Modelling pollen competition

Often, more pollen grains arrive on stigmas than there are ovules to fertilize, resulting in pollen competition. Pollen competition has been linked with inbreeding avoidance, sexual selection, reproductive barrier reinforcement, and speciation. Mathematical modeling of pollen competition allows researchers to simulate laboratory fertilization experiments on a significantly larger scale. A new paper is the first to simulate pollen competition and have pollen interference emerge as a property of the fertilization process.

Alex Capaldi, Associate Professor of Mathematics and Statistics at Valparaiso University, and coauthors created a mechanistic agent-based model (ABM) to identify and quantify which pollen performance traits cause different competitive outcomes (e.g., seed siring proportion) and to what extent each one contributes. ABMs are a type of mathematical model that show how individuals (i.e., pollen grains) interact with other individuals and with their local environment.

“Understanding which traits matter the most in pollen competition can focus genetic studies on identifying genes that lead to the most success in pollination” explains Capaldi.

The model was constructed to represent a pistil, with different components representing the stigma, style, transmitting tract, septum, ovary, and ovules. These components were broken down into patches with each having an amount of energy associated with them and an attractant/repellent index, which changed over time.

Each pollen grain had an indicator if the pollen tube has germinated, an energy value, a pollen tube length, and an indicator if it has fertilized an ovule. These properties also changed over time.

The authors modeled two accessions of Arabidopsis thaliana, Columbia (Col) and Landsberg erecta (Ler), that previously demonstrated nonrandom mating in pollen competitions. Each accession was given different pollen performance traits derived from the literature. These included:

• Amount of energy in each pollen grain
• Rate of pollen tube growth
• Energy requirement for pollen tube growth
• Energy required to fertilize an ovule

The authors calibrated the model to two quantities: the mean pollen tube lengths and distribution of pollen tube lengths during single accession experiments. The model was able to predict, on average, values similar to those found in empirical studies.

The model was then run with an equal number of pollen grains from the two accessions to determine which traits were beneficial in the ability to sire more seeds than the competing accession. Pollen performance traits that influenced pollen tube movement and direction, such as chemoattractant sensing of ovules radius, pollen grain energy harvesting limits, and pollen grain movement costs, were found to be primary factors in competition.

To test whether pollen tube interference emerged as an important competitive property, the authors compared Ler pollen tube lengths in single accession experiments versus Ler pollen tube lengths in experiments where it was in competition with Col. They found that Ler pollen tubes were shorter during competition with Col, indicating that pollen interference is a property of pollen competition. This was backed by a previous study showing that the presence of Col pollen retards the growth of Ler pollen tubes.

Capaldi concludes, “This provides us with a useful model to begin dissecting the mechanistic aspects of pollen interference. The ability to look at pollen as a population during fertilization changes what we can do genetically and can provide tools that work in large scale fertilization in the future. For example, this process may lead to technologies that allow the building of artificial species barriers.”

READ THE ARTICLE:

Charlotte Beckford, Montana Ferita, Julie Fucarino, David C Elzinga, Katherine Bassett, Ann L Carlson, Robert Swanson, Alex Capaldi, Pollen interference emerges as a property from agent-based modeling of pollen competition in Arabidopsis thaliana, in silico Plants, 2022, diac016, https://doi.org/10.1093/insilicoplants/diac016