Genome of wild olive and the evolution of oil biosynthesis

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 o...

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 44; pp. E9413 - E9422
Main Authors:	Unver, Turgay, Wu, Zhangyan, Sterck, Lieven, Turktas, Mine, Lohaus, Rolf, Li, Zhen, Yang, Ming, He, Lijuan, Deng, Tianquan, Escalante, Francisco Javier, Llorens, Carlos, Roig, Francisco J., Parmaksiz, Iskender, Dundar, Ekrem, Xie, Fuliang, Zhang, Baohong, Ipek, Arif, Uranbey, Serkan, Erayman, Mustafa, Ilhan, Emre, Badad, Oussama, Ghazal, Hassan, Lightfoot, David A., Kasarla, Pavan, Colantonio, Vincent, Tombuloglu, Huseyin, Hernandez, Pilar, Mete, Nurengin, Cetin, Oznur, Van Montagu, Marc, Yang, Huanming, Gao, Qiang, Dorado, Gabriel, Van de Peer, Yves
Format:	Journal Article
Language:	English
Published:	United States National Academy of Sciences 31-10-2017
Series:	PNAS Plus
Subjects:	Accumulation Annotations Biological Evolution Biological Sciences Biosynthesis Biosynthetic Pathways - genetics Crops Desaturation Divergence Evolution FAD2 gene Fatty Acid Desaturases - genetics Fatty acids Fruit trees Gene duplication Gene expression Gene Expression - genetics Gene families Genes Genome, Plant - genetics Genomics Linoleic Acids - genetics Nucleotide sequence Oils - metabolism Olea - genetics Olea - metabolism Olea europaea sylvestris Oleic acid Oleic Acid - genetics Olive oil Olives PNAS Plus Reproduction (copying) RNA, Small Interfering - genetics siRNA Transposons Trees fatty-acid biosynthesis oil crop polyunsaturated fatty-acid pathway whole-genome duplication siRNA regulation
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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.
AbstractList	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.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. 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. 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. 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 aof 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. 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. Here we present the genome sequence and annotation of the wild olive tree ( var. ), 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 , , and , 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 genes are regulated by an siRNA derived from a transposable element-rich region, leading to suppressed levels of gene expression. Additionally, neofunctionalization of members of the gene family has led to increased expression of , , , and , consequently resulting in an increased desaturation of steric acid. Taken together, decreased expression and increased 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.
Author	Li, Zhen Wu, Zhangyan Turktas, Mine Kasarla, Pavan Van de Peer, Yves Van Montagu, Marc Parmaksiz, Iskender Llorens, Carlos Sterck, Lieven Ilhan, Emre Deng, Tianquan Dundar, Ekrem Zhang, Baohong Gao, Qiang Yang, Ming Ghazal, Hassan Yang, Huanming Uranbey, Serkan Colantonio, Vincent Dorado, Gabriel Lightfoot, David A. Ipek, Arif Badad, Oussama Unver, Turgay Escalante, Francisco Javier Cetin, Oznur He, Lijuan Tombuloglu, Huseyin Xie, Fuliang Lohaus, Rolf Roig, Francisco J. Erayman, Mustafa Mete, Nurengin Hernandez, Pilar
Author_xml	– sequence: 1 givenname: Turgay surname: Unver fullname: Unver, Turgay organization: İzmir International Biomedicine and Genome Institute, Dokuz Eylül University, 35340 İzmir, Turkey – sequence: 2 givenname: Zhangyan surname: Wu fullname: Wu, Zhangyan organization: BGI Shenzhen, 518038 Shenzhen, China – sequence: 3 givenname: Lieven surname: Sterck fullname: Sterck, Lieven organization: Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium – sequence: 4 givenname: Mine surname: Turktas fullname: Turktas, Mine organization: Department of Biology, Faculty of Science, Cankiri Karatekin University, 18100 Cankiri, Turkey – sequence: 5 givenname: Rolf surname: Lohaus fullname: Lohaus, Rolf organization: Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium – sequence: 6 givenname: Zhen surname: Li fullname: Li, Zhen organization: Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium – sequence: 7 givenname: Ming surname: Yang fullname: Yang, Ming organization: BGI Shenzhen, 518038 Shenzhen, China – sequence: 8 givenname: Lijuan surname: He fullname: He, Lijuan organization: BGI Shenzhen, 518038 Shenzhen, China – sequence: 9 givenname: Tianquan surname: Deng fullname: Deng, Tianquan organization: BGI Shenzhen, 518038 Shenzhen, China – sequence: 10 givenname: Francisco Javier surname: Escalante fullname: Escalante, Francisco Javier organization: Plataforma de Genómica y Bioinformática de Andalucía, 41013 Sevilla, Spain – sequence: 11 givenname: Carlos surname: Llorens fullname: Llorens, Carlos organization: Biotechvana, 46980 Paterna (Valencia), Spain – sequence: 12 givenname: Francisco J. surname: Roig fullname: Roig, Francisco J. organization: Biotechvana, 46980 Paterna (Valencia), Spain – sequence: 13 givenname: Iskender surname: Parmaksiz fullname: Parmaksiz, Iskender organization: Department of Molecular Biology and Genetics, Faculty of Science, Gaziosmanpasa University, 60250 Tokat, Turkey – sequence: 14 givenname: Ekrem surname: Dundar fullname: Dundar, Ekrem organization: Department