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Title: Evolutionary trajectory of Pack-MULEs is determined by their epigenetic status

item ZHAO, DONGYAN - Michigan State University
item HAMILTON, JOHN - Michigan State University
item VAILANCOURT, BRIEANNE - Michigan State University
item ZHANG, WENLI - Nanjing Agricultural University
item Eizenga, Georgia
item CUI, YUEHUA - Michigan State University
item JIANG, JIMING - University Of Wisconsin
item BUELL, C - Michigan State University
item JIANG, NING - Michigan State University

Submitted to: Nucleic Acids Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/4/2018
Publication Date: 3/16/2018
Citation: Zhao, D., Hamilton, J.P., Vailancourt, B., Zhang, W., Eizenga, G.C., Cui, Y., Jiang, J., Buell, C., Jiang, N. 2018. Evolutionary trajectory of Pack-MULEs is determined by their epigenetic status. Nucleic Acids Research.

Interpretive Summary: “Jumping genes” or transposable elements are mechanism that increase diversity in plants. Jumping genes were first proposed by maize (corn) geneticist Dr. Barbara McClintock in the 1940s as the reason for the spotted maize kernels but it was not until scientific advances in understanding DNA structure during the 1970s confirmed the prevalence of transposable elements in living organisms, including rice, that the importance of jumping genes was realized. The current study was undertaken to better understand the function of the jumping genes classified as Pack-MULEs (Pack Mutator-like transposable elements) in rice. The DNA sequences in the approximately 3,000 different Pack-MULEs found in rice were examined and it was discovered that about 40% of the Pack-MULEs produced mRNA and proteins. The majority of these mRNAs and proteins were produced during the reproductive stage, when the panicle develops and seeds are produced. This suggests many of these Pack-MULEs, or jumping genes, have an important function in rice reproduction and seed traits. For example, these may have played a role in the evolution of the progenitor species, Oryza rufipogon which usually has an open panicle with smaller and lighter seeds, and can easily cross pollinate with other Oryza species, to the current day cultivated rice, Oryza sativa, that has a more closed panicle shape with larger and heavier seeds, and is self-pollinated. A better understanding of how Pack-MULEs increase diversity ultimately is important in improving rice yield and grain quality.

Technical Abstract: Acquisition and rearrangement of host genes by transposable elements is one mechanism to increase gene diversity. The rice genome is replete in such sequences and while ~3,000 Pack- Mutator-like transposable elements containing gene sequences (Pack-MULEs) have been identified, their function remains enigmatic. To identify signatures of functioning Pack-MULEs and gain insight into Pack-MULE evolution, we generated transcriptome, translatome, and epigenome datasets and compared Pack-MULEs with protein-coding genes, Pack-MULE parental genes, and transposable elements. Expression data from 48 tissues/treatments revealed 40% of Pack-MULEs were transcribed and 9% had translation evidence, clearly distinguishing them from other transposable elements, which have limited transcription and are rarely translated. Pack-MULEs exhibited a unique expression profile associated with specificity in reproductive tissues that may be associated with selection of seed traits. Expressed Pack-MULEs resemble regular protein-coding genes as exhibited by low DNA methylation, the presence of active histone marks and DNase I hypersensitive sites (DHSs), and an absence of repressive histone marks. In contrast, non-expressed Pack-MULEs are highly methylated, bear repressive histone marks and lack both active histone marks and DHSs. The expression potential of Pack- MULEs is not dependent on the local genomic environment as expressed Pack-MULEs are also found within pericentromeric regions suggesting that Pack-MULEs either preferentially insert into open, expression-permissive regions of the genome or alternatively, create expression competence following insertions. This study suggests that a substantial fraction of Pack-MULEs have functional potential in vivo, reinforcing the hypothesis that transposable elements can impact the expansion and diversification of genes within the existing gene pool.