13 ERA-CAPS: Plant root diffusional barriers: Genesis and implications for nutrient efficiency and stress tolerance

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

Abstract

Plant roots perform the critical function of controlling the uptake of water and essential mineral nutrients from the soil. This function is required by all land plants for their normal growth and development. Specialized cells in the root called the endodermis play a key role in controlling the transport of water and mineral nutrients from the roots to the leaves. These specialized cells have important cell wall modifications that acts as barriers to block the uncontrolled entry of water and mineral nutrients into the plant. Despite the importance of these barriers the molecular processes that control their development remain relatively unknown. By closely inspecting plants that contain mutations in genes thought to be involved in the development of these barriers the project team hopes to build a model that explains the mechanisms involved in the development of these barriers along with their function in water and nutrient uptake by the root as well as their role in preventing infection of roots by pathogens. Global food security is an issue of major international significance. The human population is predicted to reach 9 billion by 2050, increasing world demand for cereal by at least 1,000 million tons, a 50% increase on current levels. This increase needs to be achieved against a predicted decline in global crop production due to climate change causing reduced precipitation in many parts of the world where crops are currently grown. The root is the central plant organ required for water and mineral nutrient uptake from the soil by plants. More efficient water and mineral nutrient uptake by plants is needed to drive the increasing food production required to meet the challenge of increasing global crop production by 50% over the next 40 years. A better understanding of the mechanisms underlying root function will be central to the development of crops with the improved root systems needed to achieve such increased productivity to ensure global food security.

Technical Summary

We have designed an ambitious interdisciplinary research programme integrating molecular plant science with analytical chemistry, whole plant physiology and modelling. This programme aims to deliver a complete understanding of the biology of Casparian strips and suberin, across scales, from molecules to the whole plant. Such information will enable a molecularly directed manipulation of Casparian strips and suberin, providing new pathways for the development of crop varieties with improved nutrient and water use efficiencies, and enhanced resistance to root pathogens, salinity and water stress. Such traits are essential if we are to develop crops 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. By employing genomic, molecular genetic, chemical, biochemical and cell biological approaches we will discover and characterize the genes and molecular mechanisms involved in the biosynthesis of Casparian strips and suberin. Genetic resources characterized and developed through this mechanistic investigation will be leveraged to understand, at the root and whole plant level, the role of these physical and chemical barriers in mineral nutrient and water uptake, and root parasitic nematode infection. The ecological and adaptive function of these barriers to agriculturally relevant abiotic stresses such as water, mineral nutrient (deficiency and excess) and salinity will also be established. Building on this new understanding, mathematical models integrating molecular mechanistic knowledge with physiological processes at the tissue and whole plant level will also be built, providing predicative capacity to connect barrier properties with whole plant function.

Planned Impact

The beneficiaries of this research span the full spectrum of stack holders in the global agricultural enterprise, including private sector seed companies and public sector plant breeders, commercial and subsistence farmers, agricultural commodity traders, consumers and the wider general public.

Results from the research will have a significant positive impact on agricultural and horticultural crop yields through improved mineral nutrient and water use efficiencies and enhanced stress tolerance (e.g. salinity, flooding, drought, nutrient deficiencies, trace element toxicities and root pathogens). Such improvements will provide direct commercial benefits to seed companies by allowing the development and sale of cultivars better adapted to current and future changing environmental conditions. Commercial farmers will benefit economically through improved and sustainable yields with less inputs (fertilizers, water and pesticides) 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) and pesticides, helping to reduce the cost burden such inputs impose by improving their value/cost ratio. Improved water use efficiency and stress tolerance will also improve yields for subsistence farmers cultivating marginal lands. 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 will also impact food quality 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.

The ability to generate improved plant-based feedstocks for lignocellulosic biofuels through improvements in both the agronomic properties of the crop (improved mineral nutrient, water use efficiency and abiotic stress tolerance) and its chemical composition (lignin) will economically benefit seed companies and farmers in the UK through the creation of opportunities to generate, sell and cultivate new crops. Such improved biofuels feedstock would also be cultivated on more marginal agricultural lands competing less with food crops, helping to minimize the impact on overall food production.

By providing improved agricultural and horticultural crops for food production the proposed research will help 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. Further, the improved plant-based feedstocks for the production of lignocellulosic biofuels that will be enabled by this research will help transition the UK and global fossil fuel-based economies to more sustainable energy practices.