of Molecular Biology and Genetics, Faculty of Science, Balikesir University, 10145 Balikesir, Turkey – sequence: 15 givenname: Fuliang surname: Xie fullname: Xie, Fuliang organization: Department of Biology, East Carolina University, Greenville, NC 27858 – sequence: 16 givenname: Baohong surname: Zhang fullname: Zhang, Baohong organization: Department of Biology, East Carolina University, Greenville, NC 27858 – sequence: 17 givenname: Arif surname: Ipek fullname: Ipek, Arif organization: Department of Biology, Faculty of Science, Cankiri Karatekin University, 18100 Cankiri, Turkey – sequence: 18 givenname: Serkan surname: Uranbey fullname: Uranbey, Serkan organization: Department of Field Crops, Faculty of Agriculture, Ankara University, 06120 Ankara, Turkey – sequence: 19 givenname: Mustafa surname: Erayman fullname: Erayman, Mustafa organization: Department of Biology, Faculty of Arts and Science, Mustafa Kemal University, 31060 Hatay, Turkey – sequence: 20 givenname: Emre surname: Ilhan fullname: Ilhan, Emre organization: Department of Biology, Faculty of Arts and Science, Mustafa Kemal University, 31060 Hatay, Turkey – sequence: 21 givenname: Oussama surname: Badad fullname: Badad, Oussama organization: Laboratory of Plant Physiology, University Mohamed V, 10102 Rabat, Morocco – sequence: 22 givenname: Hassan surname: Ghazal fullname: Ghazal, Hassan organization: Polydisciplinary Faculty of Nador, University Mohamed Premier, 62700 Nador, Morocco – sequence: 23 givenname: David A. surname: Lightfoot fullname: Lightfoot, David A. organization: Department of Plant, Soil and Agricultural Systems, Southern Illinois University, Carbondale, IL 62901 – sequence: 24 givenname: Pavan surname: Kasarla fullname: Kasarla, Pavan organization: Department of Plant, Soil and Agricultural Systems, Southern Illinois University, Carbondale, IL 62901 – sequence: 25 givenname: Vincent surname: Colantonio fullname: Colantonio, Vincent organization: Department of Plant, Soil and Agricultural Systems, Southern Illinois University, Carbondale, IL 62901 – sequence: 26 givenname: Huseyin surname: Tombuloglu fullname: Tombuloglu, Huseyin organization: Institute for Research and Medical Consultation, University of Dammam, 34212 Dammam, Saudi Arabia – sequence: 27 givenname: Pilar surname: Hernandez fullname: Hernandez, Pilar organization: Instituto de Agricultura Sostenible, Consejo Superior de Investigaciones Científicas, 14004 Córdoba, Spain – sequence: 28 givenname: Nurengin surname: Mete fullname: Mete, Nurengin organization: Olive Research Institute of Bornova, 35100 Izmir, Turkey – sequence: 29 givenname: Oznur surname: Cetin fullname: Cetin, Oznur organization: Olive Research Institute of Bornova, 35100 Izmir, Turkey – sequence: 30 givenname: Marc surname: Van Montagu fullname: Van Montagu, Marc organization: Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium – sequence: 31 givenname: Huanming surname: Yang fullname: Yang, Huanming organization: BGI Shenzhen, 518038 Shenzhen, China – sequence: 32 givenname: Qiang surname: Gao fullname: Gao, Qiang organization: BGI Shenzhen, 518038 Shenzhen, China – sequence: 33 givenname: Gabriel surname: Dorado fullname: Dorado, Gabriel organization: Departamento Bioquímica y Biología Molecular, Campus de Excelencia Internacional Agroalimentario, Universidad de Córdoba, 14071 Córdoba, Spain – sequence: 34 givenname: Yves surname: Van de Peer fullname: Van de Peer, Yves organization: Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium
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Copyright	Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Oct 31, 2017
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewers: R.M., University of Illinois at Urbana–Champaign; and K.S., MPI for Plant Breeding Research. 1T.U. and Z.W. contributed equally to this work. Contributed by Marc Van Montagu, September 11, 2017 (sent for review May 26, 2017; reviewed by Ray Ming and Korbinian Schneeberger) 2Present address: Egitim Mah, Ekrem Guer Sok, No:26/3, 35340 Balcova, Izmir, Turkey. 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.
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Snippet	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... Here we present the genome sequence and annotation of the wild olive tree ( var. ), called oleaster, which is considered an ancestor of cultivated olive trees.... 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...
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SubjectTerms	Accumulation Annotations Biological Evolution Biological Sciences Biosynthesis Biosynthetic Pathways - genetics Crops Desaturation Divergence Evolution FAD2 gene Fatty Acid Desaturases - genetics Fatty acids Fruit trees Gene duplication Gene expression Gene Expression - genetics Gene families Genes Genome, Plant - genetics Genomics Linoleic Acids - genetics Nucleotide sequence Oils - metabolism Olea - genetics Olea - metabolism Olea europaea sylvestris Oleic acid Oleic Acid - genetics Olive oil Olives PNAS Plus Reproduction (copying) RNA, Small Interfering - genetics siRNA Transposons Trees
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Title	Genome of wild olive and the evolution of oil biosynthesis
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