Targeted plant hologenome editing for plant trait enhancement

Breeding better crops is a cornerstone of global food security. While efforts in plant genetic improvement show promise, it is increasingly becoming apparent that the plant phenotype should be treated as a function of the holobiont, in which plant and microbial traits are deeply intertwined. Using a minimal holobiont model, we track ethylene production and plant nutritional value in response to alterations in plant ethylene synthesis (KO mutation in ETO1), which induces 1-aminocyclopropane-1-carboxylic acid (ACC) synthase 5 (ACS5), or microbial degradation of ACC (KO mutation in microbial acdS), preventing the breakdown of the plant ACC pool, the product of ACS5. We demonstrate that similar plant phenotypes can be generated by either specific mutations of plant-associated microbes or alterations in the plant genome. Specifically, we could equally increase plant nutritional value by either altering the plant ethylene synthesis gene ETO1, or the microbial gene acdS. Both mutations yielded a similar plant phenotype with increased ethylene production and higher shoot micronutrient concentrations. Restoring bacterial AcdS enzyme activity also rescued the plant wild-t8yp phenotype in an eto1 background. Plant and bacterial genes build an integrated plant-microbe regulatory network amenable to genetic improvement from both the plant and microbial sides.