The natural genetic basis of cooperation in Arabidopsis: implications for crop improvement

Lead Research Organisation: University of Oxford
Department Name: Plant Sciences

Abstract

How will the UK increase its future agricultural productivity?

One of the major successes in agricultural production involved the artificial creation of dwarfed plants. On account of their small size, these plants did poorly against taller competitors. When grown together, however, dwarfed plants provided a major boost to crop productivity. This success story is sometimes told as 'reversal' of natural selection's work to produce tall and robust competitors. On the other hand, evolutionary biologists understand that natural selection will sometimes favour 'weak' competitors. This can occur when neighbours are genetically related (e.g., siblings), so that being nice to a neighbour means that you pass your genes on, albeit indirectly. My work is based on the idea that plants in nature often grow with relatives, and so these plants may have many unknown traits that benefit neighbours and promote group productivity. At the University of Oxford, I will search through many different variants of a model plant species (Arabidopsis thaliana, a relative of cabbage and mustard), aiming to discover these cooperative plant traits and their genetic basis. After finding the most cooperative types, I will determine how productive these natural variants are relative to the dwarfed plants currently used in agriculture. As the UK's need for sustainable agriculture grows, I want to know if Nature's work can be exploited to help meet the demand.

Technical Summary

Studying the genetic basis of plant adaptation can uncover natural alleles for future crop improvement. This is particularly true of 'social' adaptation, or how plants adapt to grow and compete with their neighbours. Evolutionary biology predicts that if plants grow with genetically related neighbours (e.g., siblings), then natural selection can favour cooperation, or reduced competitiveness over resources. Furthermore, because reduced competitiveness should free up resources for reproduction, cooperation can promote group productivity (e.g., crop yield); indeed, this is one way of interpreting the success of agriculture's green revolution. My proposed research, focussed on the model plant Arabidopsis thaliana, is based on the idea that wild A. thaliana plants often grow with relatives, and so their genomes may contain many unknown genes that benefit neighbours and promote group productivity. To address this, I will exploit the Arabidopsis MAGIC inbred lines--a new genetic resource that captures much of the natural variation in the species. Specifically, I will: (1) perform a QTL analysis to map the genetic basis of plants' competitiveness towards related neighbours; (2) use RNA-Seq to test whether the expression of cooperative traits depends on the detection of related neighbours; and (3) determine how the group productivity of naturally cooperative genotypes compares with that of 'green revolution' genotypes. My work will address fundamental questions about the genetic basis of plant adaptation to the social environment, and it will also have practical implications for crop improvement. As the need for sustainable agriculture grows, I want to know if nature's work can be exploited to help meet the demand.

Planned Impact

Who will benefit from this research?

-- plant breeders and agronomists working in research and industry related to food crops
-- plant breeders and agronomists working in research and industry related to energy crops
-- the general public

How will they benefit from this research?

My work will identify candidate genes associated with reduced competitiveness toward genetically similar neighbours. This reduced competitiveness will often lead to higher fruit and seed production in food crops. Hence, plant breeders and agronomists in the food industry may eventually use my results to select for or design cultivars with higher collective yield (realistically, in the next ten years). This has the potential to boost the UK's agricultural productivity without increasing the use of chemicals or expanding agricultural land use. This will benefit the health of UK society and will contribute to the protection of the UK's natural biodiversity.

My research may also help to boost the productivity of energy crops. In this case, the goal is to encourage plants to allocate more energy to competitiveness (e.g. stem biomass) and less to reproduction. Social biology suggests that increased competitiveness can be promoted by encouraging interactions among individuals who are not genetically related. Increasing the productivity of energy crops may ultimately contribute to reductions in the UK's production of greenhouse gasses.

Finally, my work will be of general interest to the public. They will benefit by learning about how evolution has shaped the productivity of plants in nature and what this says about the possibilities for further improvements in agriculture. This will contribute to UK culture by encouraging public interest in basic science and its potential practical benefits.

Publications

10 25 50
 
Description One of the greatest global challenges is to produce more food without continued expansion of agricultural land. A major question that my fellowship asked is: what kind of traits and genes could help a group of plants to grow more efficiently, producing more fruits and seeds in a given area?

I addressed the idea that all plants face a fundamental trade-off between selfishness and group productivity. Traits that are good for the individual-allowing plants to gather more resources for their own reproduction-will not be good for the group; instead, groups of plants made up of unselfish (or "cooperative") individuals will have the highest collective productivity. I tested this with a new type of genetic resource that brings together a huge amount of natural genetic variation into a single study population (so-called "MAGIC" populations).

First, using a MAGIC population of the model plant Arabidopsis thaliana, I found that traits which promote individual reproduction in the absence of competition (e.g., being tall, large-leaved, fast-growing, and using lots of water) consistently had a strong negative effect on the total fruit production of monoculture groups. I also identified several Arabidopsis genes that cause small size and reduced selfishness but high group productivity. This work suggests that plant genotypes that appear to produce small and weak individuals are actually the ideal types for high productivity in a dense group, where they can efficiently exploit the local environment without interfering with neighbours.

