COS 88-6 - Evolution of large gene families allows context-dependency in microbial symbiosis

Background/Question/Methods

Microbial symbioses underpin many essential plant functions from nutrient acquisition to stress tolerance. However, the relationships between plants and their microbes are very variable with plant-microbial symbioses able to shift between mutualistic and parasitic relationships depending on environmental context. While context-dependency in plant-microbe interactions is well-documented, we have few generalizable, mechanistic frameworks to understand why and how the costs/benefits of microbial symbioses change. Here, I propose that gene family size is a generalizable, evolutionary mechanism for mediating context-dependency in microbial symbioses. Large gene families could allow more control than a binary “off/on” switch of gene expression by allowing for more nuanced control of where, when, and how much of a gene is expressed as well as expression of genes with different efficiencies for establishing, maintaining, and/or terminating microbial symbiosis. By combining evolutionary, transcriptomic, and loss-of-function analyses, I 1) determine how gene family size has evolved in 42 plant species in relationship to whether they can symbiose with the common mutualist arbuscular mycorrhizal fungi and 2) assess how gene family size shapes context-dependency in microbial symbiosis using the ancient symbiosis between plants and arbuscular mycorrhizal fungi as a model.

Results/Conclusions

Larger gene families have more context-dependent expression which implicates gene family size as an important genomic feature of molecular mechanisms underlying microbial symbioses. I first identified gene families conserved in arbuscular mycorrhizal plants and then compared gene expression of plants grown with/without mycorrhizal fungi and with/without high salinity, low potassium, and low phosphorus stressors. Large gene families conserved in arbuscular mycorrhizal plants have 25-65% higher proportions of context-dependent expression than randomized permutations for all three stressors (p=0.0412, p=0.0033, p=0.0012 for salinity, potassium, and phosphorus, respectively). I then analyzed the kinds of gene families expanded/retained in mycorrhizal plants. Membrane-associated proteins are the most common mycorrhizal-specific gene family (~20% of all families) and are ~45% larger than the next most common type. These data are indicative of 1) membrane-associated proteins as outsized regulators of mycorrhizal symbiosis and 2) the symbiotic membrane is where much of the fine-tuning of symbiosis occurs. I am now testing if deleting genes in select families (e.g., membrane-lipid modifying enzymes) disrupts context-dependency of mycorrhizal symbiosis.

This work builds a generalizable molecular framework for understanding how plants and microbes coordinate their relationship in different environment contexts.