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; Yves Van de Peer

doi:10.1073/pnas.1708621114

New Research In

Contributed by Marc Van Montagu, September 11, 2017 (sent for review May 26, 2017; reviewed by Ray Ming and Korbinian Schneeberger)

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.

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.