Unlocking nature's drought resilience: a focus on the parsimonious root phenotype and specialised root metabolism in wild Medicago populations

Background and aims: crop wild relatives, exposed to strong natural selection, exhibit effective tolerance traits against stresses. While an aggressive root proliferation phenotype has long been considered advantageous for a range of stresses, it appears to be counterproductive under drought due to its high metabolic cost. Recently, a parsimonious root phenotype, metabolically more efficient, has been suggested to be better adapted to semiarid environments, although it is not clear that this phenotype is a trait exhibited by crop wild relatives. Methods: firstly, we analysed the root phenotype and carbon metabolism in four Medicago crop wild relatives adapted to a semiarid environment and compared them with the cultivated M. truncatula Jemalong (A17). Secondly, we exposed the cultivated (probably the least adapted genotype to aridity) and the wild (the most common one in arid zones) M. truncatula genotypes to water deficit. The carbon metabolism response in different parts of their roots was analysed. Results: a reduced carbon investment per unit of root length was a common trait in the four wild genotypes, indicative of an evolution towards a parsimonious root phenotype. During the water deficit experiment, the wild M. truncatula showed higher tolerance to drought, along with a superior ability of its taproot to partition sucrose and enhanced capacity of its fibrous roots to maintain sugar homeostasis. Conclusion: a parsimonious root phenotype and the spatial specialization of root carbon metabolism represent two important drought tolerance traits. This work provides relevant findings to understand the response of Medicago species roots to water deficit.