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. 2016 Sep 22;7:1433.
doi: 10.3389/fpls.2016.01433. eCollection 2016.

Gene Evolutionary Trajectories and GC Patterns Driven by Recombination in Zea mays

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Free PMC article

Gene Evolutionary Trajectories and GC Patterns Driven by Recombination in Zea mays

Anitha Sundararajan et al. Front Plant Sci. .
Free PMC article

Abstract

Recombination occurring during meiosis is critical for creating genetic variation and plays an essential role in plant evolution. In addition to creating novel gene combinations, recombination can affect genome structure through altering GC patterns. In maize (Zea mays) and other grasses, another intriguing GC pattern exists. Maize genes show a bimodal GC content distribution that has been attributed to nucleotide bias in the third, or wobble, position of the codon. Recombination may be an underlying driving force given that recombination sites are often associated with high GC content. Here we explore the relationship between recombination and genomic GC patterns by comparing GC gene content at each of the three codon positions (GC1, GC2, and GC3, collectively termed GCx) to instances of a variable GC-rich motif that underlies double strand break (DSB) hotspots and to meiocyte-specific gene expression. Surprisingly, GCx bimodality in maize cannot be fully explained by the codon wobble hypothesis. High GCx genes show a strong overlap with the DSB hotspot motif, possibly providing a mechanism for the high evolutionary rates seen in these genes. On the other hand, genes that are turned on in meiosis (early prophase I) are biased against both high GCx genes and genes with the DSB hotspot motif, possibly allowing important meiotic genes to avoid DSBs. Our data suggests a strong link between the GC-rich motif underlying DSB hotspots and high GCx genes.

Keywords: GC; codon usage; gene expression; maize; meiocytes; meiosis; recombination; wobble.

Figures

FIGURE 1
FIGURE 1
Outcomes of meiotic recombination. A double strand break is processed via different pathways, with very few DSBs resulting in actual crossovers while a majority are resolved via gene conversion, frequently inserting a GC bias due to mismatch repair. Thick arrows represent the major routes.
FIGURE 2
FIGURE 2
GC patterns within maize coding regions shown in kernel density plots. (A) Histogram of GC content of genes (including exons and introns). (B) Histogram of GC content of genes (just CDS sequence). The area under the curve represents the probability of getting a value in a given range of GC content, with the area under the entire curve equal to 1.
FIGURE 3
FIGURE 3
Kernel density plots of GCx distribution patterns of gene CDSs. (A) GC1. (B) GC2. (C) GC3.
FIGURE 4
FIGURE 4
Comparison of GCx distributions. (A) GC1 vs. GC2. (B) GC1 vs. GC3. (C) GC2 vs. GC3. Blue lines show the 80% cutoff separating the high and low GCx classes.
FIGURE 5
FIGURE 5
GC content within hotspot motifs was compared between 3 nt-based periodicity groups across all motif instances. (A) All hotspot motifs are plotted in groups of every third nucleotide starting with nt1, nt2, or nt3. The nt1 group includes GC content calculated across all motifs for nucleotide positions 1, 4, 7, etc. Each position was analyzed separately. Likewise, the nt2 and nt3 groups have GC content calculated for every third nucleotide position starting with nt2 and nt3, respectively. (B) All genic hotspot motifs are plotted in groups of every third nucleotide as in (A); (C) The reading frame of the motif was determined in order to place nucleotides into the GC1, GC2, and GC3 categories. Then, GC content was calculated for the GC1, GC2, and GC3 position within the motif, trimming the end nucleotide overhangs that resulted when shifting motifs to line up GC1, GC2, and GC3 positions.
FIGURE 6
FIGURE 6
Density plot of GCx content of individual motifs. (A) GC1, (B) GC2, (C) GC3.
FIGURE 7
FIGURE 7
Overview of findings. High GCx genes are overrepresented for DSB hotspots and genes down-regulated in meiocytes but underrepresented for genes up-regulated in meiocytes. Individual high GCx classes (GC1, GC2, and GC3) show less overlap than expected given the number of genes in each class. Genes up-regulated in meiocytes are underrepresented for DSB hotspots.

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