds for expression profiling of target seed oil biosynthesis/bioassembly genes in selected double haploid lines were collected (unpublished results).

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An integrated omics analysis reveals molecular mechanisms that are associated with differences in seed oil content between Glycine max and Brassica napus

BMC Plant Biology ◽

10.1186/s12870-018-1542-8 ◽

2018 ◽

Vol 18 (1) ◽

Cited By ~ 4

Author(s):

Zhibin Zhang ◽

Jim M. Dunwell ◽

Yuan-Ming Zhang

Keyword(s):

Glycine Max ◽

Brassica Napus ◽

Oil Content ◽

Molecular Mechanisms ◽

Seed Oil ◽

Seed Oil Content ◽

Omics Analysis ◽

Integrated Omics

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OPTIMUM RATIO OF CALCIUM AND BORON IN THE NUTRIENT SOLUTION OR IN CASTOR BEAN SHOOT FOR FRUIT YIELD AND SEED OIL CONTENT

Journal of Plant Nutrition ◽

10.1080/01904167.2012.639921 ◽

2012 ◽

Vol 35 (3) ◽

pp. 413-427 ◽

Cited By ~ 1

Author(s):

Henrique Coutinho Junqueira Franco ◽

José Lavres Junior ◽

Adilson de Oliveira ◽

Gean Carlos Silva Matias ◽

Cleusa Pereira Cabral ◽

...

Keyword(s):

Nutrient Solution ◽

Castor Bean ◽

Oil Content ◽

Seed Oil ◽

Fruit Yield ◽

Optimum Ratio ◽

Seed Oil Content

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Registration of ‘NC-Miller’ Soybean with High Yield and High Seed-Oil Content

Journal of Plant Registrations ◽

10.3198/jpr2012.01.0007crc ◽

2012 ◽

Vol 6 (3) ◽

pp. 294-297 ◽

Cited By ~ 2

Author(s):

J. W. Burton ◽

L. M. Miranda ◽

T. E. Carter ◽

D. T. Bowman

Keyword(s):

Oil Content ◽

Seed Oil ◽

High Yield ◽

Seed Oil Content

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Faculty Opinions recommendation of The homeobox gene GLABRA2 affects seed oil content in Arabidopsis.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1031749.367855 ◽

2006 ◽

Author(s):

Erich Grotewold

Keyword(s):

Oil Content ◽

Seed Oil ◽

Homeobox Gene ◽

Seed Oil Content

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Unravelling the Complex Interplay of Transcription Factors Orchestrating Seed Oil Content in Brassica napus L.

International Journal of Molecular Sciences ◽

10.3390/ijms22031033 ◽

2021 ◽

Vol 22 (3) ◽

pp. 1033

Author(s):

Abirami Rajavel ◽

Selina Klees ◽

Johanna-Sophie Schlüter ◽

Hendrik Bertram ◽

Kun Lu ◽

...

Keyword(s):

Gene Expression ◽

Transcription Factors ◽

Brassica Napus ◽

Oil Content ◽

Seed Oil ◽

Seed Oil Content ◽

Complex Interplay ◽

Brassica Napus L ◽

Data Set ◽

Developmental Switches

Transcription factors (TFs) and their complex interplay are essential for directing specific genetic programs, such as responses to environmental stresses, tissue development, or cell differentiation by regulating gene expression. Knowledge regarding TF–TF cooperations could be promising in gaining insight into the developmental switches between the cultivars of Brassica napus L., namely Zhongshuang11 (ZS11), a double-low accession with high-oil- content, and Zhongyou821 (ZY821), a double-high accession with low-oil-content. In this regard, we analysed a time series RNA-seq data set of seed tissue from both of the cultivars by mainly focusing on the monotonically expressed genes (MEGs). The consideration of the MEGs enables the capturing of multi-stage progression processes that are orchestrated by the cooperative TFs and, thus, facilitates the understanding of the molecular mechanisms determining seed oil content. Our findings show that TF families, such as NAC, MYB, DOF, GATA, and HD-ZIP are highly involved in the seed developmental process. Particularly, their preferential partner choices as well as changes in their gene expression profiles seem to be strongly associated with the differentiation of the oil content between the two cultivars. These findings are essential in enhancing our understanding of the genetic programs in both cultivars and developing novel hypotheses for further experimental studies.

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