Gender-specific selection on codon usage in plant genomes

Abstract

Background: Currently, there is little data available regarding the role of gender-specific gene expression on synonymous codon usage (translational selection) in most organisms, and particularly plants. Using gender-specific EST libraries (with > 4000 ESTs) from Zea mays and Triticum aestivum, we assessed whether gender-specific gene expression per se and gender-specific gene expression level are associated with selection on codon usage.

Results: We found clear evidence of a greater bias in codon usage for genes expressed in female than in male organs and gametes, based on the variation in GC content at third codon positions and the frequency of species-preferred codons. This finding holds true for both highly and for lowly expressed genes. In addition, we found that highly expressed genes have greater codon bias than lowly expressed genes for both female- and male-specific genes. Moreover, in both species, genes with female-specific expression show a greater usage of species-specific preferred codons for each of the 18 amino acids having synonymous codons. A supplemental analysis of Brassica napus suggests that bias in codon usage could also be higher in genes expressed in male gametophytic tissues than in heterogeneous (flower) tissues.

Conclusion: This study reports gender-specific bias in codon usage in plants. The findings reported here, based on the analysis of 1,497,876 codons, are not caused either by differences in the biological functions of the genes or by differences in protein lengths, nor are they likely attributable to mutational bias. The data are best explained by gender-specific translational selection. Plausible explanations for these findings and the relevance to these and other organisms are discussed.

Figure 1

The GC content at third codon positions and the frequency of preferred codons for genes expressed specifically in male and female gametes or tissues in Zea mays and Triticum aestivum and the GC content of male-specific and flower-specific genes in Brassica napus relative to gene expression level. P-values between male and female (flower for B. napus) expressed genes for GC3 and for Fpr are as follows (respectively, in parenthesis):Z. mays: high (< 1 × 10^-16**, < 1 × 10^-16**), low (< 1 × 10^-16 **, < 1 × 10^-16**), all expression levels (< 1 × 10^-16**, < 1 × 10^-16**); T. aestivum: high (< 1 × 10^-16*, 0.001*), low (< 1 × 10^-16**, < 1 × 10^-16**), all expression levels (< 1 × 10^-16**, < 1 × 10^-16**); B. napus (GC3 only): high (0.141), low (< 1 × 10^-16**) and all expression levels (< 1 × 10^-16**). P-values for high versus low expression level within gender (or flower): Z. mays: Female (< 1 × 10^-16**, < 1 × 10^-16**), Male (0.012*, 0.010*); T. aestivum: Female (< 1 × 10^-16**, < 1 × 10^-16**), Male (0.036*, 0.025*); B. napus: Male (1 × 10^-16**), Flower (0.018*). P-values for lowly expressed female-specific genes versus highly expressed male-specific genes: Z. mays (< 1 × 10^-16**, < 1 × 10^-16**) and T. aestivum (0.867, 0.553). P-values for highly expressed female-specific genes versus lowly expressed male-specific genes: Z. mays (< 1 × 10^-16**, < 1 × 10^-16**) and T. aestivum (< 1 × 10^-16**, < 1 × 10^-16**). P-value for highly expressed male-specific genes versus lowly expressed genes in flower in B. napus (0.760). P-value for highly expressed male-specific genes versus lowly expressed genes in the flower in B. napus (< 1 × 10^-16).* Indicates statistical significance (P < 0.05), **Indicates that P-value remains statistically significant after the Bonferroni correction.

Figure 2

Hierarchical clustering based on Pearson correlation matrixes on relative synonymous codon usage values derived from concatenated EST sequences for each combination of species and gender (Zea mays and Triticum aestivum male-specific and female-specific genes).

Figure 3

Biological functions of genes expressed only in the sperm and eggs in Zea mays, in the anther and ovary in Triticum aestivum and in the microspore and flower in Brassica napus. Sum of percentages may exceed 100 as some genes belong to more than one category.