Somaclonal variation arises in plants and animals when differentiated somatic cells are induced into a pluripotent state, but the resulting clones differ from each other and from their parents. In agriculture, somaclonal variation has hindered the micropropagation of elite hybrids and genetically modified crops, but the mechanism responsible remains unknown1. The oil palm fruit ‘mantled’ abnormality is a somaclonal variant arising from tissue culture that drastically reduces yield, and has largely halted efforts to clone elite hybrids for oil production2,3,4. Widely regarded as an epigenetic phenomenon5, ‘mantling’ has defied explanation, but here we identify the MANTLED locus using epigenome-wide association studies of the African oil palm Elaeis guineensis. DNA hypomethylation of a LINE retrotransposon related to rice Karma, in the intron of the homeotic gene DEFICIENS, is common to all mantled clones and is associated with alternative splicing and premature termination. Dense methylation near the Karma splice site (termed the Good Karma epiallele) predicts normal fruit set, whereas hypomethylation (the Bad Karma epiallele) predicts homeotic transformation, parthenocarpy and marked loss of yield. Loss of Karma methylation and of small RNA in tissue culture contributes to the origin of mantled, while restoration in spontaneous revertants accounts for non-Mendelian inheritance. The ability to predict and cull mantling at the plantlet stage will facilitate the introduction of higher performing clones and optimize environmentally sensitive land resources.

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Gene Expression Omnibus

Data deposits

Microarray data have been deposited in the NCBI Gene Expression Omnibus (GEO) and are accessible through GEO Series accession number GSE68410. Small RNA sequence data from the region of interest have been deposited in the NCBI Sequence Read Archive (SRA) database under the accession numbers SAMN03569290SAMN03569351. Whole-genome bisulfite sequence data have been deposited in the NCBI SRA under accession numbers SAMN03569063SAMN03569077. The cDNA sequence of the kDEF1 transcript has been deposited in GenBank under accession number KR347486.


  1. 1.

    et al. Plants regenerated from tissue culture contain stable epigenome changes in rice. Elife 2, e00354 (2013)

  2. 2.

    in CRC Handbook of Fruit Set and Development (ed. Monselise, S. P.) 253–259 (CRC Press, 1986)

  3. 3.

    The ‘mantled’ oil palm (Elaeis guineensis Jacq.). J. W. Afr. Inst. Oil Palm Res. 5, 31–33 (1973)

  4. 4.

    & Somaclonal variation associated with oil palm (Elaeis guineensis Jacq.) clonal propagation: a review. Afr. J. Biotechnol. 13, 989–997 (2014)

  5. 5.

    , , , & Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis. Plant Cell Rep. 19, 684–690 (2000)

  6. 6.

    & in Plantation Management for the 21st Century (ed. Pushparajah, E.) 279–289 (Incorp. Soc. Planters, 1997)

  7. 7.

    et al. The oil palm SHELL gene controls oil yield and encodes a homologue of SEEDSTICK. Nature 500, 340–344 (2013)

  8. 8.

    et al. Functional characterization of MADS box genes involved in the determination of oil palm flower structure. J. Exp. Bot. 58, 1245–1259 (2007)

  9. 9.

    & Preliminary evidence of a genetic cause for the floral abnormalities in some oil palm ramets. Elaies 2, 199–207 (1990)

  10. 10.

    , , & Variation in oil palm (Elaeis guineensis Jacq.) tissue culture-derived regenerants revealed by AFLPs with methylation-sensitive enzymes. Theor. Appl. Genet. 102, 971–979 (2001)

  11. 11.

    , , & Retroelements, transposons and methylation status in the genome of oil palm (Elaeis guineensis) and the relationship to somaclonal variation. Plant Mol. Biol. 52, 69–79 (2003)

  12. 12.

    et al. DNA methylation and expression of the EgDEF1 gene and neighboring retrotransposons in mantled somaclonal variants of oil palm. PLoS ONE 9, e91896 (2014)

  13. 13.

    et al. Characterization of oil palm MADS box genes in relation to the mantled flower abnormality. Plant Cell Tissue Organ Cult. 85, 331–344 (2006)

  14. 14.

    et al. Oil palm genome sequence reveals divergence of interfertile species in Old and New worlds. Nature 500, 335–339 (2013)

  15. 15.

    et al. Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471–476 (2004)

  16. 16.

    et al. Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol. 6, e302 (2008)

  17. 17.

