Skip to main content
SpringerLink
Log in

Genetic control of fatty acid composition in coconut (Cocos nucifera), African oil palm (Elaeis guineensis), and date palm (Phoenix dactylifera)

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Predominant gene isoforms and expression bias in lipid metabolism pathways are highly conserved between oil-producing Arecaceae crop species coconut and oil palm, but diverge in non-oil-producing species date palm.

Abstract

Coconut (Cocos nucifera), African oil palm (Elaeis guineensis) and date palm (Phoenix dactylifera) are three major crop species in the Arecaceae family for which genome sequences have recently become available. Coconut and African oil palm both store oil in their endosperms, while date palm fruits contain very little oil. We analyzed fatty acid composition in three coconut tissues (leaf, endosperm and embryo) and in two African oil palm tissues (leaf and mesocarp), and identified 806, 840 and 848 lipid-related genes in 22 lipid metabolism pathways from the coconut, African oil palm and date palm genomes, respectively. The majority of lipid-related genes were highly homologous and retained in homologous segments between the three species. Genes involved in the conversion of pyruvate to fatty acid had a five-to-sixfold higher expression in the coconut endosperm and oil palm mesocarp than in the leaf or embryo tissues based on Fragments Per Kilobase of transcript per Million mapped reads values. A close evolutionary relationship between predominant gene isoforms and high conservation of gene expression bias in the lipid and carbohydrate gene metabolism pathways was observed for the two oil-producing species coconut and oil palm, differing from that of date palm, a non-oil-producing species. Our results elucidate the similarities and differences in lipid metabolism between the three major Arecaceae crop species, providing important information for physiology studies as well as breeding for fatty acid composition and oil content in these crops.

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

ACP:

Acyl carrier protein

CALO:

Caleosins

DGAT:

Diacylglycerol acyltransferase

FATA(B):

Acyl-ACP thioesterase A(B)

FPKM:

Fragments Per kb per Million reads

HAD:

Hydroxyacyl-ACP dehydratase

KAR:

Ketoacyl-ACP reductase

KAS:

Ketoacyl-ACP synthase

LPAAT:

Lysophosphatidic acid acyltransferase

OBO:

Oil-body oleosins

PDAT:

Phospholipid:diacylglycerol acyltransferase

PDHC:

Pyruvate dehydrogenase complex

SAD:

Stearoyl-ACP desaturase

STERO:

Steroleosins

TAG:

Triacylglycerol

WPA:

Week post-anthesis

References

  • Al-Dous EK, George B, Al-Mahmoud ME, Al-Jaber MY, Wang H, Salameh YM, Al-Azwani EK, Chaluvadi S, Pontaroli AC, DeBarry J, Arondel V, Ohlrogge J, Saie IJ, Suliman-Elmeer KM, Bennetzen JL, Kruegger RR, Malek JA (2011) De novo genome sequencing and comparative genomics of date palm (Phoenix dactylifera). Nat Biotech 29:521–527

    Article  CAS  Google Scholar 

  • Al-Mssallem IS, Hu S, Zhang X, Lin Q, Liu W, Tan J, Yu X, Liu J, Pan L, Zhang T, Yin Y, Xin C, Wu H, Zhang G, Ba Abdullah MM, Huang D, Fang Y, Alnakhli YO, Jia S, Yin A, Alhuzimi EM, Alsaihati BA, Al-Owayyed SA, Zhao D, Zhang S, Al-Otaibi NA, Sun G, Majrashi MA, Li F, Tala Wang J, Yun Q, Alnassar NA, Wang L, Yang M, Al-Jelaify RF, Liu K, Gao S, Chen K, Alkhaldi SR, Liu G, Zhang M, Guo H, Yu J (2013) Genome sequence of the date palm Phoenix dactylifera L. Nat Commun 4:2274

    Article  CAS  PubMed  Google Scholar 

  • Alshahib W, Marshall RJ (2003) Fatty acid content of the seeds from 14 varieties of date palm Phoenix dactylifera L. Int J Food Sci Tech 38:709–712

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bourgis F, Kilaru A, Cao X, Ngando-Ebongue G-F, Drira N, Ohlrogge JB, Arondel V (2011) Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proc Natl Acad Sci USA 108:12527–12532

