Skip to main content
SpringerLink
Log in

Genome-Wide Identification and Comparative Expression Profile Analysis of the Long-Chain Acyl-CoA synthetase (LACS) Gene Family in Two Different Oil Content Cultivars of Brassica napus

  • Original Article
  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

Long-chain acyl-CoA synthetase (LACS) is one of the key enzymes involved in fatty acid metabolism, including phospholipid biosynthesis, triacylglycerol (TAG) biosynthesis, and fatty acid β-oxidation in plants. However, the characterization of LACSs family in seed oil biosynthesis of Brassica napus (B. napus) remains unknown. In the present study, we performed a comprehensive genome-wide analysis of this gene family in B. napus, and 34 B. napus LACS genes (BnaLACSs) were identified. Phylogenetic analysis classified the BnaLACS proteins into four groups (A, B, C, and D), which were supported by highly conserved gene structures and consensus motifs. RNA-Sequencing (RNA-Seq) and qRT-PCR combined analysis revealed that 18 BnaLACSs (BnaLACS1-2, 1–3, 1–4, 1–9, 1–10, 2–1, 2–2, 4–1, 4–2, 6–1, 6–2, 6–4, 7–1, 7–2, 8–1, 8–2, 9–3, and 9–4) were highly expressed in developmental seeds. Comparative expression analysis between extremely high oil content (P1-HO) and low oil content (P2-LO) B. napus cultivars revealed that BnaLACS6-4, BnaLACS9-3, and BnaLACS9-4 may be involved in fatty acid synthesis in chloroplast, and BnaLACS1-10 and 4–1 may play a vital role in lipid biosynthesis in B. napus, which is important for further seed oil accumulation in oilseed rape. The present study provides important information for functional characterization of BnaLACSs in seed oil metabolism in B. napus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201

    CAS  PubMed  Google Scholar 

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Black PN, DiRusso CC (2007) Yeast acyl-CoA synthetases at the crossroads of fatty acid metabolism and regulation. Bba-Mol Cell Biol L 1771:286–298

    CAS  Google Scholar 

  • Black PN, Dirusso CC, Metzger AK, Heimert TL (1992) Cloning, sequencing, and expression of the fadd gene of Escherichia-Coli encoding acyl coenzyme-a synthetase. J Biol Chem 267:25513–25520

    CAS  PubMed  Google Scholar 

  • Chalhoub B, Denoeud F, Liu SY, Parkin IAP, Tang HB, Wang XY, Chiquet J, Belcram H, Tong CB, Samans B, Correa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao MX, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier MC, Fan GY, Renault V, Bayer PE, Golicz AA, Manoli S, Lee TH, Thi VHD, Chalabi S, Hu Q, Fan CC, Tollenaere R, Lu YH, Battail C, Shen JX, Sidebottom CHD, Wang XF, Canaguier A, Chauveau A, Berard A, Deniot G, Guan M, Liu ZS, Sun FM, Lim YP, Lyons E, Town CD, Bancroft I, Wang XW, Meng JL, Ma JX, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury JM, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou YM, Hua W, Sharpe AG, Paterson AH, Guan CY, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953

    CAS  PubMed  Google Scholar 

  • Chao H, Wang H, Wang X, Guo L, Gu J, Zhao W, Li B, Chen D, Raboanatahiry N, Li M (2017) Genetic dissection of seed oil and protein content and identification of networks associated with oil content in Brassica napus. Sci Rep 7:46295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng F, Liu SY, Wu J, Fang L, Sun SL, Liu B, Li PX, Hua W, Wang XW (2011) BRAD, the genetics and genomics database for Brassica plants. Bmc Plant Biol 11:136

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choi SC, Hobolth A, Robinson DM, Kishino H, Thorne JL (2007) Quantifying the impact of protein tertiary structure on molecular evolution. Mol Biol Evol 24:1769–1782

    CAS  PubMed  Google Scholar 

  • Deng W, Wang Y, Liu Z, Cheng H, Xue Y (2014) HemI: a toolkit for illustrating heatmaps. PLoS ONE 9:e111988

    PubMed  PubMed Central  Google Scholar 

  • Di F, Jian H, Wang T, Chen X, Ding Y, Du H, Lu K, Li J, Liu L (2018) Genome-wide analysis of the PYL gene family and identification of PYL genes that respond to abiotic stress in Brassica napus. Genes (Basel) 9:156

    Google Scholar 

  • Fulda M, Shockey J, Werber M, Wolter FP, Heinz E (2002) Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid beta-oxidation. Plant J 32:93–103

    CAS  PubMed  Google Scholar 

  • Gasteiger E (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788

    CAS  PubMed  PubMed Central  Google Scholar 

  • Groot PH, Scholte HR, Hulsmann WC (1976) Fatty acid activation: specificity, localization, and function. Adv Lipid Res 14:75–126

    CAS  PubMed  Google Scholar 

  • Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Hereditas 29:1023–1026

    CAS  PubMed  Google Scholar 

  • He X, Chen GQ, Kang ST, McKeon TA (2007) Ricinus communis contains an acyl-CoA synthetase that preferentially activates ricinoleate to its CoA thioester. Lipids 42:931–938

