Pollen performance traits reveal prezygotic nonrandom mating and interference competition in Arabidopsis thaliana

The lack of ability to measure pollen performance traits in mixed pollinations has been a major hurdle in understanding the mechanisms of differential success of compatible pollen donors. In previous work, we demonstrated that nonrandom mating between two accessions of Arabidopsis thaliana, Columbia (Col) and Landsberg (Ler), is mediated by the male genotype. Despite these genetic insights, it was unclear at what stage of reproduction these genes were acting. Here, we used an experimental strategy that allowed us to differentiate different pollen populations in mixed pollinations to ask: (1) What pollen performance traits differed between Col and Ler accessions that direct nonrandom mating? (2) Is there evidence of interference competition?

We used genetically marked pollen that can be visualized colorimetrically to quantify pollen performance of single populations of pollen in mixed pollinations. We used this and other assays to measure pollen viability, germination, tube growth, patterns of fertilization, and seed abortion. Finally, we assessed interference competition.

In mixed pollinations on Col pistils, Col pollen sired significantly more seeds than Ler pollen. Col pollen displayed higher pollen viability, faster and greater pollen germination, and faster pollen tube growth. We saw no evidence of nonrandom seed abortion. Finally, we found interference competition occurs in mixed pollinations.

The lack of differences in postzygotic processes coupled with direct observation of pollen performance traits indicates that nonrandom mating in Arabidopsis thaliana is prezygotic, due mostly to differential pollen germination and pollen tube growth rates. Finally, this study unambiguously demonstrates the existence of interference competition.