Related Projects

Project Reference Relationship Related To Start End Award Value
BB/L027739/1 01/08/2014 31/07/2016 £388,019
BB/L027739/2 Transfer BB/L027739/1 01/08/2016 30/11/2017 £157,259
 
Description We have identified the transcription fact that controlled the development of the Casparian strip in the endodermis of plant roots. We have also identified SGN3 as playing a key role in detecting damage to the Casparian strip and signalling a response by the plant which includes the deposition of ectopic lignin and suberin, a reduction in root hydraulic conductivity and ABA signalling leading reduced transpiration. Using the a combination of esb1 sgn3 and esb1 aba1 double mutants coupled to various physiological measurements we have show that these responses help to counteract ion-leakage by enhancing the ion concentration in the xylem by reducing xylem flow. These responses are essential for plants to cope with defective Casparian strips. This allows use to understand how plants balance plasticity in endodermal cell wall barriers (Casparain strips and suberin) with mineral nutrient and water uptake. Further, we have identified new components of the molecular machinery that builds Casparian strips, these include the two new dirigent proteins DIR9 and DIR18 and uclacyanin1 all of which appear to be involved in structured lignin deposition at the Casparian strip domain. Work is ongoing to determine the biochemical function of these proteins.
Exploitation Route The Casparian strip provide a physical barrier to diffusion of solutes and water across the endodermis allowing the plant to control the movement of water and mineral nutrients in and out of the root. Manipulation of this barrier provide the opportunity to affect such processes in crops to improve water and mineral nutrient use efficiency, and water and salinity stress.
Sectors Agriculture, Food and Drink,Environment

 
Description The identification of the transcription factor MYB36 is now allowing us to determine the molecular components required for the positioning and biosynthesis of the Casparian strip. We have also clearly identified a chemically specific role for the dirigent-protein ESB1 in the biosynthesis of lignin-based Casparian strips. This opens up a new way to control lignin structure, potentially impacting various uses of lignin including paper making and biofuels.
First Year Of Impact 2015
Sector Agriculture, Food and Drink,Environment
 
Description ERA-CAPS Root Barriers 
Organisation INRA (UMR-MISTEA) Montpellier, France
Country France 
Sector Academic/University 
PI Contribution Molecular plant physiology including Casparian strip development
Collaborator Contribution David E Salt (project leaders) at the University of Aberdeen is the overall coordinator for the consortium. The work of the consortium is split into five main work packages being performed at six institutions by eight groups. Work packages 1 and 2 at Aberdeen and Bonn will deliver a molecular mechanistic understanding of the genes and biochemical processes involved in the biosynthesis of Casparian strips and suberin. Mutant resources developed in work package 1 and 2 will be provided to labs performing work packages 3, 4 and 5 at the IPK, Copenhagen, Wageningen, INRA and Bonn, in order to develop a fuller understanding of physiological roles of the Casparian strip and suberin barriers.
Impact Held the first partnership meeting in Aberdeen in May 2014 to start the project. Each group has hired a postdoc or grad student as part of the project. A core set of A. thaliana mutants has been established and shared with each group.
Start Year 2014
 
Description ERA-CAPS Root Barriers 
Organisation Leibniz Association
Department Leibniz Institute of Plant Genetics and Crop Plant Research
Country Germany 
Sector Charity/Non Profit 
PI Contribution Molecular plant physiology including Casparian strip development
Collaborator Contribution David E Salt (project leaders) at the University of Aberdeen is the overall coordinator for the consortium. The work of the consortium is split into five main work packages being performed at six institutions by eight groups. Work packages 1 and 2 at Aberdeen and Bonn will deliver a molecular mechanistic understanding of the genes and biochemical processes involved in the biosynthesis of Casparian strips and suberin. Mutant resources developed in work package 1 and 2 will be provided to labs performing work packages 3, 4 and 5 at the IPK, Copenhagen, Wageningen, INRA and Bonn, in order to develop a fuller understanding of physiological roles of the Casparian strip and suberin barriers.
Impact Held the first partnership meeting in Aberdeen in May 2014 to start the project. Each group has hired a postdoc or grad student as part of the project. A core set of A. thaliana mutants has been established and shared with each group.
Start Year 2014
 
Description ERA-CAPS Root Barriers 
Organisation University of Bonn
Country Germany 
Sector Academic/University 
PI Contribution Molecular plant physiology including Casparian strip development
Collaborator Contribution David E Salt (project leaders) at the University of Aberdeen is the overall coordinator for the consortium. The work of the consortium is split into five main work packages being performed at six institutions by eight groups. Work packages 1 and 2 at Aberdeen and Bonn will deliver a molecular mechanistic understanding of the genes and biochemical processes involved in the biosynthesis of Casparian strips and suberin. Mutant resources developed in work package 1 and 2 will be provided to labs performing work packages 3, 4 and 5 at the IPK, Copenhagen, Wageningen, INRA and Bonn, in order to develop a fuller understanding of physiological roles of the Casparian strip and suberin barriers.
Impact Held the first partnership meeting in Aberdeen in May 2014 to start the project. Each group has hired a postdoc or grad student as part of the project. A core set of A. thaliana mutants has been established and shared with each group.
Start Year 2014
 
Description ERA-CAPS Root Barriers 
Organisation University of Copenhagen
Country Denmark 
Sector Academic/University 
PI Contribution Molecular plant physiology including Casparian strip development
Collaborator Contribution David E Salt (project leaders) at the University of Aberdeen is the overall coordinator for the consortium. The work of the consortium is split into five main work packages being performed at six institutions by eight groups. Work packages 1 and 2 at Aberdeen and Bonn will deliver a molecular mechanistic understanding of the genes and biochemical processes involved in the biosynthesis of Casparian strips and suberin. Mutant resources developed in work package 1 and 2 will be provided to labs performing work packages 3, 4 and 5 at the IPK, Copenhagen, Wageningen, INRA and Bonn, in order to develop a fuller understanding of physiological roles of the Casparian strip and suberin barriers.
Impact Held the first partnership meeting in Aberdeen in May 2014 to start the project. Each group has hired a postdoc or grad student as part of the project. A core set of A. thaliana mutants has been established and shared with each group.
Start Year 2014
 
