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Research Article

Genome of wild olive and the evolution of oil biosynthesis

Turgay Unver, Zhangyan Wu, Lieven Sterck, Mine Turktas, Rolf Lohaus, Zhen Li, Ming Yang, Lijuan He, Tianquan Deng, Francisco Javier Escalante, Carlos Llorens, Francisco J. Roig, Iskender Parmaksiz, Ekrem Dundar, Fuliang Xie, Baohong Zhang, Arif Ipek, Serkan Uranbey, Mustafa Erayman, Emre Ilhan, Oussama Badad, Hassan Ghazal, David A. Lightfoot, Pavan Kasarla, Vincent Colantonio, Huseyin Tombuloglu, Pilar Hernandez, Nurengin Mete, Oznur Cetin, Marc Van Montagu, Huanming Yang, Qiang Gao, Gabriel Dorado, and Yves Van de Peer
PNAS October 31, 2017 114 (44) E9413-E9422; first published October 9, 2017; https://doi.org/10.1073/pnas.1708621114
Turgay Unver
aİzmir International Biomedicine and Genome Institute, Dokuz Eylül University, 35340 İzmir, Turkey;
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  • For correspondence: turgayunver@icloud.com marc.vanmontagu@ugent.be yves.vandepeer@psb.vib-ugent.be
Zhangyan Wu
bBGI Shenzhen, 518038 Shenzhen, China;
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Lieven Sterck
cDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium;
dCenter for Plant Systems Biology, VIB, 9052 Ghent, Belgium;
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Mine Turktas
eDepartment of Biology, Faculty of Science, Cankiri Karatekin University, 18100 Cankiri, Turkey;
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Rolf Lohaus
cDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium;
dCenter for Plant Systems Biology, VIB, 9052 Ghent, Belgium;
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Zhen Li
cDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium;
dCenter for Plant Systems Biology, VIB, 9052 Ghent, Belgium;
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Ming Yang
bBGI Shenzhen, 518038 Shenzhen, China;
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Lijuan He
bBGI Shenzhen, 518038 Shenzhen, China;
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Tianquan Deng
bBGI Shenzhen, 518038 Shenzhen, China;
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Francisco Javier Escalante
fPlataforma de Genómica y Bioinformática de Andalucía, 41013 Sevilla, Spain;
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Carlos Llorens
gBiotechvana, 46980 Paterna (Valencia), Spain;
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Francisco J. Roig
gBiotechvana, 46980 Paterna (Valencia), Spain;
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Iskender Parmaksiz
hDepartment of Molecular Biology and Genetics, Faculty of Science, Gaziosmanpasa University, 60250 Tokat, Turkey;
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Ekrem Dundar
iDepartment of Molecular Biology and Genetics, Faculty of Science, Balikesir University, 10145 Balikesir, Turkey;
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Fuliang Xie
jDepartment of Biology, East Carolina University, Greenville, NC 27858;
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Baohong Zhang
jDepartment of Biology, East Carolina University, Greenville, NC 27858;
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Arif Ipek
eDepartment of Biology, Faculty of Science, Cankiri Karatekin University, 18100 Cankiri, Turkey;
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Serkan Uranbey
kDepartment of Field Crops, Faculty of Agriculture, Ankara University, 06120 Ankara, Turkey;
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Mustafa Erayman
lDepartment of Biology, Faculty of Arts and Science, Mustafa Kemal University, 31060 Hatay, Turkey;
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Emre Ilhan
lDepartment of Biology, Faculty of Arts and Science, Mustafa Kemal University, 31060 Hatay, Turkey;
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Oussama Badad
mLaboratory of Plant Physiology, University Mohamed V, 10102 Rabat, Morocco;
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Hassan Ghazal
nPolydisciplinary Faculty of Nador, University Mohamed Premier, 62700 Nador, Morocco;
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David A. Lightfoot
oDepartment of Plant, Soil and Agricultural Systems, Southern Illinois University, Carbondale, IL 62901;
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Pavan Kasarla
oDepartment of Plant, Soil and Agricultural Systems, Southern Illinois University, Carbondale, IL 62901;
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Vincent Colantonio
oDepartment of Plant, Soil and Agricultural Systems, Southern Illinois University, Carbondale, IL 62901;
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Huseyin Tombuloglu
pInstitute for Research and Medical Consultation, University of Dammam, 34212 Dammam, Saudi Arabia;
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Pilar Hernandez
qInstituto de Agricultura Sostenible, Consejo Superior de Investigaciones Científicas, 14004 Córdoba, Spain;
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Nurengin Mete
rOlive Research Institute of Bornova, 35100 Izmir, Turkey;
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Oznur Cetin
rOlive Research Institute of Bornova, 35100 Izmir, Turkey;
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Marc Van Montagu
cDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium;
dCenter for Plant Systems Biology, VIB, 9052 Ghent, Belgium;
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  • For correspondence: turgayunver@icloud.com marc.vanmontagu@ugent.be yves.vandepeer@psb.vib-ugent.be
Huanming Yang
bBGI Shenzhen, 518038 Shenzhen, China;
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Qiang Gao
bBGI Shenzhen, 518038 Shenzhen, China;
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Gabriel Dorado
sDepartamento Bioquímica y Biología Molecular, Campus de Excelencia Internacional Agroalimentario, Universidad de Córdoba, 14071 Córdoba, Spain;
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Yves Van de Peer
cDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium;
dCenter for Plant Systems Biology, VIB, 9052 Ghent, Belgium;
tDepartment of Genetics, Genomics Research Institute, University of Pretoria, Pretoria 0028, South Africa
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  • For correspondence: turgayunver@icloud.com marc.vanmontagu@ugent.be yves.vandepeer@psb.vib-ugent.be
  1. Contributed by Marc Van Montagu, September 11, 2017 (sent for review May 26, 2017; reviewed by Ray Ming and Korbinian Schneeberger)

