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RESEARCH ARTICLE 12
Genomic Imprinting was Evolutionarily Conserved during Wheat 3Polyploidization 4
81 State Key Laboratory for Agrobiotechnology, Key Laboratory of Crop Heterosis Utilization 9(MOE), Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, 10Beijing, 100193, China. 112 College of Agronomy, Northwest A&F University, Yangling 712100, Shaanxi, China. 123 These authors contributed equally to this work 13*Corresponding author: Mingming Xin, [email protected], Tel: 010-6273145214
15Short title: Genomic imprinting in wheat 16
17One-sentence summary: Genes controlled by imprinting were evolutionarily conserved during 18wheat polyploidization. 19
20The author responsible for distribution of materials integral to the findings presented in this 21article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) 22is: Mingming Xin ([email protected]) 23
24ABSTRACT 25
Genomic imprinting is an epigenetic phenomenon that causes genes to be differentially expressed 26depending on their parent-of-origin. To evaluate the evolutionary conservation of genomic 27imprinting and the effects of ploidy on this process, we investigated parent-of-origin-specific gene 28expression patterns in the endosperm of diploid (Aegilops spp.), tetraploid, and hexaploid wheat 29(Triticum spp.) at various stages of development via high-throughput transcriptome sequencing. 30We identified 91, 135, and 146 maternally or paternally expressed genes (MEGs or PEGs, 31respectively) in diploid, tetraploid, and hexaploid wheat, respectively, 52.7% of which exhibited 32dynamic expression patterns at different developmental stages. Gene ontology enrichment 33analysis suggested that MEGs and PEGs were involved in metabolic processes and 34DNA-dependent transcription, respectively. Nearly half of the imprinted genes exhibited 35conserved expression patterns during wheat hexaploidization. In addition, forty percent of the 36homeolog pairs originating from whole genome duplication were consistently maternally or 37paternally biased in the different subgenomes of hexaploid wheat. Furthermore, imprinted 38expression was found for 41.2% and 50.0% of homolog pairs that evolved by tandem duplication 39after genome duplication in tetraploid and hexaploid wheat, respectively. These results suggest 40that genomic imprinting was evolutionarily conserved between closely related Triticum and 41Aegilops species, and in the face of polyploid hybridization between species in these genera. 42
Plant Cell Advance Publication. Published on January 3, 2018, doi:10.1105/tpc.17.00837
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Diploid Wheat Mapped to CS_D
Tetraploid Wheat Mapped to CS_A&B
Hexaploid Wheat Mapped to CS_A&B&D
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No. of genes with SNP: 3,485No. of genes: 434 (p < 0.05)
No. of genes with SNP: 4,612No. of genes: 1,307 (p < 0.05)
No. of genes with SNP: 5,063No. of genes: 1,630 (p < 0.05)
Figure 1. Most Genes Exhibited the Expected Expression Ratios in Developing Wheat Endosperm. Parental expression ratios plot for each reciprocal cross in diploid, tetraploid, and hexaploid wheat species. The expression levels of paternal (y-axis) and maternal (x-axis) alleles are represented by the log -transformed read counts of the paternally- and maternally-derived reads in the reciprocal crosses, respectively. The expression patterns of 3,485, 4,612, and 5,063 genes with SNPs were analyzed in reciprocally crossed endosperm for diploid, tetraploid, and hexaploid wheat, respectively. Of these, 434, 1,307, and 1,630 genes were identified as parental biased expressed genes in diploid, tetraploid, and hexaploid wheat endosperm, respectively, according to a Chi-Square Goodness-of-Fit Test (FDR-adjusted < 0.05). The dashed diagonal line represents the expected 2m:1p ratio. DAP: days after pollination, CS: Chinese Spring.
Figure 2. Computational Identification of Imprinted Genes in Wheat Endosperm.(A) Ratio-based cutoff to identify MEGs and PEGs. Spots clustered in the upper-right corners have more than 90% maternal reads (red, MEGs), whereas spots clustered in the lower-left corners have more than 70% paternal reads (green, PEGs). Black dots represent non-imprinted genes. The intersection of the dashed lines indicates a 2m:1p ratio. Dots representing MEGs and PEGs are semitransparent. Y: Y177, R: RM220, J: Jinying 8, S: SCAUP, D: Doumai, K: Keyi5214.(B) Venn diagram analysis of imprinted genes. The number of imprinted genes identified at 15, 20, and 25 DAP are shown in the red, green, and blue circles, respectively. DAP: days after pollination, MEG: maternally expressed gene, PEG: paternally expressed gene.
6.06.57.07.58.08.59.09.5 Average expression level
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Figure 3. Expression of Imprinted Genes in Different Wheat Tissues.(A) The expression levels of MEGs and PEGs were examined in 13 wheat tissues. The average expression level is higher in endosperm than in other tissues. MEGs appeared to be more endosperm-specific than PEGs. Dashedline indicates the average expression level of imprinted genes in different tissues. The color scale from blue (low) to red (high) indicates relative gene expression level. (B) The expression levels of MEGs and PEGs are higher than those of non-imprinted genes in diploid, tetraploid, and hexaploid wheat species at all stages examined. The number indicates the average expression level (log -transformed FPKM).
Figure 4. Imprinted Genes that were Evolutionarily Conserved during Hexaploidization. (A) Parent-of-origin expression patterns of imprinted genes are highly conserved among wheat species. The white barindicates the number of imprinted genes in different subgenomes of diploid, tetraploid, and hexaploid wheat; light gray barindicates the number of imprinted genes with SNPs in other wheat species; dark gray bar indicates the number of conservedimprinted genes in different wheat species; black bar indicates the number of conserved candidate imprinted genes withbiased expression patterns in different wheat species only considering the criterion of FDR-adjusted value.(B–D) Thirteen pairs of homeologs show similar imprinted expression patterns in tetraploid and hexaploid wheat. Verticallines indicate the 13 groups of homeologous wheat genes. Blue (low), white (medium), and red (high) represent the relativeexpression levels of maternal or paternal alleles. DAP: days after pollination, S: SCAUP, J: Jinying 8, D: Doumai, K: Keyi5214,MEG: maternally expressed gene, PEG: paternally expressed gene.