    CAS  PubMed  Google Scholar 

  • Ichihara K, Kobayashi N, Saito K (2003) Lipid synthesis and acyl-CoA synthetase in developing rice seeds. Lipids 38:881–884

    CAS  PubMed  Google Scholar 

  • Jang YE, Kim MY, Shim S, Lee J, Lee S-H (2015) Gene expression profiling for seed protein and oil synthesis during early seed development in soybean. Genes Genom 37:409–418

    CAS  Google Scholar 

  • Jessen D, Roth C, Wiermer M, Fulda M (2015) Two activities of long-chain acyl-coenzyme A synthetase are involved in lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis. Plant Physiol 167:351–366

    CAS  PubMed  Google Scholar 

  • Jetter R, Kunst L (2008) Plant surface lipid biosynthetic pathways and their utility for metabolic engineering of waxes and hydrocarbon biofuels. Plant J 54:670–683

    CAS  PubMed  Google Scholar 

  • Jia B, Song Y, Wu M, Lin B, Xiao K, Hu Z, Huang Y (2016) Characterization of long-chain acyl-CoA synthetases which stimulate secretion of fatty acids in green algae Chlamydomonas reinhardtii. Biotechnol Biofuels 9:184

    PubMed  PubMed Central  Google Scholar 

  • Jian H, Lu K, Yang B, Wang T, Zhang L, Zhang A, Wang J, Liu L, Qu C, Li J (2016) Genome-wide analysis and expression profiling of the SUC and SWEET gene families of sucrose transporters in oilseed rape (Brassica napus L.). Front Plant Sci 7:1464

  • Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202–1210

    CAS  PubMed  Google Scholar 

  • Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, Debono A, Durrett TP, Franke RB, Graham IA, Katayama K, Kelly AA, Larson T, Markham JE, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid KM, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J (2010) Acyl-lipid metabolism. Arabidopsis Book 8:e0133

    PubMed  Google Scholar 

  • Lu S, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA (2009) Arabidopsis CER8 encodes long-chain acyl-coa synthetase 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J 59:553–564

    CAS  PubMed  Google Scholar 

  • Lu K, Guo W, Lu J, Yu H, Qu C, Tang Z, Li J, Chai Y, Liang Y (2015) Genome-wide survey and expression profile analysis of the mitogen-activated protein kinase (MAPK) gene family in Brassica rapa. PLoS ONE 10:e0132051

    PubMed  PubMed Central  Google Scholar 

  • Overath P, Pauli G, Schairer HU (1969) Fatty acid degradation in Escherichia coli. An inducible acyl-CoA synthetase, the mapping of old-mutations, and the isolation of regulatory mutants. Eur J Biochem 7:559–574

    CAS  PubMed  Google Scholar 

  • Pongdontri P, Hills M (2001) Characterization of a novel plant acyl-CoA synthetase that is expressed in lipogenic tissues of Brassica napus L. Plant Mol Biol 47:717–726

    CAS  PubMed  Google Scholar 

  • Pulsifer IP, Kluge S, Rowland O (2012) Arabidopsis long-chain acyl-CoA synthetase 1 (LACS1), LACS2, and LACS3 facilitate fatty acid uptake in yeast. Plant Physiol Biochem 51:31–39

    CAS  PubMed  Google Scholar 

  • Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33:W116–W120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schnurr JA, Shockey JM, de Boer GJ, Browse JA (2002) Fatty acid export from the chloroplast. Molecular characterization of a major plastidial acyl-coenzyme A synthetase from Arabidopsis. Plant Physiol 129:1700–1709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schnurr J, Shockey J, Browse J (2004) The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16:629–642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shockey JM, Fulda MS, Browse JA (2002) Arabidopsis contains nine long-chain acyl-coenzyme a synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol 129:1710–1722

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tan X, Zheng X, Zhang Z, Wang Z, Xia H, Lu C, Gu S (2014) Long chain acyl-coenzyme a synthetase 4 (BnLACS4) gene from Brassica napus enhances the yeast lipid contents. J Integr Agric 13:54–62

    CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    CAS  PubMed  Google Scholar 

  • Wan H, Cui Y, Ding Y, Mei J, Dong H, Zhang W, Wu S, Liang Y, Zhang C, Li J, Xiong Q, Qian W (2016) Time-series analyses of transcriptomes and proteomes reveal molecular networks underlying oil accumulation in Canola. Front Plant Sci 7:2007

    PubMed  Google Scholar 

  • Wan HF, Cui YX, Ding YJ, Mei JQ, Dong HL, Zhang WX, Wu SQ, Liang Y, Zhang CY, Li JN, Xiong Q, Qian W (2017) Time-series analyses of transcriptomes and proteomes reveal molecular networks underlying oil accumulation in Canola. Front Plant Sci 7:1

    Google Scholar 

  • Wang XL, Li XB (2009) The GhACS1 gene encodes an acyl-CoA synthetase which is essential for normal microsporogenesis in early anther development of cotton. Plant J 57:473–486

