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

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Abstract

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

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  1. This dichotomy between soil chemical stressors and drought potentially points to two distinct molecular syndromes driving the ecological strategies plants use to regulate AM symbiosis during persistent stress lasting years/decades versus seasonal/episodic stress (see Supplementary Text).

    This is a really interesting finding; isn’t drought also often seasonal/episodic?

  2. We found plants disproportionately target larger AM-expanded gene families for context-dependent regulation under soil chemical stress, with 200%, 86%, and 41% greater context-dependent expression of these gene families than expected by chance in response to low phosphorus, low potassium, and high salinity stress, respectively (p = 0.0006, p = 0.0054, and p = 0.0297; Fig. 3a), indicating the gene expression plasticity facilitated by gene family expansions is important for context-dependent regulation under soil chemical stress.

    Supporting this with some transcription factor analysis might be useful to assess if there are commonalities in who the molecular regulators are for these AM-expanded gene families.

  3. 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.

    Great paper with lots of food for thought regarding genomic trends associated with symbioses.