Identification of novel genes involved in phosphate accumulation in Lotus japonicus through Genome Wide Association mapping of root system architecture and anion content

Abstract

Phosphate is a key nutrient for plants and as it is needed in high quantities. It is highly immobile in the soil and represents a major limiting factor for plant productivity. Plants have evolved different solutions to forage the soil for phosphate and to adapt to phosphate limitation ranging from a profound tuning of their root system architecture and metabolic profile to the evolution of widespread mutualistic interactions, such as those with arbuscular mycorrhizal fungi (AM symbiosis). Despite the prevalence of AM symbiosis throughout land plants, most studies aimed at identifying genes that regulate plant responses to phosphate have been conducted in species incapable of AM symbiosis, such as Arabidopsis. Here we elucidated plant responses and their genetic basis to different phosphate levels in a plant species that is widely used as a model for AM symbiosis: Lotus japonicus. Rather than focusing on a single model strain, we measured root growth and anion content in response to different levels of phosphate in a large panel of Lotus japonicus natural accessions. This allowed us not only to uncover common as well as divergent responses within this species, but also enabled Genome Wide Association Studies by which we identified new genes regulating phosphate homeostasis in Lotus. Under low phosphate conditions, we uncovered a correlation between plant biomass and the decrease of plant phosphate concentration in plant tissues, suggesting a dilution effect. Altogether our data of the genetic and phenotypic variation within a species capable of AM complements studies that have been conducted in Arabidopsis, and advances our understanding of the continuum of genotype by phosphate level interaction that exists throughout dicot plants. Author SummaryPhosphate represents a major limiting factor for plant productivity. Plants have evolved different solutions to adapt to phosphate limitation ranging from a profound tuning of their root system architecture and metabolic profile to the evolution of widespread mutualistic interactions, such as arbuscular mycorrhizal symbiosis. Here we elucidated plant responses and their genetic basis to different phosphate levels in model legume plant species, Lotus japonicus, a plant commonly used for studying arbuscular mycorhizal symbiosis. We investigated Lotus responses to phosphate levels by combining high throughput root system architecture phenotyping and nutrient measurements with a natural variation approach. We investigated relations between root phenotypic responses and nutrient accumulation and we uncovered, under low phosphate conditions, a correlation between plant biomass and the decrease of plant phosphate concentration in plant tissues, suggesting a dilution effect. By means of Genome Wide Association mapping and integration of multiple traits, we identified new genes regulating phosphate homeostasis in Lotus.