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

Lead Research Organisation: University of Glasgow
Department Name: College of Medical, Veterinary &Life Sci

Abstract

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.

Technical Summary

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.

Planned Impact

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.

Publications

10 25 50

publication icon
Asensi-Fabado MA (2017) Plant responses to abiotic stress: The chromatin context of transcriptional regulation. in Biochimica et biophysica acta. Gene regulatory mechanisms

 
Description To enable large-scale phenotyping of root system architecture (RSA) we have further developed a software package to analyses RSA in plants (EZ-Root-VIS; Shahzad et al 2018 Plant Physiol.). We then used the software for a Genome-Wide Association Study (GWAS) of RSA in 147 Arabidopsis thaliana accessions under four combinatorial nutrient regimes involving K, P and Fe. The GWAS identified several hundred loci associated with RSA in specific nutrient conditions. For selected genes we have characterised the changes of RSA in Col-0 KO mutants. Following a detailed molecular and genetic analysis of one candidate gene we discovered a novel role for RNA-directed DNA methylation (RdDM) in providing plants with robustness against failure in the auxin pathway. This pathway essentially underpins lateral root development in plants. Natural genetic variation in CLSY1 controls expression of auxin targets through DNA-methylation when the canonical auxin-controlled protein degradation pathways is disturbed. We found that the latter occurs under potassium deficiency conditions in an iron-dependent manner. CLS1 variants show differences in robustness to the low-K stress. Enhanced robustness mediated by the functional CLSY1 allele leads to improved lateral root development and plant performance under K-deficiency. Full proof of a gene locus identified through GWAS is difficult and rarely achieved, and the discoveries are novel in several aspects. In particular, the findings reveal a new physiological output of RdDM and a new link between epigenetic, transcriptional regulation and post-translational regulation. . The results were published in Nature Communication (Shahzad et al. 2020).
Exploitation Route The identified genes can be used as markers for marker assisted breeding of improved crop varieties. The software package is already used by many colleagues in academia,
Sectors Agriculture, Food and Drink

URL http://blog.garnetcommunity.org.uk/?powerpress_pinw=5441-podcast
 
Description The findings from this work have been disseminated through social media and have reached and generated interest beyond the scientific community.
First Year Of Impact 2021
Sector Agriculture, Food and Drink,Education
Impact Types Cultural

 
Description Member of BBSRC panel UK-India Newton Bhaaba Fund, Pulses and Oilseed Research Initiative (PORI)
Geographic Reach Asia 
Policy Influence Type Influenced training of practitioners or researchers
URL http://www.bbsrc.ac.uk/funding/filter/2017-newton-fund-joint-call-pulses-oilseeds/
 
Description Exploring chemical 'de-priming' and quantitative genetics to improve growth and yield of soybean under abiotic stress.
Amount £502,636 (GBP)
Funding ID BB/R019894/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 08/2018 
End 08/2022
 
Title EZ-Root-VIS 
Description EZ-Root-VIS combines an updated version of our EZ-Rhizo software with a new software Root-VIS that allows visual reconstruction of riit system architecture from the image analysis data collected with EZ-Rhizo. 
Type Of Technology Software 
Year Produced 2018 
Impact Used for GWAS the software has allowed us to identify new genes required for root development in Arabidopsis thaliana. The paper has been submitted. 
 
Description Editor of a Special Issue on Root Phenotypes for the Future, Plant, Cell & Environment March 2022, with guest-editors Amelia Henry and Malcolm Bennett 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I initiated, organised and edited a Special Issue on 'Root Phenotypes for the Future with co-editors Amelia Henry, IRRI, and Malcolm Bennett (University of Nottingham). The Special Issue collates 12 review articles and 12 original papers on this important topic of plant science, related to food security and climate change. The Issue received wide interest over Twitter and other social media as well as the journal web page.
Year(s) Of Engagement Activity 2022
URL https://onlinelibrary.wiley.com/toc/13653040/2022/45/3
 