    CAS  PubMed  Google Scholar 

  • Wang L, Yin X, Cheng C, Wang H, Guo R, Xu X, Zhao J, Zheng Y, Wang X (2015) Evolutionary and expression analysis of a MADS-box gene superfamily involved in ovule development of seeded and seedless grapevines. Mol Genet Genomics 290:825–846

    CAS  PubMed  Google Scholar 

  • Weng H, Molina I, Shockey J, Browse J (2010) Organ fusion and defective cuticle function in a lacs1 lacs2 double mutant of Arabidopsis. Planta 231:1089–1100

    CAS  PubMed  Google Scholar 

  • Wu G, Zhang L, Wu Y, Cao Y, Lu C (2010) Comparison of five endogenous reference genes for specific PCR detection and quantification of Brassica napus. J Agric Food Chem 58:2812–2817

    CAS  PubMed  Google Scholar 

  • Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci USA 109:1187–1192

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Katavic V, Li F, Haughn GW, Kunst L (2010) Insertional mutant analysis reveals that long-chain acyl-CoA synthetase 1 (LACS1), but not LACS8, functionally overlaps with LACS9 in Arabidopsis seed oil biosynthesis. Plant J 64:1048–1058

    CAS  PubMed  Google Scholar 

  • Zhou Y, Xu D, Jia L, Huang X, Ma G, Wang S, Zhu M, Zhang A, Guan M, Lu K, Xu X, Wang R, Li J, Qu C (2017) Genome-wide identification and structural analysis of bZIP transcription factor genes in Brassica napus. Genes (Basel) 8:E288

    Google Scholar 

  • Zhu X, Dunand C, Snedden W, Galaud JP (2015) CaM and CML emergence in the green lineage. Trends Plant Sci 20:483–489

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was funded by National Key R & D Program of China (2018YFD0200903; 2018YFD0100504), the “111″ Project (B12006), Modern Agro-industry Technology Research System (CARS-13), the National Natural Science Foundation of China (31400063; 31571701, U1302266), Chongqing Minsheng Technology Funds (cstc2016shms-ztzx80020), and Fundamental Research Funds for the Central Universities (XDJK2017B030). We extend our thanks to the reviewers for their careful reading and helpful comments on this manuscript.

Author information

Author notes

  1. Zhongchun Xiao and Nannan Li have contributed equally to this work.

Authors and Affiliations

  1. Chongqing Engineering Research Center for Rapeseed, College of Agronomy and Biotechnology, Southwest University, Chongqing, 400715, China

    Zhongchun Xiao, Liyuan Zhang, Chao Zhang, Hong Yang, Huiyan Zhao, Bo Yang, Lijuan Wei, Hai Du, Cunmin Qu, Kun Lu & Jiana Li

  2. Research Center of Bioenergy and Bioremediation, College of Resources and Environment, Southwest University, Chongqing, 400715, China

    Nannan Li, Shufeng Wang & Juanjuan Sun

  3. Academy of Agricultural Sciences, Southwest University, Beibei, Chongqing, 400715, China

    Zhongchun Xiao, Nannan Li, Liyuan Zhang, Chao Zhang, Hong Yang, Huiyan Zhao, Bo Yang, Lijuan Wei, Hai Du, Cunmin Qu, Kun Lu & Jiana Li

Authors
  1. Zhongchun Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nannan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shufeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juanjuan Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liyuan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Huiyan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bo Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lijuan Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hai Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Cunmin Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Kun Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jiana Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.N.L. and N.N.L. conceived and designed the experiments. Z.C.X. performed the experiments. Z.C.X., S. F.W., J.J.S., L.Y. Z., C.Z., H.Y., H.Y.Z., B.Y., L.J.W., H.D., C.M.Q, and K.L. analyzed the data. Z.C.X. and N.N.L. wrote the paper. All authors reviewed the manuscript.

Corresponding authors

Correspondence to Nannan Li or Jiana Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10528_2019_9921_MOESM1_ESM.tif

Chromosomal locations of the BnaLACS genes in the B. napus genome. The distribution of each BnaLACS gene was mapped according to the B. napus genome. The chromosome numbers are indicated at the top of each chromosome. The gene names are on the right side of each chromosome, according to the physical location (left side) of each BnaLACS gene. Supplementary file1 (XLSX 13 kb)

10528_2019_9921_MOESM2_ESM.tif

3D models of identified LACSs proteins. The tertiary structures were generated by online SWISS-MODEL Workspace. Supplementary file2 (XLSX 13 kb)

Supplementary file3 (XLSX 13 kb)

Supplementary file4 (XLSX 11 kb)

Supplementary file5 (XLSX 26 kb)

Supplementary file6 (XLSX 11 kb)

Supplementary file7 (XLSX 11 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiao, Z., Li, N., Wang, S. et al. Genome-Wide Identification and Comparative Expression Profile Analysis of the Long-Chain Acyl-CoA synthetase (LACS) Gene Family in Two Different Oil Content Cultivars of Brassica napus. Biochem Genet 57, 781–800 (2019). https://doi.org/10.1007/s10528-019-09921-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-019-09921-5

Keyword

Search

Navigation