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Significance

We sequenced the genome and transcriptomes of the wild olive (oleaster). More than 50,000 genes were predicted, and evidence was found for two relatively recent whole-genome duplication events, dated at approximately 28 and 59 Mya. Whole-genome sequencing, as well as gene expression studies, provide further insights into the evolution of oil biosynthesis, and will aid future studies aimed at further increasing the production of olive oil, which is a key ingredient of the healthy Mediterranean diet and has been granted a qualified health claim by the US Food and Drug Administration.

Abstract

Here we present the genome sequence and annotation of the wild olive tree (Olea europaea var. sylvestris), called oleaster, which is considered an ancestor of cultivated olive trees. More than 50,000 protein-coding genes were predicted, a majority of which could be anchored to 23 pseudochromosomes obtained through a newly constructed genetic map. The oleaster genome contains signatures of two Oleaceae lineage-specific paleopolyploidy events, dated at ∼28 and ∼59 Mya. These events contributed to the expansion and neofunctionalization of genes and gene families that play important roles in oil biosynthesis. The functional divergence of oil biosynthesis pathway genes, such as FAD2, SACPD, EAR, and ACPTE, following duplication, has been responsible for the differential accumulation of oleic and linoleic acids produced in olive compared with sesame, a closely related oil crop. Duplicated oleaster FAD2 genes are regulated by an siRNA derived from a transposable element-rich region, leading to suppressed levels of FAD2 gene expression. Additionally, neofunctionalization of members of the SACPD gene family has led to increased expression of SACPD2, 3, 5, and 7, consequently resulting in an increased desaturation of steric acid. Taken together, decreased FAD2 expression and increased SACPD expression likely explain the accumulation of exceptionally high levels of oleic acid in olive. The oleaster genome thus provides important insights into the evolution of oil biosynthesis and will be a valuable resource for oil crop genomics.

  • oil crop
  • whole-genome duplication
  • siRNA regulation
  • fatty-acid biosynthesis
  • polyunsaturated fatty-acid pathway

Footnotes

  • ↵1T.U. and Z.W. contributed equally to this work.

  • ↵2Present address: Egitim Mah, Ekrem Guer Sok, No:26/3, 35340 Balcova, Izmir, Turkey.

