Gene family expansions underpin context-dependency of the oldest mycorrhizal symbiosis.

As environments worldwide change at unprecedented rates during the Anthropocene, understanding context-dependency – how species regulate interactions to match changing environments – is crucial. However, generalizable molecular mechanisms underpinning context-dependency remain elusive. Combining comparative genomics across 42 angiosperms with transcriptomics, genome-wide association mapping, and gene duplication origin analyses, we show for the first time that gene family expansions undergird context-dependent regulation of species interactions. Gene families expanded in mycorrhizal fungi-associating plants display up to 200% more context-dependent gene expression and double the genetic variation associated with mycorrhizal benefits to plant fitness. Moreover, we discover these gene family expansions arise primarily from tandem duplications with >2-times more tandem duplications genome-wide, indicating gene family expansions continuously supply genetic variation allowing fine-tuning of context-dependency in species interactions throughout plant evolution. One-Sentence Summary Gene family expansions arising from tandem duplications underpin genetic regulation and fitness effects of context-dependency