Perception and integration of nutritional signals in plant root systems: Solving the mystery of K-Fe-P interactions.

Mineral elements are essential to human nutrition. For example, potassium (K) is the major electrolyte in the human body and is required for kidney, muscle, nerve and heart functions. Iron (Fe) is a component of redox enzymes enabling cellular energy metabolism and of hemoglobin carrying oxygen to the brain and to the peripheral tissues. Minerals are introduced into the food chain through plants. Their root systems actively forage the soil for beneficial mineral nutrients and extract them with the help of specialized transport proteins. As for humans, mineral nutrition is essential for plant health. The importance of the root system for yield and nutritional value of food crops has been recognized, and root research has taken a center stage in food security.
Plants can perceive signals about mineral nutrient availability in the soil and translate them into developmental and physiological processes that adapt root shape and transport activity, thereby maximizing foraging and uptake capacity. If we want to enhance nutrient usage efficiency of crops we need to understand the signaling pathways that mediate between soil conditions and root adaptations. The underlying mechanisms are complicated. Root systems act simultaneously as receptors perceiving nutrient availability and as effectors carrying out nutrient uptake. To achieve the best result they need to differentially regulate growth of individual root parts and transport in different cells. Without a centralized brain this involves both local and systemic signals and responses. Roots also need to integrate information on different nutrients and prioritize their responses, which requires crosstalk between individual nutrient signaling pathways.
We have recently made several discoveries that should enable a better understanding of how plants process multiple nutrient signals and regulate root system architecture. We identified two different ecotypes of the model species Arabidopsis thaliana that respond differently to low K supply. The Columbia (Col-0) accession maintains growth of the primary root but halts lateral root extension, thus displaying a long, narrow root system. By contrast, Catania (Ct-1) halts main root growth but extends lateral roots thus displaying a short, bulky root system. Both accessions look very similar when K supply is sufficient. Surprisingly, we could transform the Ct-1 root phenotype into the Col-0 root phenotype by subjecting the plants to low Fe together with low K - both accessions now developed long, narrow root architectures. Fe is known to play a role in root responses of Col-0 to low P, nevertheless, both accessions showed a similar response to low P (inhibition of main root only). Clearly, the Col-0/Ct-1 pair provides us with an excellent experimental model to discover the molecular processes that underpin developmental decisions of plants under nutrient stress, and to unravel nutrient-nutrient interactions.
In this project, we will combine electrophysiological methods and confocal microscopy with molecular genetics and automated root phenotyping to address the following questions: How is low-K perceived by root cells and what is the link to Fe redox metabolism? Which cellular processes underlie main root inhibition? Which signals link developmental responses of the main root with those of the lateral roots? How do different root architectures impact on nutrient uptake and on final nutrient contents in the leaves? Which genes determine root architectural responses to nutrient signals?
The results from this study can be expected to lead to a detailed understanding of the fundamental biological processes and genetic components that link soil-derived nutrient signals with root development and nutrient uptake. In particular we will provide new information on the functional relationship between three essential nutrients, K, P and Fe, which will be invaluable for future efforts to improve crop performance and nutritional quality.

As plants forage the soil for essential mineral nutrients they translate a multi-factorial input from different nutritional signals into a multi-factorial output of different root features. This process results in a root architecture that represents a particular adaptive strategy to cope with limited nutrient availability. In this project we will characterize the signaling pathway that links K/Fe availability in the root environment to the development of genotype-specific root architectures.The project is based on our recent discovery that two Arabidopsis accessions respond differently to low K supply. The Columbia (Col-0) accession maintains growth of the primary root but halts lateral root extension, thus displaying a long, narrow root system. By contrast, Catania (Ct-1) halts main root growth but extends lateral roots thus displaying a short, bulky root system. Both accessions look very similar when K supply is sufficient. Surprisingly, we could transform the Ct-1 root phenotype into the Col-0 root phenotype by subjecting the plants to low Fe together with low K; both accessions now developed long, narrow root architectures. The Col-0/Ct-1 pair provides us with an excellent experimental model to discover the molecular processes that underpin developmental decisions of plants, and to unravel nutrient-nutrient interactions. We will test mutants with diverse functions in K and Fe transport, Fe redox homeostasis and auxin transport for their ability to mediate the genotype-specific responses, and we will use electrophysiology and super-high-resolution confocal microscopy to characterize the cellular events occurring in roots subjected to changes in K and Fe supply. The targeted experimental programme will be complemented by genome-wide studies into the genetic and transcriptional differences between the two genotypes. The new information obtained in this project will be invaluable for future efforts to improve crop performance and nutritional quality.

Potassium (K) and iron (Fe) are essential minerals for human nutrition. Biofortification of crops for these elements would improve the nutritional quality of crops and hence make an important contribution to food security. Biofortification relies on a strong root system to ensure efficient uptake of the minerals form the soil, particularly when minerals are scarce. Fertilization comes at a considerable financial and environment cost. Nutrient uptake efficiency is therefore a core activity for ensuring sustainability of agriculture and food security. However, any success in improving uptake efficiency for a particular nutrient has to be measured against the effects that this may have on the usage of other nutrients. Understanding the interactive effects of different nutrients is therefore a prerequisite for effective enhancement of nutrient uptake/usage efficiency and for successful improvement of nutritional quality. This project will generate new understanding of interactive effects of K and Fe on root system architecture (RSA). RSA has been recognized as an important target of crop improvement, but due to its underground position our knowledge of the underlying regulatory processes is in its infancy.

A strong argument can be made for carrying out fundamental research into nutrient interactions and RSA in model species. Firstly, commercial high-performance crop varieties have been bred with optimal nutrient and water supply and have therefore lost genetic potential for adaptation to nutritional deficiencies or to water stress-induced nutrient imbalance. Secondly, the prospect of genome editing technology generates new promise for gene-targeted strategies to generate crop varieties with improved and robust nutrient usage efficiency. Such rationale design of new crop varieties requires detailed knowledge of the relationship between environmental signals and plant growth, and hence crucially depends on a detailed knowledge base generated in model species.

In addition to targeted investigation of the signaling pathways underling interactive effects between K and Fe, the project includes genome-wide approaches that will enable the identification of novel genetic components underpinning nutrient signaling and root architecture. The project has therefore excellent potential for gene discovery. Novel gene functions can provide markers for breeding efforts and could be commercialised to support crop development programmes in industry. The PI has ample experience with the commercialisation process and has recently licensed novel gene function to Bayer CropScience. Opportunities arising from this project will be spotted early on in discussions with the IP team at Glasgow University and with prospective industrial partners.

The project will contribute to scientific progress worldwide, not only through its fundamental new discoveries but also through the generation of raw data that can assist other scientists with their research. Root architectural data arising from this project will be processed with our new EZ Rhizo II software. EZ Rhizo II incorporates a searchable database in XLM format that is compatible with Root System Markup Language (RSML). RSML enables portability of root architecture data between different software tools and provides a standard format for a central repository for root phenotyping data. Thus, all data generated in this project can be combined with data generated in other labs using different softwares (e.g. RootNav and SmartRoot), genotypes and conditions for future incorporation into a publically available root architecture database.

The project offers excellent training opportunities for PDRA and technicians in a wide range of experimental techniques, including root phenotyping, electrophysiology, molecular biology, genetics, histochemical analyses and high-resolution microscopy. It will also provide training in bioinformatics and statistical analyses underpinning GWAS.