Genome-wide association mapping and landscape scale modelling of heritable ionomic diversity in Arabidopsis thaliana populations

Lead Research Organisation: University of Nottingham
Department Name: Sch of Biosciences

Abstract

The proposed research utilizes genetic approaches to identify the genes that control the way plants take up mineral nutrient found in fertilizers such as potassium and phosphorus and potential toxic substances such as sodium (for the plant), and arsenic and cadmium (for humans that eat the plants). By understanding how different forms of the genes we discover are used by plants to allow them to grow in soils containing different levels of mineral nutrients or potentially toxic elements we can understand the role these genes play in allowing plants to adapt to the varied soil conditions they are exposed to in their natural habitats. A better understanding of these adaptations in natural populations of plants would have significant practical benefits for agriculture by providing the information needed for the development of new varieties of crops better able to provide the increased yields needed to meet the future demand for more cereals for biofuels, more grain for meat, and more food for the additional 2 billion people expected by 2050. The increased crop yields needed to meet these coming challenges will require a significant increase in irrigated agricultural production which will bring with it increased salinity (elevated sodium) in soils and associated yield losses. Crops adapted to maintain yields in the face of increasing salinity will therefore be essential. More efficient use of mineral nutrient fertilizers by crops would also improve yields for farmers, enhance productivity of crops on poor soils, and limit the environmental and ecological damage the production and excess use of fertilizers causes. For most of the world's population, plants are also the major source of essential dietary mineral nutrients such as calcium, potassium, manganese, iron and zinc, and therefore efforts to improve the mineral nutrient content of staple foods such as rice, maize and cassava would have significant human health impacts. Plants are also the primary entry point for a variety of toxic minerals into the food chain such as arsenic and cadmium. A better understanding of how natural plant populations have evolved over thousands of years to grow in mineral nutrient poor soils or soils with elevated salinity, cadmium or arsenic would help guide how we develop crop varieties for the future that could deliver the needed increases in yield and quality while insuring these gains against a changing climate to ensure food security for all.

Technical Summary

The proposed research utilizes association, linkage and molecular genetic approaches to identify genes that underlie heritable natural diversity in mineral nutrition and trace element accumulation in natural Arabidopsis thaliana populations. Landscape scale modelling of this diversity will allow exploration of associations between this genetic diversity and the environment, providing a pathway to understanding the ecological function of these alleles in adaptation to soils. Incorporation of predicted climate scenarios within these landscape models will generate projected allele distributions across future landscapes, providing an approach to understanding and tracking climate change . This project builds on the PIs recent success in using genome-wide association (GWA) mapping to identify the causal genes underlying natural variation in foliar accumulation of sodium and cadmium in A. thaliana, and establishes a new collaboration with Prof. Pete Smith and Dr Alex Douglas. This partnership will allow the linking of plant genetic diversity to ecological function using the agriculturally and ecologically relevant trait of mineral nutrient and trace element homeostasis. The approach will combine genome-wide association mapping (validated by linkage mapping and molecular genetics) with landscape scale modelling. It utilizes the large pool of genetic diversity in natural populations of A. thaliana to identify genes, alleles and mechanisms of value in adaptation to the varied edaphic conditions A. thaliana populations encounter across the landscape. Once characterized this natural diversity offers potentially new approaches to manipulate such agriculturally important traits as salinity tolerance and mineral nutrient efficiency to develop crop varieties that are more resilient to the predicted impacts of climate change on soil fertility, and to improve yields in a more sustainable manner to deliver the yield gains required to meet future population growth.

Planned Impact

Results from the research could have a significant long term positive impact on agricultural and horticultural crop yields through improved mineral nutrient use efficiencies and enhanced stress tolerance (e.g. salinity, nutrient deficiencies, trace element toxicities). Such improvements could provide direct commercial benefits to seed companies by facilitating the development of cultivars better adapted to current and future changing environmental conditions. Commercial farmers would benefit from these improved varieties through improved and sustainable yields with less inputs (fertilizers and water) and through the ability to utilize new cultivars to adapt their agricultural practices to changing climatic conditions. Further, such improvements in agricultural and horticultural crops will also benefit subsistence farmers with limited access to inorganic fertilizers (primarily nitrogen, phosphate and potassium, secondarily sulphur and magnesium), helping to reduce the cost burden such fertilizers impose by improving the value/cost ratio for fertilizer usage. In addition, reduced utilization of fertilizers, achieved through improved mineral nutrient use efficiencies, will limit the environmental and ecological damage their production and excess use causes, benefiting the general public through enhanced quality of life.

Results from the research could also impact food quality in the long term by helping to increase the content of essential mineral nutrients and reduce toxic trace elements in food crops. For most of the world's population plants are the major source of essential minerals such as calcium, potassium, manganese, iron and zinc, and therefore efforts to improve the mineral nutrient content of staple foods such as rice, maize and cassava will have a positive impact on public health both in the UK and internationally. Plants are also the primary entry point for a variety of toxic minerals into the food chain such as arsenic and cadmium, and being able to limit there accumulation in food would also have a positive impact on public health both in the UK and internationally.

By providing improved agricultural and horticultural crops for food production the proposed research will help in efforts to move the UK and international agricultural systems towards more sustainable food production, providing improved food security against the backdrop of a changing earth's climate and surface chemistry.

