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. 2012 Jul;7(7):864-73.
doi: 10.4161/psb.20486. Epub 2012 Jul 1.

Bimodal Expression Level Polymorphisms in Arabidopsis Thaliana

Free PMC article

Bimodal Expression Level Polymorphisms in Arabidopsis Thaliana

Atsushi J Nagano et al. Plant Signal Behav. .
Free PMC article


Differences in gene expression are termed expression level polymorphisms (ELPs). Here, we propose a new ELP class, bimodal ELPs (bELPs), as a criterion to screen for genes that are responsible for natural phenotypic variation and/or that are targeted by balancing selection. bELP genes are characterized by two expression level modes. Genomic scans based on nucleotide sequences are not ideal for identifying genes targeted for selection. A critical concern is that several genes can be present in the selection-targeted regions identified by such scans. This situation indicates the importance of integrating genomic sequence data and other information, such as gene expression data. Comparative transcriptomics is useful for determining evolutionarily and ecologically important polymorphisms. In a genome-wide expression screen of 34 accessions, we identified 344 Arabidopsis thaliana genes exhibiting bELPs. Population genetic analysis revealed that bELP genes had high nucleotide diversities and long linkage disequilibriums. The highest nucleotide diversity (11-fold greater than the genomic mean) was found in the At1g23780 gene, which encodes a putative F-box protein. We observed a clear association between the expression mode and sequence type of the At1g23780 gene. Our results suggest that bELPs will be useful for the screening and functional analysis of genes responsible for phenotypic polymorphisms. Such a "multi-omics" approach has the potential to facilitate the scanning of genes relevant to balanced polymorphisms not only in A. thaliana, but also in other model and non-model organisms.


Figure 1. Schematic representation of bELPs. (A) Histograms depicting typical ELPs (left) and bELPs (right). In the bELP histogram, two expression modes are clearly distinguishable. The ELP gene superclass includes the class of bELP genes. (B) Screening criterion for identifying bELP genes. Expression levels of a specific gene in each accession are plotted (circles) on an axis. dmax is the greatest difference observed between the expression levels of two neighboring accessions.
Figure 2. bELPs in A. thaliana and analyses of the selected sequences. (A) Heat map of bELP gene expression (dmax = 1). Low and high levels of expression are shown by blue and yellow colors, respectively. Thirty-four accessions are aligned horizontally and 356 genes are aligned vertically. Red arrowheads indicate the 20 sequenced genes. A full resolution image with AGI codes and annotations of bELP genes is available as Figure S2. (B) Frequency distribution of the ratio of two expression types. Inset, enlarged view. (C) Examples of bELP genes. Each histogram shows two expression modes. (D) Histogram of silent-site nucleotide diversity (π) of the 20 sequenced bELP genes (red, upper) compared with the genomic distribution (gray, two lower histograms). Data for the genomic distribution are from Schmid et al. and Nordborg et al. (E) Histogram of Tajima’s D of the 20 sequenced bELP genes (red, upper) compared with the genomic distribution (gray, lower). Data for the genomic distribution are from Nordborg et al. (F) Histograms of the lengths of LD blocks. Upper: LD blocks including bELP genes. Lower: genome-wide distribution estimated from Clark et al. LD blocks over 250 kb (0.002%) are not shown in the lower histogram.
Figure 3. Nucleotide diversity, neighbor-joining trees and expression levels of At1g23780 and flanking genes. (A) Nucleotide diversity was calculated with a sliding window (100 bp). Gray arrows indicate genes. The dashed line indicates the average level of silent-site π for A. thaliana. (B) Neighbor-joining trees of At1g23780 and flanking genes (from At1g23760 to At1g23800). Open circles and closed triangles indicate low and high expression accessions of the At1g23780 gene, respectively. Closed boxes represent A. lyrata as an outgroup. (C) Gene expression levels of At1g23780 and flanking genes. Data for At1g23770 are not available, because there was no corresponding probe-set on the ATH1 gene chip. (D) The r2 plot of At1g23780 and its flanking region (~35 kb). Black indicates strong LD (r2 = 1) and white indicates weak LD (r2 = 0).
Figure 4. Relationship between haplotypes of the At1g23780 gene. (A) The haplotype network for At1g23780. Names of accessions with low expression levels are shaded. Minimum steps are indicated for each node. (B) Col-0 and Cvi polymorphic nucleotides. Nucleotides also shared by Col-0 are depicted by dots. Nucleotides also shared by Cvi are shaded. (C) Schematic of the At1g23780 gene. The upper line indicates the putative recombined region in the Van-0 accession. Triangles indicate amino acid substitutions. (Closed triangles represent amino acid differences between the Col-0 and Cvi alleles; gray triangles indicate minor variations). The closed box indicates the F-box domain.

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