Description ERA-CAPS Root Barriers 
Organisation University of Wageningen
Country Netherlands 
Sector Academic/University 
PI Contribution Molecular plant physiology including Casparian strip development
Collaborator Contribution David E Salt (project leaders) at the University of Aberdeen is the overall coordinator for the consortium. The work of the consortium is split into five main work packages being performed at six institutions by eight groups. Work packages 1 and 2 at Aberdeen and Bonn will deliver a molecular mechanistic understanding of the genes and biochemical processes involved in the biosynthesis of Casparian strips and suberin. Mutant resources developed in work package 1 and 2 will be provided to labs performing work packages 3, 4 and 5 at the IPK, Copenhagen, Wageningen, INRA and Bonn, in order to develop a fuller understanding of physiological roles of the Casparian strip and suberin barriers.
Impact Held the first partnership meeting in Aberdeen in May 2014 to start the project. Each group has hired a postdoc or grad student as part of the project. A core set of A. thaliana mutants has been established and shared with each group.
Start Year 2014
 
Description Niko Geldner Université de Lausanne 
Organisation University of Lausanne
Department Department of Plant Molecular Biology
Country Switzerland 
Sector Academic/University 
PI Contribution The Salt group works very closely with the group of Niko Geldner on the molecular biology and function of root diffusional barriers at the endodermis, including Casparian strips and suberin. We share reagents and analytical expertise in ICP-MS and mineral nutrient homeostasis.
Collaborator Contribution The group of Niko Geldner shares reagents, protocols and expertise in cell biology including confocal microscopy.
Impact 1: Li B, Kamiya T, Kalmbach L, Yamagami M, Yamaguchi K, Shigenobu S, Sawa S, Danku JM, Salt DE, Geldner N, Fujiwara T. Role of LOTR1 in Nutrient Transport through Organization of Spatial Distribution of Root Endodermal Barriers. Curr Biol. 2017 Mar 6;27(5):758-765. doi: 10.1016/j.cub.2017.01.030. PubMed PMID: 28238658. 2: Barberon M, Vermeer JE, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE, Geldner N. Adaptation of Root Function by Nutrient-Induced Plasticity of Endodermal Differentiation. Cell. 2016 Jan 28;164(3):447-59. doi: 10.1016/j.cell.2015.12.021. PubMed PMID: 26777403. 3: Kamiya T, Borghi M, Wang P, Danku JM, Kalmbach L, Hosmani PS, Naseer S, Fujiwara T, Geldner N, Salt DE. The MYB36 transcription factor orchestrates Casparian strip formation. Proc Natl Acad Sci U S A. 2015 Aug 18;112(33):10533-8. doi: 10.1073/pnas.1507691112. PubMed PMID: 26124109; PubMed Central PMCID: PMC4547244. 4: Geldner N, Salt DE. Focus on roots. Plant Physiol. 2014 Oct;166(2):453-4. doi: 10.1104/pp.114.900494. PubMed PMID: 25288635; PubMed Central PMCID: PMC4213078. 5: Pfister A, Barberon M, Alassimone J, Kalmbach L, Lee Y, Vermeer JE, Yamazaki M, Li G, Maurel C, Takano J, Kamiya T, Salt DE, Roppolo D, Geldner N. A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects. Elife. 2014 Sep 16;3:e03115. doi: 10.7554/eLife.03115. PubMed PMID: 25233277; PubMed Central PMCID: PMC4164916. 6: Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot ML, Salt DE. Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proc Natl Acad Sci U S A. 2013 Aug 27;110(35):14498-503. doi: 10.1073/pnas.1308412110. Erratum in: Proc Natl Acad Sci U S A. 2013 Oct 1;110(40):16283. PubMed PMID: 23940370; PubMed Central PMCID: PMC3761638.
Start Year 2011
 
Description 2nd Workshop on Plant Development & Drought Stress, Asilomar, Pacific Grove, USA 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Give a talk on role of Casparian strip on water and ion transport at the 2nd Workshop on Plant Development & Drought Stress, Asilomar, Pacific Grove, USA
Year(s) Of Engagement Activity 2017
 
Description Casparian strip as a transport gateway, IPNC, Copenhagen 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Gave a talk on the Casparian strip as a transport gateway, IPNC, Copenhagen
Year(s) Of Engagement Activity 2017
 
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 Max Planck Institute of Plant Breeding Research, Cologne, Germany, 24th 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 the Max Planck Institute for Plant Breeding
Year(s) Of Engagement Activity 2018
 
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 School of Biological Sciences, University of Birmingham, UK 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Give a talk on Casparian strip biogenesis at School of Biological Sciences, University of Birmingham, UK
Year(s) Of Engagement Activity 2018
 
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