Publications

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Busoms S (2018) Fluctuating selection on migrant adaptive sodium transporter alleles in coastal Arabidopsis thaliana. in Proceedings of the National Academy of Sciences of the United States of America

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Henderson IR (2017) Natural genetic variation and hybridization in plants. in Journal of experimental botany

 
Description We have developed the system needed to analyse the 20,000 plants required by the project including new growth conditions and better environmental control in the plant growth room. We have completed a pilot experiment designed to assess the best experimental design for the main experiment which include determining the optimum number of check lines to include in the main experiment and how best to use these lines statistically to control for variation in the experimental system over the 12-months it will take to grow and analyse 20,000 plants. We have completed the growth of 10,000 plants, harvested leaves and performed ICP-MS analysis on these 10,000 leaf samples. We have also completed the growth of 10,000 plants for collection of seed and analysed seeds from all accessions by ICP-MS. We have normalized all the data and used both the leaf and seed ionomic data to perform genome-wide association (GWA) analysis with 4 million SNPs per accessions. This analysis replicated the 5 major leaf ionomics associations we have previously published (HKT1, MOT1, HMA3, HAC1 and FPN2) and also revealed numerous other significant associations which we are analyzing. GWA analysis on the seed ionomic data has also been performed which revealed numerous significant associations which we are currently analyzing. Further, we have obtained elemental composition data for soil imputed to the collection sites of the 1200 accessions A. thaliana used for the above leaf and seed analyses, and performed GWA analysis using this soil data as phenotypes with 4 million SNPs per accessions. This analysis revealed numerous significant associations which we are now analyzing. We have also recently determined the existence of fluctuating selection on migrant adaptive sodium transporter alleles in coastal A. thaliana as part of our study extending GWA analyses into the native habitat of A. thaliana. We have recently published (Campos et al., 2021 Plant Journal) the leaf and seed ionomes of 1,135 accessions of A. thaliana studied in the project. This data has been made accessible to the community via a new tool called IonExplorer developed specifically for the exploration and download of the data. The tool is described in the publication and can be accessed at https://ffionexplorer.nottingham.ac.uk/ionmap/. The code base for the tool is available at https://bitbucket.org/ADAC_UoN/dr000081-web-service-ionome-seed-and-leaf-map/
Exploitation Route Our work should help other when designed large experiments that required phenotyping 1000's of plants over several months in a way that allows all the date to be combined for analysis. Once completed the alleles identified by GWA analysis will allow a better understanding at the genetic level how plants adapt to their soil environment and using conservation of gene function such knowledge can be translated into crops.
Sectors Agriculture, Food and Drink,Environment

URL https://ffionexplorer.nottingham.ac.uk/ionmap/
 
Description As part of a large phenotypic data set to help drive open access science through the iHUB (http://www.ionomicshub.org/home/PiiMS), GWA portal (https://gwas.gmi.oeaw.ac.at/), Araport (https://www.araport.org/), and the IonExplorer https://ffionexplorer.nottingham.ac.uk/ionmap/
First Year Of Impact 2015
Sector Agriculture, Food and Drink,Environment
 
Description AAAS 2017 annual meeting, Boston, 17th Feb, 2017 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Session on 'Arsenic in Food'
Year(s) Of Engagement Activity 2016
URL https://aaas.confex.com/aaas/2017/webprogram/Session15234.html
 
Description Bob Hirshon, Host/Producer, AAAS Science Update on talk/news radio stations nationwide, and on the national program "America in the Morning.", Feb 2017. 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Interviewed about arsenic in food for talk/news radio
Year(s) Of Engagement Activity 2017
 
Description Cadmium accumulation in cocoa, South American Cocoa Producers Cadmium workshop, June, 2017 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Cadmium accumulation in cocoa, South American Cocoa Producers Cadmium workshop
Year(s) Of Engagement Activity 2017
 
Description Carnegie Institute, Department of Plant Biology, Stanford, USA 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Talk on natural ionomic variation at the Carnegie Institute, Department of Plant Biology, Stanford, USA
Year(s) Of Engagement Activity 2017
 
Description GARNet 'Natural Variation as a Tool for Gene Discovery', Cambridge, UK 12 - 13th Dec, 2016 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Workshop on use of natural plant genetic variation
Year(s) Of Engagement Activity 2016
URL http://garnetnatvar2016.weebly.com/
 
Description GARNet 'Natural Variation as a Tool for Gene Discovery', Cambridge, UK 12 - 13th Dec, 2016 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Organised the workshop on natural genetic variation in plants
Year(s) Of Engagement Activity 2016
URL http://garnetnatvar2016.weebly.com/
 
Description Invited talk at Purdue University 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Purdue University, West Lafayette, Indiana, USA, 20 - 23rd May 2019
Year(s) Of Engagement Activity 2019
 
Description Keynote lecture, 2nd Asia-Pacific Plant Phenotyping Conference, Nanjing, China 23 - 25th March, 2018 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Key note talk on ionomic phenotyping
Year(s) Of Engagement Activity 2018
 
Description Keynote talk at Gordon Conference Salt and Water Stress in Plants 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Gordon Conference, Salt and Water Stress in Plants, Les Diablerets, Switzerland, 31st May - 5th June 2020
Year(s) Of Engagement Activity 2020
 
Description Pennsylvania State University, Department of Plant Sciences, State College, USA, 11th Oct, 2018 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Talk at Penn State Plant Science Department
Year(s) Of Engagement Activity 2018
 
Description Press conference AAAS annual meeting on Session 'Arsenic in Food: From Soil to Plate to Policy', 17th Feb 2017 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact Press briefing at AAAS
Year(s) Of Engagement Activity 2017
 
Description University of Lausanne, Lausanne, Switzerland, 14th Feb, 2019 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Talk at the Department of Plant Molecular Biology, University of Lausanne
Year(s) Of Engagement Activity 2019