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao J, Li J, Li D, Tobin JF, Gimeno RE (2006) Molecular identification of microsomal acyl-CoA:glycerol-3-phosphate acyltransferase, a key enzyme in de novo triacylglycerol synthesis. Proc Natl Acad Sci USA 103:19695–19700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585

    Article  CAS  PubMed  Google Scholar 

  • Davies HM, Hawkins DJ, Nelsen JS (1995) Lysophosphatidic acid acyltransferase from immature coconut endosperm having medium chain length substrate specificity. Phytochemistry 39:989–996

    Article  CAS  Google Scholar 

  • Dussert S, Guerin C, Andersson M, Joët T, Tranbarger TJ, Pizot M, Sarah G, Omore A, Durand-Gasselin T, Morcillo F (2013) Comparative transcriptome analysis of three oil palm fruit and seed tissues that differ in oil content and fatty acid composition. Plant Physiol 162:1337–1358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan J, Yan C, Zhang X, Xu C (2013) Dual role for phospholipid:diacylglycerol acyltransferase: enhancing fatty acid synthesis and diverting fatty acids from membrane lipids to triacylglycerol in Arabidopsis leaves. Plant Cell 25:3506–3518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Focks N, Benning C (1998) Wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol 118:91–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gidda SK, Shockey JM, Rothstein SJ, Dyer JM, Mullen RT (2009) Arabidopsis thaliana GPAT8 and GPAT9 are localized to the ER and possess distinct ER retrieval signals: functional divergence of the dilysine ER retrieval motif in plant cells. Plant Physiol Biochem 47:867–879

    Article  CAS  PubMed  Google Scholar 

  • Horn PJ, James CN, Gidda SK, Kilaru A, Dyer JM, Mullen RT, Ohlrogge JB, Chapman KD (2013) Identification of a new class of lipid droplet-associated proteins in plants. Plant Physiol 162:1926–1936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang AH (1996) Oleosins and oil bodies in seeds and other organs. Plant Physiol 110:1055–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang YY, Lee CP, Fu JL, Chang BC, Matzke AJ, Matzke M (2014) De novo transcriptome sequence assembly from coconut leaves and seeds with a focus on factors involved in RNA-directed DNA methylation G3 (Bethesda)(4):2147–2157

    Google Scholar 

  • Jing F, Cantu DC, Tvaruzkova J, Chipman JP, Nikolau BJ, Yandeau-Nelson MD, Reilly PJ (2011) Phylogenetic and experimental characterization of an acyl-ACP thioesterase family reveals significant diversity in enzymatic specificity and activity. BMC Biochem 12:44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim HU, Li Y, Huang AHC (2005) Ubiquitous and endoplasmic reticulum–located lysophosphatidyl acyltransferase, LPAT2, is essential for female but not male gametophyte development in Arabidopsis seeds. Plant Cell 17:1073–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knutzon DS, Lardizabal KD, Nelsen JS, Bleibaum JL, Davies HM, Metz JG (1995) Cloning of a coconut endosperm cDNA encoding a 1-acyl-sn-glycerol-3-phosphate acyltransferase that accepts medium-chain-length substrates. Plant Physiol 109:999–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knutzon DS, Hayes TR, Wyrick A, Xiong H, Davies HM, Voelker TA (1999) Lysophosphatidic acid acyltransferase from coconut endosperm mediates the insertion of laurate at the sn-2 position of triacylglycerols in lauric rapeseed oil and can increase total laurate levels. Plant Physiol 120:739–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laffargue A, de Kochko A, Dussert S (2007) Development of solid-phase extraction and methylation procedures to analyse free fatty acids in lipid-rich seeds. Plant Physiol Biochem 45:250–257

    Article  CAS  PubMed  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laureles LR, Rodriguez FM, Reano CE, Santos GA, Laurena AC, Mendoza EM (2002) Variability in fatty acid and triacylglycerol composition of the oil of coconut (Cocos nucifera L.) hybrids and their parentals. J Agric Food Chem 50:1581–1586

    Article  CAS  PubMed  Google Scholar 

  • Lee ST, Radu S, Ariffin A, Ghazali HM (2015) Physico-chemical characterization of oils extracted from noni, spinach, lady’s finger, bitter gourd and mustard seeds, and copra. Int J Food Prop 18:2508–2527