    , & Two-step regulation and continuous retrotransposition of the rice LINE-type retrotransposon Karma. Plant Cell 15, 1934–1944 (2003)

  18. 18.

    et al. Control of transposon activity by a histone H3K4 demethylase in rice. Proc. Natl Acad. Sci. USA 110, 1953–1958 (2013)

  19. 19.

    , , & Somatically heritable switches in the DNA modification of Mu transposable elements monitored with a suppressible mutant in maize. Genes Dev. 4, 331–343 (1990)

  20. 20.

    , & An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157–161 (1999)

  21. 21.

    & Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J. 26, 3641–3652 (2007)

  22. 22.

    , , & Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122, 3433–3441 (1996)

  23. 23.

    et al. The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res. 23, 1651–1662 (2013)

  24. 24.

    , , & Meristem-specific expression of epigenetic regulators safeguards transposon silencing in Arabidopsis. EMBO Rep. 15, 446–452 (2014)

  25. 25.

    et al. Pathogenic exon-trapping by SVA retrotransposon and rescue in Fukuyama muscular dystrophy. Nature 478, 127–131 (2011)

  26. 26.

    et al. Control of alternative splicing through siRNA-mediated transcriptional gene silencing. Nature Struct. Mol. Biol. 16, 717–724 (2009)

  27. 27.

    et al. RNA-mediated trans-communication can establish paramutation at the b1 locus in maize. Proc. Natl Acad. Sci. USA 107, 12986–12991 (2010)

  28. 28.

    & Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc. Natl Acad. Sci. USA 100, 6558–6563 (2003)

  29. 29.

    et al. Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J. 9, 605–613 (1990)

  30. 30.

    , & The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68, 683–697 (1992)

  31. 31.

    Propagation of clonal oil palms by tissue culture. Planter 50, 374–381 (1974)

  32. 32.

    & Multiplication vegetative du palmier a huile (Elaeis guineensis Jacq.) a l’aide de cultures de tissues foliares. C. R. Acad. Sci. Paris. Ser. D 283, 1735–1737 (1976)

  33. 33.

    , , & Oil palm (Elaeis guineensis Jacq.) plantations in Cote-d’Ivoire obtained through in vitro culture. First results. Oléagineux 45, 10–11 (1990)

  34. 34.

    et al. Current status of oil palm tissue culture in Malaysia. In Proceedings of the Clonal and Quality Replanting Material Workshop. Towards Increasing the Annual National Productivity by One Tonne FFB/ha/year 3–14 (Malaysian Palm Oil Board, 2006)

  35. 35.

    et al. in Advances in Oil Palm Research (eds Yusof, B., Jalani, B. S. & Chan, K. W.) 238–283 (Malaysian Palm Oil Board, 2000)

  36. 36.

    et al. Determination of flower structure in Elaeis guineensis: do palms use the same homeotic genes as other species? Ann. Bot. 100, 1–12 (2007)

  37. 37.

    & Dependence of McrBC cleavage on distance between recognition elements. Biol. Chem. 379, 611–616 (1998)

  38. 38.

    et al. Comprehensive DNA methylation profiling in a human cancer genome identifies novel epigenetic targets. Carcinogenesis 27, 2409–2423 (2006)

  39. 39.

    et al. Evaluation of reference genes for quantitative real-time PCR in oil palm elite planting materials propagated by tissue culture. PLoS ONE 9, e99774 (2014)

  40. 40.

    et al. Epigenetic imbalance and the floral developmental abnormality of the in vitro-regenerated oil palm Elaeis guineensis. Ann. Bot. 108, 1453–1462 (2011)

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We acknowledge the contributions of staff members of the Breeding and Tissue Culture Unit at MPOB for creating the valuable clonal lines, and for their extensive data collection and sampling efforts. We thank Genomics Unit at MPOB for conducting DNA fingerprinting to verify clonal lines. We thank The McDonnell Genome Institute at Washington University for genomic bisulfite sequencing and transcriptome sequencing support, and MOgene for microarray hybridizations. At Orion Genomics, we thank N. Sander, J. Reed, J. Brune, K. Soe, J. McDonald, C. Brown and B. Dove for technical support, and M.-F. Wu and M. Sachdeva for assistance with the manuscript and additional informatics support. We would also like to thank T. Dalmay for recommendations on sRNA library construction. We appreciate the constant support of the Director-General of MPOB, Datuk Dr. Yuen-May Choo, and the Ministry of Plantation Industries and Commodities, Malaysia.

