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Planta

, Volume 249, Issue 2, pp 333–350 | Cite as

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

  • Yong Xiao
  • Wei XiaEmail author
  • Annaliese S. Mason
  • Zengying Cao
  • Haikuo Fan
  • Bo Zhang
  • Jinlan Zhang
  • Zilong Ma
  • Ming Peng
  • Dongyi Huang
Original Article
  • 165 Downloads

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.

Keywords

Expression bias Homologous segment Lipid-related genes Oil composition Predominant gene isoforms 

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

Notes

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.

Supplementary material

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References

  1. 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 29:521–527CrossRefGoogle Scholar
  2. 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 4:2274CrossRefGoogle Scholar
  3. 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 38:709–712CrossRefGoogle Scholar
  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  5. 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 108:12527–12532CrossRefGoogle Scholar
  6. 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 103:19695–19700CrossRefGoogle Scholar
  7. Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585CrossRefGoogle Scholar
  8. Davies HM, Hawkins DJ, Nelsen JS (1995) Lysophosphatidic acid acyltransferase from immature coconut endosperm having medium chain length substrate specificity. Phytochemistry 39:989–996CrossRefGoogle Scholar
  9. 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 162:1337–1358CrossRefGoogle Scholar
  10. 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 25:3506–3518CrossRefGoogle Scholar
  11. 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 118:91–101CrossRefGoogle Scholar
  12. 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 47:867–879CrossRefGoogle Scholar
  13. 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 162:1926–1936CrossRefGoogle Scholar
  14. Huang AH (1996) Oleosins and oil bodies in seeds and other organs. Plant Physiol 110:1055–1061CrossRefGoogle Scholar
  15. 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):2147–2157Google Scholar
  16. 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 12:44CrossRefGoogle Scholar
  17. 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 17:1073–1089CrossRefGoogle Scholar
  18. 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 109:999–1006CrossRefGoogle Scholar
  19. 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 120:739–746CrossRefGoogle Scholar
  20. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  21. 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 45:250–257CrossRefGoogle Scholar
  22. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359CrossRefGoogle Scholar
  23. 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 50:1581–1586CrossRefGoogle Scholar
  24. 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 18:2508–2527CrossRefGoogle Scholar
  25. 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 14:205CrossRefGoogle Scholar
  26. 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:e0161CrossRefGoogle Scholar
  27. 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 18:1509–1517CrossRefGoogle Scholar
  28. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628CrossRefGoogle Scholar
  29. 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 55:798–809CrossRefGoogle Scholar
  30. 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 18:1961–1974CrossRefGoogle Scholar
  31. 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 500:335–339CrossRefGoogle Scholar
  32. 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 156:564–584CrossRefGoogle Scholar
  33. 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 28:511–515CrossRefGoogle Scholar
  34. 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 68:1014–1027CrossRefGoogle Scholar
  35. 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:e49CrossRefGoogle Scholar
  36. 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 92:179–186CrossRefGoogle Scholar
  37. 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 5:584–589Google Scholar
  38. 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 6:1–11CrossRefGoogle Scholar
  39. 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 223:5–9CrossRefGoogle Scholar
  40. 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:e0154882CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Coconut Research Institute, CATASWenchangPeople’s Republic of China
  2. 2.Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, Institute of Tropical Agriculture and ForestryHainan UniversityHaikouPeople’s Republic of China
  3. 3.MOA Key Laboratory of Tropical Crop Biology and Genetic Resources UtilizationInstitute of Tropical Bioscience and Biotechnology, CATASHaikouPeople’s Republic of China
  4. 4.Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and NutritionJustus Liebig University GiessenGiessenGermany

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