Plant systemic responses to changing root environments – PSYCHE

Plants, as sessile organisms, are highly impacted by environmental conditions. The soil is a highly heterogeneous environment for plant nutrition composed of a mosaic of local favorable versus stressful areas. Different stresses can be experienced locally by root systems, such as nutrient limitation, water deficit, and pathogen infections. Legume plants have also a unique capacity to associate with soil nitrogen fixing bacteria (rhizobia) to form specific root endosymbiotic organs called nodules. This plant-bacteria symbiosis allows legumes, in contrast to other crops, to acquire nitrogen from an unlimited source of gaseous atmospheric nitrogen (N2). This way, legume crops can escape from soil mineral nitrogen shortage that frequently limits plant growth in unfertilized soils. As root and nodule organ development and function are highly sensitive to abiotic and biotic stresses, this currently leads to unstable yields in many legume crops. There is therefore an urgent need to improve the adaptation of legumes to environmental stresses to allow generalizing the use of efficient symbiotic nitrogen-fixing plants in agro-ecological practices. Integrative developmental strategies allow plants to adapt to heterogeneous and fluctuating soil environments. Signals induced by local stresses in different part of the root system are integrated at the whole plant level to generate long distance systemic responses to promote root and symbiotic nodule development in non-stressed soil areas. These so-called foraging compensatory responses allow the plant to improve its nutrient acquisition capacity in non-stressed areas to compensate the effect of stresses. A better understanding of these systemic regulatory mechanisms may provide a biological basis to improve plant stress tolerance through innovative selection strategies. The PSYCHE project thus aims to compare systemic responses to various local stresses, namely Nitrogen (N)-deficiency, water-deficiency (drought), or pathogen infection, to identify gene co-expression networks involved in wide-ranging developmental compensatory responses induced by these different stresses to the local suppression of root and/or nodule formation and/or function. To discriminate unambiguously between direct responses associated to local stresses and responses related to systemic signaling, the PSYCHE project will use split-root experimental systems in the Medicago truncatula model legume. Preliminary data have already shown that systemic responses to a local N-deficit or to a local drought induce similar developmental compensatory responses, suggesting that systemic regulatory pathways related to the whole plant nutritional status may regulate the development of both roots and symbiotic nodules in response to different environmental stresses. These systemic responses to a local N- or water-deficiency will then be investigated at physiological and transcriptomic levels to identify common gene co-expression networks. In addition, to test if the concept of a shared systemic regulation of root and/or nodule compensatory responses can be extended to a biotic stress, we will use a local Aphanomyces euteiches root infection. The common systemic stress-regulated gene networks identified will then be functionally tested in mutants or transgenic plants altered in systemic pathways regulating both root and nodule responses. In addition, using a collection of natural stress-contrasting M. truncatula genotypes, we will identify evolutionary adaptive gene networks, whose genetic variation is both targeted by natural selection and associated with drought- and/or Aphanomyces-tolerance. Finally, we will determine the conservation of the systemic signaling pathways identified from the M. truncatula model to the pea legume crop, with the aim of developing molecular breeding strategies in different crops to improve plant compensatory responses to various heterogeneous soil stresses.