Deleterious Mutation Accumulation in Arabidopsis thaliana Pollen Genes: A Role for a Recent Relaxation of Selection.

In many studies, sex-related genes have been found to evolve rapidly. We therefore expect plant pollen genes to evolve faster than sporophytic genes. In addition, pollen genes are expressed as haploids which can itself facilitate rapid evolution because recessive advantageous and deleterious alleles are not masked by dominant alleles. However, this mechanism is less straightforward to apply in the model plant species Arabidopsis thaliana. For 1 Myr, A. thaliana has been self-compatible, a life history switch that has caused: a reduction in pollen competition, increased homozygosity, and a dilution of masking in diploid expressed, sporophytic genes. In this study, we have investigated the relative strength of selection on pollen genes compared with sporophytic genes in A. thaliana. We present two major findings: 1) before becoming self-compatible, positive selection was stronger on pollen genes than sporophytic genes for A. thaliana and 2) current polymorphism data indicate that selection is weaker on pollen genes compared with sporophytic genes. This weaker selection on pollen genes can in part be explained by their higher tissue specificity, which in outbreeding plants can be outweighed by the effects of haploid expression and pollen competition. These results indicate that since A. thaliana has become self-compatible, selection on pollen genes has become more relaxed. This has led to higher polymorphism levels and a higher build-up of deleterious mutations in pollen genes compared with sporophytic genes.

The 5'-untranslated region of the ntp303 gene strongly enhances translation during pollen tube growth, but not during pollen maturation.

Transcripts of the ntp303 gene accumulate abundantly throughout pollen development, whereas the protein only accumulates to detectable levels after pollen germination. In an attempt to explain the divergence in the accumulation profiles of the mRNA and the protein, we investigated the role of the untranslated regions (UTRs) in enhancing ntp303 translation during the transition from developing to germinating pollen. Luciferase reporter gene fusion constructs containing the ntp303 5'-UTR gave rise to luciferase activity that was up to 60-fold higher during pollen tube growth than that of constructs containing different 5'-UTRs. No apparent differences in the luciferase activity of these constructs were observed during pollen development. The ntp303 5'-UTR-mediated increase in luciferase activity was not significantly influenced by coding region or 3'-UTR sequences. Furthermore, enhanced luciferase activity directed by the ntp303 5'-UTR occurred predominantly at the post-transcriptional level. A series of 5'-UTR deletion constructs was created to identify putative regulatory sequences required for the high level of translation during pollen tube growth. Two predicted stem loop structures (H-I and H-II) caused a complete inhibition of the enhanced translation after their total or partial deletion. A (GAA)(8) repeat within the H-I stem loop structure was demonstrated to be important for the modulation of translation efficiency. The H-II stem loop structure was found to be essential for the determination of mRNA stability.