Second, I applied my approach to a MAGIC population of UK winter wheat, grown as individual plants (without competition) and in monoculture groups in a crop environment. Here, I found that whilst the tallest genotypes did best when growing alone, the very shortest genotypes produced the highest collective grain yield in groups, especially when plants were grown at high-density (roughly twice the typical density used by UK farmers). These results suggest that wheat varieties with relatively non-selfish traits and genes (e.g., for being very short) could be highly productive in ultra-high-density crops. Harnessing more cooperation among plants could be the key to future breakthroughs in the sustainable intensification of agriculture.
Exploitation Route 1. Findings from Arabidopsis MAGIC lines
The candidate cooperative genes that I have discovered come from natural populations. One question to address is why some plants in nature have evolved traits that result in relatively little competition with neighbouring plants. The candidate genes involved could also be studied further to understand the mechanistic basis of how they allow the plant to cope with competition and associated stresses. Some of these genes could be incorporated into a crop species to ask whether they boost the crop's collective productivity (e.g., total grain yield). More generally, the approach of my Arabdopsis experiments can be applied to crop species, in order to identify key traits, and the underlying genes, that promote group productivity in high-density food crops.

2. Findings from Diverse Wheat MAGIC lines
I discovered traits that are not good for individual reproduction but which promote the collective grain yield of high-density crops. My experimental approach could be used to find additional traits with these same effects, and genetic mapping could be used to uncover the underlying genes. Ultimately, plant breeders could design new wheat varieties that incorporate a whole suite of "cooperative" traits and genes that would be ideal for ultra-high-density crop environments. We could further ask if these cooperative varieties are able to succeed not only in high-density environments but also in low-resource environments (e.g., using less nitrogen fertiliser) and high-stress environments (e.g., drought and high temperatures).
Sectors Agriculture, Food and Drink,Environment

 
Description My work with Arabidopsis thaliana, a so-called "model organism", showed how to use a genetically-diverse population to discover traits, and their underlying genes, that promote the collective productivity of plant groups. I have recently taken this discovery research and applied it to a preliminary field trial using a genetically-diverse population of UK winter wheat (in collaboration with the National Institute of Agricultural Botany and helped by a BBSRC Seeding Catalyst Award [BB/SCA/Oxford/17]). This initial trial has proven that my approach with Arabidopsis can feasibly be scaled up to the crop environment, promoting productivity in the agri-food sector. For example, we showed that the maximum grain yield from experimental plots comes from using the very shortest wheat lines (shorter than varieties typically used by UK farmers), grown at ultra-high-density (roughly twice the density of most UK wheat crops). These highly-productive genetic lines are available to farmers and plant breeders, and future research is aimed at finding even more traits and genes that will contribute to ultra-high-density grain yield. This work will ultimately contribute to the sustainable intensification of wheat farming in the UK and beyond.
First Year Of Impact 2017
Sector Agriculture, Food and Drink
Impact Types Societal,Economic

 
Description Seeding Catalyst Award
Amount £17,294 (GBP)
Funding ID BB/SCA/Oxford/17 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 09/2017 
End 02/2018
 
Title Arabidopsis MAGIC phenotypes 
Description A database of Arabidopsis phenotypes, involving genotypes grown both alone (no competition) and in groups (with competition). These are phenotypes of a relatively new mapping population--the mulitiparent advanced generation intercross (MAGIC) lines-- which can be used for fine-mapping the genetic basis of phenotypic variation in Arabidopsis. The dataset includes height, branching, leaf size, growth rate, water use, and reproductive success when plants are growing alone and in monoculture groups (all competitors from the same MAGIC line). 
Type Of Material Database/Collection of data 
Year Produced 2017 
Provided To Others? No  
Impact Mapping the genetic basis of growth and reproduction in Arabidopsis, with potential applications to other plant species. Testing predictions about which traits, measured on individual plants in the absence of competition, will predict the productivity of plant groups. For example, plant breeders may want to know which individual plant traits from a genetically-variable population will predict a genotype's success when the plants are grown in a dense crop environment. 
 
Title Diverse MAGIC wheat phenotypes 
Description Phenotypes of 500 lines of the NIAB Diverse MAGIC wheat population. All 500 lines were sown in field plots at NIAB at a density of 600 plants/m^2. Measured traits include: flag leaf size and angle, plant height, green leaf area, and total grain yield of each plot. The data can be used to map variation in any of these measured traits to a location in the wheat genome. 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? No  
Impact No impacts yet, but the data will be used to identify genes underlying variation in high-density wheat yield. The most productive MAGIC lines in high-density may also be used by plant breeders to develop new, high-yielding, high-density varieties of UK winter wheat. 
 
