Microbial Mediation of Pollen Germination: A Hidden Driver of Plant Reproduction and Hybridization in Asclepias

Sexual reproduction in plants is essential for species survival. It is a complex process that extends beyond pollen transfer by pollinators. This study focuses on post-pollination events, examining how stigmatic secretions, and the potential microbes within them, affect pollen viability and germination. To do this we utilized Asclepias as a model system, its pollen is packaged into pollinia which are visible to the naked eye, and its stigmatic secretion is accessible and readily produced. Experimentally, pollinia from Asclepias syriaca, Asclepias exaltata and naturally occurring hybrid individuals were germinated in artificial and field collected nectar. DNA was extracted and sequenced from nectar samples to identify microbial communities, while whole nectar was plated to quantify microbial abundance. We found that both sugar concentration and nectar species significantly influence the ability of pollinia to grow pollen tubes. A. exaltata serves as an effective pollinia receptor, while A. syriaca appears to be a strong pollinia donor. This asymmetric pollinia germination potentially contributes to previously observed patterns of biased introgression between these species. The microbial communities associated with A. syriaca and A. exaltata differ significantly in both composition and abundance. A. syriaca nectar contains a high concentration of bacteria and fungi, whereas A. exaltata contains minimal levels of fungal microbes. These results indicate that microbes may be playing a previously unidentified role in sexual reproduction in plants, specifically, through impacting pollen germination. Microbial communities may be functioning as a prezygotic barrier, potentially acting asymmetrically and impacting the direction of gene flow and evolution. Beyond ecological implications, this study highlights an underappreciated role of stigmatic secretions and their associated microbes in agricultural systems. Given that successful sexual reproduction is essential for crop productivity and global food security, further investigation into these microbial influences is necessary.