    Article  CAS  Google Scholar 

  • Liang Y, Yuan Y, Liu T, Mao W, Zheng Y, Li D (2014) Identification and computational annotation of genes differentially expressed in pulp development of Cocos nucifera L. by suppression subtractive hybridization. BMC Plant Biol 14:205

    Article  CAS  PubMed  PubMed Central  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 (2013) Acyl-lipid metabolism. Arabidopsis Book 11:e0161

    Article  PubMed  PubMed Central  Google Scholar 

  • Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18:1509–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Shimada TL, Shimada T, Takahashi H, Fukao Y, Haranishimura I (2008) A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. Plant J 55:798–809

    Article  CAS  PubMed  Google Scholar 

  • Siloto RMP, Findlay K, Lopezvillalobos A, Yeung EC, Nykiforuk C, Moloney MM (2006) The accumulation of oleosins determines the size of seed oilbodies in Arabidopsis. Plant Cell 18:1961–1974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh R, Ong-Abdullah M, Low ET, Manaf MA, Rosli R, Nookiah R, Ooi LC, Ooi SE, Chan KL, Halim MA, Azizi N, Nagappan J, Bacher B, Lakey N, Smith SW, He D, Hogan M, Budiman MA, Lee EK, Desalle R, Kudrna D, Goicoechea JL, Wing RA, Wilson RK, Fulton RS, Ordway JM, Martienssen RA, Sambanthamurthi R (2013) Oil palm genome sequence reveals divergence of interfertile species in old and new worlds. Nature 500:335–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tranbarger TJ, Dussert S, Joët T, Argout X, Summo M, Champion A, Cros D, Omore A, Nouy B, Morcillo F (2011) Regulatory mechanisms underlying oil palm druit mesocarp maturation, ripening, and functional specialization in lipid and carotenoid metabolism. Plant Physiol 156:564–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and abundance estimation from RNA-Seq reveals thousands of new transcripts and switching among isoforms. Nat Biotech 28:511–515

    Article  CAS  Google Scholar 

  • Troncoso-Ponce MA, Kilaru A, Cao X, Durrett TP, Fan J, Jensen JK, Thrower NA, Pauly M, Wilkerson C, Ohlrogge JB (2011) Comparative deep transcriptional profiling of four developing oilseeds. Plant J 68:1014–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia W, Liu Z, Yang Y, Xiao Y, Mason AS, Zhao S, Ma Z (2013) Selection of reference genes for quantitative real-time PCR in Cocos nucifera during abiotic stress. Botany 92:179–186

    Article  Google Scholar 

  • Xiao Y, Yang Y, Cao H, Fan H, Ma Z, Lei X, Mason AS, Xia Z, Huang X (2012) Efficient isolation of high quality RNA from tropical palms for RNA-seq analysis. Plant Omics 5:584–589

    CAS  Google Scholar 

  • Xiao Y, Xu P, Fan H, Baudouin L, Xia W, Bocs S, Xu J, Li Q, Guo A, Zhou L, Li J, Wu Y, Ma Z, Armero A, Issali AE, Liu N, Peng M, Yang Y (2017) The genome draft of coconut (Cocos nucifera). Gigascience 6:1–11

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan Y, Gao L, Sun R, Yu T, Liang Y, Li D, Zheng Y (2017) Seed-specific expression of an acyl–acyl carrier protein thioesterase CnFatB3 from coconut (Cocos nucifera L.) increases the accumulation of medium-chain fatty acids in transgenic Arabidopsis seeds. Sci Hortic 223:5–9

    Article  CAS  Google Scholar 

  • Zhang L, Wang SB, Li QG, Song J, Hao YQ, Zhou L, Zheng HQ, Dunwell JM, Zhang YM (2016) An Integrated bioinformatics analysis reveals divergent evolutionary pattern of oil biosynthesis in high- and low-oil plants. PLoS One 11:e0154882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Thanks to Tingting Luo at Huazhong Agricultural University for the technical help in fatty acid extraction. This work was supported by grants from Hainan Natural Science Foundation (No. 313058) and the Fundamental Scientific Research Funds for Chinese Academy of Tropical Agricultural Sciences (Project No. 1630152018007, No. 1630152017004 and No. 1630152017005). ASM is supported by DFG Emmy Noether grant MA6473/1-1.