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Author notes

    • Michael Hogan

    Present address: Thermo Fisher Scientific, 110 Miller Avenue, Ann Arbor, Michigan 48104, USA.


  1. Malaysian Palm Oil Board, 6, Persiaran Institusi, Bandar Baru Bangi, 43000 Kajang, Selangor, Malaysia

    • Meilina Ong-Abdullah
    • , Siew-Eng Ooi
    • , Sau-Yee Kok
    • , Norashikin Sarpan
    • , Nuraziyan Azimi
    • , Ahmad Tarmizi Hashim
    • , Zamzuri Ishak
    • , Samsul Kamal Rosli
    • , Fadila Ahmad Malike
    • , Nor Azwani Abu Bakar
    • , Marhalil Marjuni
    • , Norziha Abdullah
    • , Zulkifli Yaakub
    • , Mohd Din Amiruddin
    • , Rajanaidu Nookiah
    • , Rajinder Singh
    • , Eng-Ti Leslie Low
    • , Kuang-Lim Chan
    • , Norazah Azizi
    •  & Ravigadevi Sambanthamurthi
  2. Orion Genomics, 4041 Forest Park Avenue, St Louis, Missouri 63108, USA

    • Jared M. Ordway
    • , Nan Jiang
    • , Steven W. Smith
    • , Blaire Bacher
    • , Muhammad A. Budiman
    • , Andrew Van Brunt
    • , Corey Wischmeyer
    • , Melissa Beil
    • , Michael Hogan
    •  & Nathan Lakey
  3. United Plantations Berhad, Jendarata Estate, 36009 Teluk Intan, Perak, Malaysia

    • Chin-Ching Lim
    •  & Xaviar Arulandoo
  4. Applied Agricultural Resources Sdn Bhd, No. 11, Jalan Teknologi 3/6, Taman Sains Selangor 1, 47810 Kota Damansara, Petaling Jaya, Selangor, Malaysia

    • Choo-Kien Wong
    • , Chin-Nee Choo
    •  & Wei-Chee Wong
  5. FELDA Global Ventures R&D Sdn Bhd, c/o FELDA Biotechnology Centre, PT 23417, Lengkuk Teknologi, 71760 Bandar Enstek, Negeri Sembilan, Malaysia

    • Yen-Yen Kwan
    •  & Sharifah Shahrul Rabiah Syed Alwee
  6. Howard Hughes Medical Institute-Gordon and Betty Moore Foundation, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA

    • Robert A. Martienssen


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M.O.-A. led the work on the MANTLED marker/gene. M.O.-A., R.Si., E.-T.L.L. and R.Sa. conceptualized the research programme. M.O.-A., R.Si., E.-T.L.L., R.N., N.L., S.W.S., J.M.O., R.Sa. and R.A.M. developed the overall strategy, designed experiments and coordinated the project. A.T.H., Z.I. and S.K.R. performed tissue culture on selected ortets and field-planted the ramets. Field data collection and fruit bunch census were conducted at various research stations by F.A.M., N.A.A.B., M.M., N.A., Z.Y. and M.D.A. M.O.-A., C.-C.L., X.A., C.-N.C., W.-C.W., S.S.R.S.A. and Y.-Y.K. identified samples for discovery and validation panels. M.O.-A., C.-C.L. and X.A. identified materials used in the mosaic experiments. M.O.-A., S.-E.O., S.-Y.K., N.S. and N.A. conducted laboratory experiments, histological staging of inflorescences and data analyses. N.J. and S.W.S performed microarray analyses. B.B. and M.A.B. prepared fractions for microarray hybridizations. B.B. designed and analysed qPCR experiments. B.B. and M.B. performed qPCR assays. A.V.B. designed and analysed clone-based bisulfite sequencing experiments, and A.V.B. and M.B. performed bisulfite sequencing assays. M.B. designed and performed qRT–PCR experiments. C.W. and J.M.O. analysed transcriptome data. K.-L.C., N.A., S.W.S., M.H., C.W. and A.V.B. provided bioinformatics support. M.O.-A., R.Si., E.-T.L.L., R.N., N.L., S.W.S., J.M.O., R.Sa. and R.A.M. prepared and revised the manuscript.

Competing interests

R.A.M. is a former consultant of Orion Genomics, LLC.

Corresponding authors

Correspondence to Ravigadevi Sambanthamurthi or Robert A. Martienssen.

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