Gender-specific selection on codon usage in plant genomes.

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.

Male-biased transmission of deleterious mutations to the progeny in Arabidopsis thaliana.

The extent and cause of male-biased mutation rates, the higher number of mutations in sperm than in eggs, is currently an active and controversial subject. Recent evidence indicates that this male (sperm) bias not only occurs in animals but also in plants. The higher mutation rate in plant sperm was inferred from rates of evolution of neutral DNA regions, and the results were confined to the mitochondria and chloroplasts of gymnosperms. However, the relative transmission rates of deleterious mutations, which have substantial evolutionary consequences, have rarely been studied. Here, an investigation is described by using the hermaphroditic self-compatible flowering plant Arabidopsis thaliana, in which we artificially increased the rate of mutation in pollen (i.e., sperm donor) and maternal (i.e., egg donor) parents, by using two kinds of UV irradiation in parallel and separate experiments, and assessed the deleterious effects on fitness of the F(2) generation. The results show that more deleterious induced mutations are transmitted to the progeny by a sperm than by an egg. These findings provide the first experimental evidence that more deleterious mutations are inherited from sperm than from an egg in any organism. Possible causes underlying this male bias are discussed.

Broad-scale analysis contradicts the theory that generation time affects molecular evolutionary rates in plants.

Several studies of plant taxa have concluded that generation time, including annual/perennial life history, may explain molecular evolutionary rate variation in selectively neutral DNA. Unlike in animals, there is little theoretical basis for why generation-time effects would exist in plants. Furthermore, previous reports fail to establish the generality of a generation-time effect in plants because of the small size of the datasets, a large proportion of which compared very widely divergent taxa differing in many characteristics other than generation time. Using 24 phylogenetically independent species pairs, each containing a species with an annual and a species with a perennial life history, and nine species pairs, each containing a tree species with a short and a long minimum generation time, we found no evidence that generation time is related to molecular evolutionary rate variation of the nuclear 18S ITS1 and ITS2 regions. This analysis strongly contradicts the growing belief that evolutionary rates are affected by generation time in plants. Possible reasons for the absence of generation-time effects are discussed, including an evaluation of the cell-division theory.

Male-driven evolution of mitochondrial and chloroplastidial DNA sequences in plants.

Although there is substantial evidence that, in animals, male-inherited neutral DNA evolves at a higher rate than female-inherited DNA, the relative evolutionary rate of male- versus female-inherited DNA has not been investigated in plants. We compared the substitution rates at neutral sites of maternally and paternally inherited organellar DNA in gymnosperms. The analysis provided substantial support for the presence of a higher evolutionary rate in both the mitochondrial and chloroplastidial DNA when the organelle was inherited paternally than when inherited maternally. These results suggest that, compared with eggs, sperm tend to carry a greater number of mutations in mitochondrial and chloroplastidial DNA. The existence of a male mutation bias in plants is remarkable because, unlike animals, the germ-lines are not separated from the somatic cells throughout an individual's lifetime. The data therefore suggest that even a brief period of male and female germ-line separation can cause gender-specific mutation rates. These results are the first to show that, at least in some species, germ-lines influence the number of mutations carried in the gametes. Possible causes of male mutation bias in plants are discussed.