Author information

Authors and Affiliations

  1. Coconut Research Institute, CATAS, Wenchang, 571339, Hainan, People’s Republic of China

    Yong Xiao & Haikuo Fan

  2. Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, 570228, People’s Republic of China

    Wei Xia, Bo Zhang, Jinlan Zhang & Dongyi Huang

  3. MOA Key Laboratory of Tropical Crop Biology and Genetic Resources Utilization, Institute of Tropical Bioscience and Biotechnology, CATAS, Haikou, 571101, Hainan, People’s Republic of China

    Zengying Cao, Zilong Ma & Ming Peng

  4. Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, 35392, Giessen, Germany

    Annaliese S. Mason

Authors
  1. Yong Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Annaliese S. Mason
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zengying Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haikuo Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bo Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jinlan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zilong Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ming Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dongyi Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wei Xia.

Electronic supplementary material

Supplementary files

Fig. S1 Schematic map for homologous segments between coconut, African oil palm, and date palm. The colored lines indicate homologous genes between species. The numbers on the left side and right side represent the start and end positions of homologous segments on African oil palm relative to date palm and coconut palm, respectively. The red box represents a homologous segment between the three species containing the FatB4 gene

Fig. S2 Phylogenetic relationship of FatA genes in coconut palm, oil palm, and date palm, and the FPKM values for expressed FatA genes. Gene names in grey boxes indicate very low (FPKM < 5) or no expression across all tissue types assessed. 15 and 23 W refer to 15 week post-anthesis (WPA) and 23 week post-anthesis, respectively

Fig. S3 Gene expression profiles for CnCT-α, CnBCCP, CnKAS III, CnKAR, CnHAD, CnKAS II, CnKAS I, CnSAD, CnFatA, and CnFatB at 30, 36, 42 and 47 WPA in the endosperm

Table S1 Short-sequence read archives (SRAs) used for analysis of relative gene expression using the FPKM method

Table S2 Genes and primer sets used for RT-qPCR analysis

Table S3 Size and location of homologous segments between the coconut, African oil palm, and date palm genomes which contain genes related to lipid metabolism

Table S4 a Annotation and RFKM (Reads Per kb per Million reads) values for selected genes associated with lipid metabolism in leaf, embryo, endosperm, and mesocarp tissues of coconut, African oil palm, and date palm. b Annotation and RFKM values for selected genes involved in carbohydrate and organic acid metabolism in leaf, embryo, endosperm, and mesocarp tissues of coconut, African oil palm, and date palm

Table S5 Number of lipid metabolism-related gene orthologs relative to Arabidopsis (Ath) in coconut, oil palm and date palm

Table S6 Gene copy number for selected genes associated with lipid metabolism in coconut, African oil palm, and date palm. Bold values indicate the total number of genes for isoforms, subunits, and enzymes in a specific pathway. The number of genes in parentheses indicates highly expressed genes (with FPKM values higher than 30) in at least one of the analyzed tissues

Table S7 Selected genes associated with lipid metabolism in the coconut genome located within homologous segments relative to the African oil palm and date palm genomes

Below is the link to the electronic supplementary material.

Supplementary material 1 (JPEG 2503 kb)

Supplementary material 2 (JPEG 605 kb)

Supplementary material 3 (JPEG 736 kb)

Supplementary material 4 (XLSX 21 kb)

Supplementary material 5 (XLSX 9 kb)

Supplementary material 6 (XLSX 1204 kb)

Supplementary material 7 (XLSX 5302 kb)

Supplementary material 8 (XLSX 12 kb)

Supplementary material 9 (XLSX 27 kb)

Supplementary material 10 (XLSX 97 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiao, Y., Xia, W., Mason, A.S. et al. Genetic control of fatty acid composition in coconut (Cocos nucifera), African oil palm (Elaeis guineensis), and date palm (Phoenix dactylifera). Planta 249, 333–350 (2019). https://doi.org/10.1007/s00425-018-3003-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-3003-x

Keywords

Search

Navigation