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. 2013 Nov 26;110(48):19639-44.
doi: 10.1073/pnas.1309182110. Epub 2013 Nov 11.

Comprehensive Analysis of Imprinted Genes in Maize Reveals Allelic Variation for Imprinting and Limited Conservation With Other Species

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Comprehensive Analysis of Imprinted Genes in Maize Reveals Allelic Variation for Imprinting and Limited Conservation With Other Species

Amanda J Waters et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

In plants, a subset of genes exhibit imprinting in endosperm tissue such that expression is primarily from the maternal or paternal allele. Imprinting may arise as a consequence of mechanisms for silencing of transposons during reproduction, and in some cases imprinted expression of particular genes may provide a selective advantage such that it is conserved across species. Separate mechanisms for the origin of imprinted expression patterns and maintenance of these patterns may result in substantial variation in the targets of imprinting in different species. Here we present deep sequencing of RNAs isolated from reciprocal crosses of four diverse maize genotypes, providing a comprehensive analysis that allows evaluation of imprinting at more than 95% of endosperm-expressed genes. We find that over 500 genes exhibit statistically significant parent-of-origin effects in maize endosperm tissue, but focused our analyses on a subset of these genes that had >90% expression from the maternal allele (69 genes) or from the paternal allele (108 genes) in at least one reciprocal cross. Over 10% of imprinted genes show evidence of allelic variation for imprinting. A comparison of imprinting in maize and rice reveals that 13% of genes with syntenic orthologs in both species exhibit conserved imprinting. Genes that exhibit conserved imprinting between maize and rice have elevated nonsynonymous to synonymous substitution ratios compared with other imprinted genes, suggesting a history of more rapid evolution. Together, these data suggest that imprinting only has functional relevance at a subset of loci that currently exhibit imprinting in maize.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Discovery of imprinted genes in maize. (A) Allele-specific expression analysis for the reciprocal F1 genotypes generated by crossing B73 and Oh43. The proportion of maternal transcripts in both reciprocal hybrids is plotted for the 13,478 genes that had at least 10 allelic reads in both directions of the cross of B73 and Oh43 (plots for other genotypes are in Fig. S2). The shaded areas indicate moderate (pink), strong (blue), or complete (arrows) MEGs (upper right) or PEGs (lower left). The green shaded areas indicate genes with potential allelic variation for imprinting. (B) The number of nonredundant moderate (pink), strong (blue), and complete (gray) MEGs and PEGs that were detected in at least one of the five reciprocal crosses are shown.
Fig. 2.
Fig. 2.
Conservation of imprinting among maize haplotypes. (A) The proportion of expression from the maternal allele using a heat map (blue = 0; red = 1; yellow = 0.66; gray = missing data) is shown for all 10 genotypes for each of the nonredundant imprinted genes. The genotypes are abbreviated using the first letter of each parent, and the maternal parent is listed first. (B) A similar heat map is shown for the 17 genes with allelic variation for imprinting. (C) The expression patterns for one of the allele-specific imprinted MEGs (GRMZM2G384780) is shown. For this gene, the B73 allele is not silenced when paternally inherited, but alleles from the other haplotypes are silenced when inherited from the paternal parent. For each bar, the upper portion represents the proportion of paternal expression and the lower portion represents the proportion of maternal expression (see gray bars in key for expectations for MEGs, biallelic expression, and PEGs). The colors represent the four alleles assessed (see key for descriptions), and the values listed inside the bars are the number of maternal (M, upper portion of each bar) or paternal (P, lower portion of each bar) reads. The orange dashed line across the plot represents the expected biallelic ratio of 66% maternal reads. Black boxes highlight the nonimprinted allele. (D) Allele-specific imprinting pattern for the PEG GRMZM2G106222, which exhibits a failure to silence the Oh43 when it is maternally inherited. This gene was also validated by a quantitative SNP assay. SNPs were available to distinguish B73-Mo17 and B73-Oh43 alleles. The values listed above the bars are the proportion of the maternal allele determined from the quantitative SNP assay.
Fig. 3.
Fig. 3.
Genes with conserved imprinting exhibit evidence for positive selection. Genes with conserved imprinting exhibit differential evidence of selection. dN/dS values for genome-wide comparisons of maize (M), rice (R), and sorghum (S). In each comparison, the width of the violin plot (white) represents the genome-wide distributions of dN/dS, red dots represent values for nonconserved imprinted genes in maize, and blue dots represent values for genes with conserved imprinting. Because imprinting data are not available in sorghum, the sorghum ortholog of maize-imprinted genes was used in the RS comparison.

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