Description Diverse MAGIC wheat trials at National Institute of Agricultural Botany 
Organisation National Institute of Agronomy and Botany (NIAB)
Country United Kingdom 
Sector Academic/University 
PI Contribution I initiated this project as an application of my research on the ecology and genetics of competition in Arabidopsis. The project will use my expertise with analysing a type of genetic reference population ("MAGIC" lines) to discover new traits and genes that promote grain yield of winter wheat in high-density crop conditions. This project is partly funded by an Agri-Food Seeding Catalyst grant awarded to me, which has allowed us to measure early-season growth of all plants in the experiment.
Collaborator Contribution Collaborators at NIAB contributed seeds of the Diverse MAGIC wheat lines in this experiment and the experimental plots and staff expertise to sow, maintain, and harvest the experiment. NIAB will provide access to data arising from this experiment and from a concurrent experiment with MAGIC wheat grown at a standard density.
Impact A manuscript with the results from this experiment is now being prepared for submission to leading journals. I have also presented the results in several invited seminars, both in Canada and in the UK. This work is a multidisciplinary collaboration, combining evolutionary ecology, social evolution theory, genetics, and agro-ecology.
Start Year 2017
 
Description Phenomics of Arabidopsis MAGIC lines at the National Plant Phenomics Cente 
Organisation National Plant Phenomics Centre
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution I brought the idea of performing a competition experiment using the Arabidopsis MAGIC lines on the NPPC's small-plant phenotyping facility. I provided the seed material, designed the experiments, and analysed the data.
Collaborator Contribution Partners at IBERS performed pilot experiments and helped to design the main experiment on their small-plant phenotyping facility. They provided raw data from plant images taken over the course of the experiments.
Impact A manuscript with the results from this experiment is now being prepared for submission to leading journals. I have also presented the results at a conference and in several invited seminars, both in Canada and in the UK. This collaboration is multidisciplinary, involving plant ecology, social adaptation theory, plant phenomics, genomics, and quantitative genetics.
Start Year 2015
 
Description Phenomics of Arabidopsis MAGIC lines at the National Plant Phenomics Cente 
Organisation National Plant Phenomics Centre
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution I brought the idea of performing a competition experiment using the Arabidopsis MAGIC lines on the NPPC's small-plant phenotyping facility. I provided the seed material, designed the experiments, and analysed the data.
Collaborator Contribution Partners at IBERS performed pilot experiments and helped to design the main experiment on their small-plant phenotyping facility. They provided raw data from plant images taken over the course of the experiments.
Impact A manuscript with the results from this experiment is now being prepared for submission to leading journals. I have also presented the results at a conference and in several invited seminars, both in Canada and in the UK. This collaboration is multidisciplinary, involving plant ecology, social adaptation theory, plant phenomics, genomics, and quantitative genetics.
Start Year 2015
 
Description Invited seminar, Carleton University 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact I was invited to present a seminar at the Department of Biology, Carleton University (Ottawa, Canada) to its faculty and students. I presented my fellowship research results and future directions ("The Social Lives of Plants").
Year(s) Of Engagement Activity 2018
 
Description Invited seminar, University College London 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Other audiences
Results and Impact I was invited to present a seminar at the Genetics Institute of University College London, for faculty and students. I presented my fellowship research results and future directions ("Growing the Field of Darwinian Agriculture").
Year(s) Of Engagement Activity 2019
 
Description Invited seminar, University of Alberta 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact I was invited to present a seminar at the Department of Biological Sciences, University of Alberta (Edmonton, Canada) to its faculty and students. I presented my fellowship research results and future directions ("The Social Lives of Plants").
Year(s) Of Engagement Activity 2016
 
Description Invited seminar, University of Manitoba 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact I was invited to present a seminar at the Department of Biology, University of Manitoba (Winnipeg, Canada) to its faculty and students. I presented my fellowship research results and future directions ("The Social Lives of Plants").
Year(s) Of Engagement Activity 2017
 
Description Invited talk at MAGIC 2019 
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 This was an invited talk at a multi-parental populations workshop at NIAB (Cambridge), discussing genetic tools for crop improvement. About 50-60 national and international scientists and agronomists attended to present recent research and to discuss potential collaborations and future advances. As a result of the workshop, we submitted a review article to Heredity, called "Multi-parent populations in crops: a toolbox integrating genomics and gene-level QTL mapping with pre-breeding" (23 authors, including me).
Year(s) Of Engagement Activity 2019
 
Description Presentations for school students 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact Year 12 students from non-selective state schools were invited to Oxford University for a 'study day', where they learn about what Oxford researchers do. I used my research on the social lives of plants to explain how research in evolutionary biology can address both basic and applied problems. Students also played an interactive game involving cooperation and conflict to generate discussion and questions.
Year(s) Of Engagement Activity 2018
URL https://www.pathways.ox.ac.uk
 
Description Seminar, Imperial College London 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Other audiences
Results and Impact I was invited to present a seminar at Imperial College London (Silwood Park campus) on my fellowship research results and future directions ("Growing the Field of Darwinian Agriculture").
Year(s) Of Engagement Activity 2020