Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm

Abstract

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 micropropagation of elite hybrids and genetically modified crops, but the mechanism remains a mystery1. The oil palm fruit abnormality, mantled, is a somaclonal variant arising from tissue culture that drastically reduces yield, and has largely halted efforts to clone elite hybrids for oil production2–4. Widely regarded as epigenetic5, mantling has defied explanation, but here we identify the MANTLED gene using Epigenome Wide Association Studies. 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 (the Good Karma epiallele) predicts normal fruit set, while hypomethylation (the Bad Karma epiallele) predicts homeotic transformation, parthenocarpy and dramatic loss of yield. Loss of Karma methylation and 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.

Genetic Fidelity Testing Using SSR Marker Assay Confirms Trueness to Type of Micropropagated Coconut (Cocos nucifera L.) Plantlets Derived from Unfertilized Ovaries

“…This is claimed to be a somaclonal variation resulting in a conversion of the male floral organs into supernumerary carpels [27] and may lead to partial or complete flower sterility, depending on the severity of the abnormality [26]. It has been reported that hypo-methylation during tissue culture contributes to the origin of this 'mantled' phenotype in tissue culture effectively preventing the clonal propagation from elite palms [28]. In our study, the coconut plantlets were derived through somatic embryogensis and a prolonged callus phase was introduced by multiplying callus in two additional cycles.…”

The effect of transposable elements on phenotypic variation: insights from plants to humans

“…In normal fruits, the Karma insertion at the intron of EgDEF1 is hypermethylated (Good Karma) and EgDEF1 produces full-length transcripts. By contrast, hypomethylated Karma (Bad Karma) mediates alternative splicing of EgDEF1 to yield truncated transcripts responsible for the mantled-fruit phenotype (Ong-Abdullah et al, 2015). Therefore, weeding out plants carrying the Bad Karma epiallele at the plantlet stage provides an effective means to improve oil palm yield (Ong-Abdullah et al, 2015;Paszkowski, 2015).…”

“…By contrast, hypomethylated Karma (Bad Karma) mediates alternative splicing of EgDEF1 to yield truncated transcripts responsible for the mantled-fruit phenotype (Ong-Abdullah et al, 2015). Therefore, weeding out plants carrying the Bad Karma epiallele at the plantlet stage provides an effective means to improve oil palm yield (Ong-Abdullah et al, 2015;Paszkowski, 2015). The interplay between alternative splicing and DNA methylation reveals another mechanism for regulating gene expression and phenotypic variation in plants.…”

“…The null allele e resulted from an insertional mutation in the coding region of FAE1 by a 3,100 bp PIF/Harbinger-like DNA TE, causing zero erucic contents (Zeng and Cheng, 2014). Recent work described a fascinating example of TE-induced epigenetic alleles, the Karma-mediated epiallele of EgDEF1, which causes the defective "mantled" trait in vegetative propagation of oil palm (Elaeis guineensis) cultivars (Ong-Abdullah et al, 2015). EgDEF1 encodes a MADS-box transcription factor essential for the formation of flower organs, like its ortholog, Arabidopsis APETALA3 (AP3) (Adam et al, 2007).…”

High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development

“…Several studies have demonstrated that local DNA methylation variants, which are represented by differential cytosine methylation at particular loci, can have major effects on the transcription of nearby genes and can be inherited over generations [18][19][20] .…”