Description Editor-in-Chief of Plant, Cell and Environment 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Anna Amtmann has taken over as Editor-in-Chief of the International journal Plant Cell and Environment, which is widely read and has an Impact Factor of 6.2.
Year(s) Of Engagement Activity 2018
URL http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-3040
 
Description Glasgow Botanic Gardens 200th anniversary 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Displays of plant science research carried out at University of Glasgow in the main glasshouse (Kibble Palace) of the Glasgow Botanc Gardens as part of the 200th Anniversary celebratios. Our stalls offered a range of displays and hands-on activities related to our research in plant science as well as instructive games for children.
Year(s) Of Engagement Activity 2017
URL https://www.ugplantsci.org/gallery
 
Description Invited plenary speaker at Rooting 2021 (Joint: 9th International Symposium on Root Development & 11th Symposium of the International Society of Root Research) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited plenary talk in the Session 'Water & Nutrient Relations' at this large joint International conference, including a Q&A session after the talk.
Year(s) Of Engagement Activity 2021
URL https://www.rooting2021.com/
 
Description Invited presetentation at science conference 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited speaker at 2nd Workshop on Plant Development & Drought Stress, Pacific Grove, CA, USA. Organised by Carnegie Institute and American Society of Plant Biology (ASPB).
Year(s) Of Engagement Activity 2017
URL https://ww2.eventrebels.com/er/EventHomePage/CustomPage.jsp?ActivityID=21616&ItemID=77745
 
Description Invited talk at the SEB Annual Conference 2018 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Two talks in the Session 'Shaping Root Architecture..' at the SEB Annual meeting in Florence. : PI (invited) and post doc (selected from abstracts)
Year(s) Of Engagement Activity 2018
URL http://www.sebiology.org/events/event/seb-florence-2018
 
Description Plant Science cartoons 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact We produced a booklet featuring research topics in the Glasgow Plant Science Group in the form of cartoons. The booklet was (and is) distributed among visitors of the 200th anniversary celebrations of Glasgow Botanic Gardens and other public events.
Year(s) Of Engagement Activity 2017
URL https://docs.wixstatic.com/ugd/8cabfa_bcc30b9859b347e294d6ffe6c924205b.pdf
 
Description Social Media activity 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact I regularly share scientific news and topics through my Twitter account (1.5 K followers).
Year(s) Of Engagement Activity 2019,2020,2021,2022
URL https://twitter.com/AnnaAmtmann
 
Description Soeaker at the Festival of Algae2 17-18 Nov 2021 Birmingham organised by BBSRC NIBB Algae UK 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact A networking event between academia and Industry aim.ed at enhancing opportunities to grow Industry based on algal products (BBSRC NIBB Algae UK)
Year(s) Of Engagement Activity 2021
URL https://www.algae-uk.org.uk/events/a-festival-of-algae/
 
Description Speaker at COST Conference on Epigenetic Mechanisms of Crop Adaptation To Climate Change 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Talk with subsequent discussion at this conference organised by the EU COST action enhancing networking activities in Europe.
Year(s) Of Engagement Activity 2021
URL https://www.epicatch.eu/conference/
 
Description Tutor at Graduate Course: Transcription factors and transcriptional regulation 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact I contributed a talk and discussion to this joint post-graduate workshop of The University of Amsterdam and the University of Wageningen (organised by Gerco Angenent (Wageningen University) and Maike Stam (University of Amsterdam)).
Year(s) Of Engagement Activity 2021
 
Description Video Conversation on Plant-Plant Interactions with Dr. Tom Bennett (Leeds), Editor of a Special Issue in Plant, Cell & Environment: 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact In this video two scientists discuss how plants communicate with each other; widely accessed and attracted interest on Social Media (Twitter)
Year(s) Of Engagement Activity 2021
URL https://onlinelibrary.wiley.com/page/journal/13653040/homepage/plant_plant_interactions_conversation