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Hypomethylation of karma transposon causes catastrophic mantled epi-mutation in oil palm

Study published in Nature reveals epigenetic cause of mantling, seen in oil palms cloned from top-performing plants

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IMAGE: Somaclonal variation among otherwise highly productive oil palm clones raises sustainability concerns. Karma transposon DNA methylation and splicing of a homeotic gene controls mantled ('Bad Karma') and normal ('Good Karma')... view more

Credit: Meilina Ong Abdullah, MPOB

A multinational team of researchers from the Malaysian Palm Oil Board in Selangor, Orion Genomics in St. Louis and Cold Spring Harbor Laboratory in New York, has identified a novel epigenetic mechanism - called Bad Karma - that explains mantling, a catastrophic phenotype which occurs in a significant but unpredictable portion of oil palms that are propagated by cloning. Although mantled palms are genetically identical to their high performing parent, their fruit is abnormally disfigured and often sterile. The epi-mutation that causes the abnormality also results in dramatically reduced oil yields. The risk of field planting clonal palms only to learn years later, when the palms begin to fruit, that they will not be productive has largely halted efforts to clone elite hybrids. In a paper published online September 9 ahead of print in Nature, the researchers identified that the loss of DNA methylation of the oil palm Karma transposon embedded within an important flowering transcription factor gene, disrupts normal splicing of the gene and causes the mantled phenotype. The discovery has led to the development of a simple, leaf-based test that can predict the mantling phenotype at a stage before palms are planted in the field, years before the phenotype would normally appear. The new precision agriculture approach will enable the exclusive cultivation of high-performing clonal oil palms, further optimizing the use of environmentally sensitive land resources.

"Decades ago, the development of tissue culture techniques provided promise to growers that they could significantly increase the yield of plantations by cultivating palms which are genetically identical to the highest performing palms," noted Meilina Ong-Abdullah, Ph.D., Head of the Breeding and Tissue Culture Unit of the Malaysian Palm Oil Board (MPOB) and lead author on the paper. "However, inexplicably and unpredictably, a significant portion of the resulting plants had a low-yielding mantled characteristic and were not commercially viable, thereby limiting the cultivation of clonal palms. The Bad Karma finding has solved a problem that has puzzled researchers and hampered the adoption of advanced propagation techniques for almost three decades."

Although the crop is planted on 5 percent of the land dedicated to producing vegetable oil, the African and South American oil palms, Elaeis guineensis and E. oleifera, respectively, together account for 45 percent of the edible oil production worldwide. The crop is also the most efficient producer of oil, yielding ten times more oil per unit of land than soybean. However, oil palm grows in the tropics, and its expanded cultivation can threaten sensitive habitats. Advancements that enable increased yields on existing planted area can help increase the sustainability of oil palm cultivation.

"Typically, palms that are propagated through tissue culture are clones of the best hybrid trees with yields that are 20 to 30 percent higher than trees propagated through seeds," said Ravigadevi Sambanthamurthi, Ph.D., Director of the Advanced Breeding and Biotechnology Centre of MPOB and co-corresponding author of the study. "But the threat of mantling has severely limited the cultivation of clonal palms to approximately one percent of land committed to oil palm. By identifying and culling mantled palms at the nursery stage, one could expect a rapid expansion of the use of clonal palms, and up to a 30 percent increase in yield across relevant planted areas."

To understand the mechanism behind mantling, the researchers used a novel DNA methylation profiling technology to perform the first epigenome-wide association study in any plant, which resulted in the identification of a single trait-causing locus, in this case a transposable element embedded within a key oil palm flowering gene, that was responsible for the mantled phenotype. The authors found that in mantled palms, the Karma transposon has significantly lower DNA methylation than in normal clonal and non-clonal palms. This decrease of DNA methylation in turn triggers the aberrant mRNA splicing of the flowering gene transcript into the repetitive element, resulting in a dominant but truncated protein causing the mantling phenotype. The identification of a single differentially methylated locus for MANTLED provides an opportunity to develop a DNA test that would identify defective palms from a simple leaf punch at the nursery stage, before they are planted in the 25-year cultivation cycle.

The research builds upon work published in 2013 in Nature detailing the sequencing of the oil palm and the identification of the gene SHELL, which is responsible for a 30 percent yield increase in hybrid palms.

"In the space of just over two years, the breakthrough research that MPOB and Orion Genomics have accomplished has provided mechanisms to develop tools that promise to dramatically increase the yield and thereby sustainability of the oil palm industry," said Datuk Dr. Choo Yuen May, Director General of MPOB, which funded and led the research reported. "The success of MPOB's genome program is in part credited to the close working relationship it has with members of the oil palm industry."

Rob Martienssen, Ph.D., scientific co-founder of Orion Genomics, who is a Professor of plant genetics at Cold Spring Harbor Laboratory in New York, added, "while the importance of these findings for creating a more sustainable palm oil industry cannot be understated, a particularly compelling implication of this work is that it provides an epigenetic explanation for somaclonal variation, which is the technical term for when a clone differs from its genetically identical parent. The finding that transposons and small RNA are responsible for somaclonal variation builds on decades of research in epigenetics, going back to Barbara McClintock's work on maize at Cold Spring Harbor. The technology we used will have widespread applicability to similar phenomena in many important crops."

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About Oil Palm

Oil palm is the most productive oil-bearing crop, which accounts for 33 percent of vegetable oil, and 45 percent of edible oil worldwide. The oil palm is 10 times more productive than soybean, the second most productive oil crop. Additionally, palm oil based biodiesel is in use across the globe, and biomass from the oil palm plant has applicability as a renewable biofuel, as well.

About the Malaysian Palm Oil Board

The Malaysian Palm Oil Board (MPOB) is a Malaysian government agency dedicated to serving the country's palm oil industry. The agency envisions the development of a highly diversified, globally competitive and sustainable oil palm industry. MPOB is focused on improving production efficiency and the quality of palm oil-derived products, optimizing land use in oil palm areas and finding new uses for palm oil derivatives. The Malaysian government halted the conversion of new forest land for agriculture, including oil palm, in the 1990s. It has also committed to preserve 50 percent of its total land area as forest. To meet increased demand for the palm oil, the Malaysian government converted colonial rubber and cocoa plantations to oil palm plantations.

About Orion Genomics

Orion Genomics LLC is a St. Louis-based biotechnology company that develops epigenetic and genomic research tools and molecular diagnostics to help fulfill the promise of personalized medicine and precision agriculture. The company's lead diagnostic product is a simple epigenetic blood test, in late-stage clinical trials, that identifies people at elevated risk of developing colorectal cancer in the future. Orion's proprietary precision agricultural tests are being marketed to the tropical plantation agricultural sector world-wide through its subsidiary companies. Through the company's services division, Orion offers genomics research and assay development services to the medical, agricultural and bio-fuels research communities.

Nature Citations and Funding

Ong-Abdullah, Sambanthamurthi, Martienssen and other coauthors of "Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm," Nature (doi 10.1038/nature15365) include investigators from MPOB, the oil palm industry and Orion Genomics. The project was endorsed by the Malaysian Cabinet Committee on the Competitiveness of the Palm Oil Industry (CCPO) and funded by a contract between Orion Genomics and MPOB.

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