  • ↵3To whom correspondence may be addressed. Email: turgayunver{at}icloud.com, marc.vanmontagu{at}ugent.be, or yves.vandepeer{at}psb.vib-ugent.be.
  • Author contributions: T.U., M.V.M., G.D., and Y.V.d.P. designed research; T.U., Z.W., L.S., M.T., R.L., Z.L., M.Y., F.J.E., C.L., F.J.R., E.D., F.X., B.Z., O.B., H.G., D.A.L., P.K., V.C., H.T., P.H., N.M., O.C., G.D., and Y.V.d.P. performed research; T.U., Z.W., L.S., M.T., R.L., Z.L., M.Y., F.J.E., C.L., F.J.R., E.D., F.X., B.Z., O.B., H.G., D.A.L., P.K., V.C., H.T., P.H., N.M., O.C., G.D., and Y.V.d.P. analyzed data; T.U., L.S., R.L., G.D., and Y.V.d.P. wrote the paper; Z.W., M.T., M.Y., L.H., T.D., I.P., A.I., S.U., M.E., E.I., N.M., H.Y., and Q.G. contributed data production; and T.U., G.D., and Y.V.d.P. contributed to the project leadership.

  • Reviewers: R.M., University of Illinois at Urbana–Champaign; and K.S., MPI for Plant Breeding Research.

  • The authors declare no conflict of interest.

  • Data deposition: The oleaster genome assembly has been deposited in the GenBank database, https://www.ncbi.nlm.nih.gov/genbank (accession no. MSRW00000000; BioProject record ID PRJNA350614). Transcriptome datasets were deposited in the at National Center for Biotechnology Information Sequence Read Archive, https://www.ncbi.nlm.nih.gov/sra (accession nos. SRR4473639, SRR4473641, SRR44742, SRR4473643, SRR4473644, SRR4473645, SRR4473646, and SRR4473647). The genome and annotation files were uploaded to Online Resource for Community Annotation of Eukaryotes (ORCAE), bioinformatics.psb.ugent.be/orcae; Phytozome, https://phytozome.jgi.doe.gov; and the olive genome consortium Web site, olivegenome.org. .

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1708621114/-/DCSupplemental.

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Wild olive genome and oil biosynthesis
Turgay Unver, Zhangyan Wu, Lieven Sterck, Mine Turktas, Rolf Lohaus, Zhen Li, Ming Yang, Lijuan He, Tianquan Deng, Francisco Javier Escalante, Carlos Llorens, Francisco J. Roig, Iskender Parmaksiz, Ekrem Dundar, Fuliang Xie, Baohong Zhang, Arif Ipek, Serkan Uranbey, Mustafa Erayman, Emre Ilhan, Oussama Badad, Hassan Ghazal, David A. Lightfoot, Pavan Kasarla, Vincent Colantonio, Huseyin Tombuloglu, Pilar Hernandez, Nurengin Mete, Oznur Cetin, Marc Van Montagu, Huanming Yang, Qiang Gao, Gabriel Dorado, Yves Van de Peer
Proceedings of the National Academy of Sciences Oct 2017, 114 (44) E9413-E9422; DOI: 10.1073/pnas.1708621114

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Wild olive genome and oil biosynthesis
Turgay Unver, Zhangyan Wu, Lieven Sterck, Mine Turktas, Rolf Lohaus, Zhen Li, Ming Yang, Lijuan He, Tianquan Deng, Francisco Javier Escalante, Carlos Llorens, Francisco J. Roig, Iskender Parmaksiz, Ekrem Dundar, Fuliang Xie, Baohong Zhang, Arif Ipek, Serkan Uranbey, Mustafa Erayman, Emre Ilhan, Oussama Badad, Hassan Ghazal, David A. Lightfoot, Pavan Kasarla, Vincent Colantonio, Huseyin Tombuloglu, Pilar Hernandez, Nurengin Mete, Oznur Cetin, Marc Van Montagu, Huanming Yang, Qiang Gao, Gabriel Dorado, Yves Van de Peer
Proceedings of the National Academy of Sciences Oct 2017, 114 (44) E9413-E9422; DOI: 10.1073/pnas.1708621114
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