Root SAT-NAV: uncovering the molecular mechanisms guiding root angle in soil

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

Abstract

Food security represents a major global issue. Crop production has to double by 2050 to keep pace with global population increasing to 9 billion. This target is even more challenging given the impact of climate change on water availability and the aim to reduce fertilizer inputs to make agriculture become more environmentally sustainable. In both cases, developing crops with improved water and nutrient uptake efficiency would contribute significantly to the solution. Root architecture critically influences nutrient and water uptake efficiency. For example, phosphate uptake efficiency could be significantly improved by manipulating root growth angle to better explore the topsoil where it accumulates. Despite this knowledge, the genes that regulate root angle in crops remain to be identified. Root angle is primarily regulated by the gravitropic response. However, other directional signals like water gradients induce roots' stress-activated-tropisms navigation (SAT-NAV) system when encountering drying soil. Despite their obvious importance, it is currently unclear how hydrotropism interacts with gravitropism to enable roots to forage for water. Understanding the genetic and environmental regulation of root angle is therefore of vital importance to crop improvement.

Together with our collaborators, we have recently shown that root tips respond to changes in gravity or moisture by forming gradients of the plant hormones, auxin and ABA, respectively. After a gravity stimulus, auxin accumulates on the lower side of roots, inhibiting cell growth and causing roots to bend in the direction of gravity. We suspect that ABA functions in a similar way to direct root growth towards water. How do these hormones cause these changes? We have identified ~570 genes that auxin regulates to cause root bending. The effect of auxin on root bending is therefore very complicated. To help us deal with this complexity, we will employ a new approach termed Systems Biology that brings together the best of Biology and Maths. This involves generating a large body of experimental information about these different genes and the processes they control that is then integrated into mathematical models. Auxin regulates root bending by inducing responses in many different cells and tissues. Our model therefore has to include information not just about a list of genes but also consider their behaviour in many different root cells and tissues. We then need to determine how realistic our root model is, by designing experiments to test its ability to accurately predict real results. The model can then be used to test ideas and provide new insight about how auxin (or ABA) controls root bending at the gene, cell and tissue level. It will be very important to test whether our findings in the lab are relevant to soil. We will address this important question by exploiting new advances in non-invasive imaging to monitor root growth in soils using X-ray micro Computed Tomography (CT). Using this new imaging capability we will test the impact of altering root gravitropism and hydrotropism on root water and nutrient uptake efficiency in rice. The knowledge gained from this study will help scientists understand how best to manipulate root angle and enhance crop yield.

Technical Summary

Roots employ directional signals to explore the soil environment and acquire anchorage and resources. Root angle is primarily regulated by the gravitropic response. However, other signals like touch and water/oxygen gradients induce roots' stress-activated-tropisms navigation (SAT-NAV) system when encountering compacted, drying and water logged soil, respectively. Despite their importance, it is currently unclear how these signals and their tropic responses interact and override root gravitropism.

This project aims to uncover the mechanistic basis and functional importance of gravitropic and hydrotropic responses in roots of Arabidopsis growing on agar and crops growing in soil. Unlike previous genetic studies, our multidisciplinary approach will help develop a deeper understanding about how these directional signals and components of their tropic response pathways interact to control root angle. The experimental programme is broken down into 3 clearly defined objectives:

- Objective A will employ systems approaches to characterise the signals, networks and cellular mechanisms controlling root gravitropic and hydrotropic responses.
- Objective B will determine how these tropic response pathways interact to control root angle and regulate the biomechanics of organ curvature employing a multiscale mathematical model that will include hormone signalling, water fluxes, cell-wall remodelling, cell growth and tissue stresses.
- Objective C will employ microCT imaging of roots in soil to uncover the roles and relative importance of gravitropism and hydrotropism, exploiting recent advances at Nottingham

The knowledge gained from this study will be very relevant to the BBSRC Highlight Area "effects of environmental change on the soil-water interface: implications for food production and water supply".

Planned Impact

Who will benefit from this research? This BBSRC Award will help establish a knowledge base about the genetic regulation of root angle that will benefit breeders by generating molecular markers to select for root traits. Project results can also be exploited in other current grants with industrial collaborators. For example, in the BBSRC IPA award (BB/H020314/1) the modes of action of a series of root growth promoting agrochemicals developed by our Industrial Partner, Syngenta, are being explored.

The microCT technology and newly developed imaging tools employed in this project will facilitate deep phenotyping for root traits in crops. The PI and several of the CI/RCIs are part of the Nottingham hub for the new European Plant Phenotyping Network (EPPN) that will enable other European researchers access to these and other facilities.

The project will also generate a number of new and innovative experimental tools, data resources and models that a wide spectrum of researchers from academic and commercial organisations would be interested in employing. For example, Life Scientists are likely to use the new imaging tools, such as the vertical imaging confocal, and image analysis software, such as CellSeT and RootTrace. Researchers in the areas of mathematics and computer sciences would also be interested in using the multicellular models.

How will they benefit from this research? The research will enable scientists at commercial collaborators to understand how to improve root function for enhanced crop performance. These outputs provide practical solutions for improving crop performance and help deliver food security, and is very relevant to the BBSRC Highlight Area effects of environmental change on the soil-water interface: implications for food production and water supply

Data generated during the project will be stored in accordance with UKAS guidelines and published in peer reviewed journals in accordance with our data release statement (see section 1b of the case for support). All biological materials generated will be deposited at the Nottingham Arabidopsis Stock Centre (NASC); whilst models would be downloadable from the Edinburgh-based Plant Model Repository and then, following their publication, the Biomodels database at EMBL. Image analysis tools will be deposited on www.sourceforge.com where researchers can download code. Note: RootTrace has been downloaded over 1500 times, to date.

The project will also generate researchers experienced with working as part of a multidisciplinary research team. This multidisciplinary expertise will uniquely position them for employment in the UK Life Science and Pharmaceutical Industries.

In terms of timescales of benefits, selected data, materials and models generated would be made publically available during the period of the award as outlined in accordance with our data release agreement (see section 1b of the case for support). Staff would be available to enter the UK work force in 2015. Application of findings made by the award to create, for example, new products and IP, is anticipated to be on the scale of 5-10 years.

Engagement with end users and beneficiaries about the project: The PI, co-I's and PDRAs will disseminate their results at scientific conferences, via the CPIB website, and through published journal articles.

Publications

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Antoni R (2016) Hydrotropism: Analysis of the Root Response to a Moisture Gradient. in Methods in molecular biology (Clifton, N.J.)

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Band LR (2012) Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. in Proceedings of the National Academy of Sciences of the United States of America

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Belda-Palazon B (2018) PYL8 mediates ABA perception in the root through non-cell-autonomous and ligand-stabilization-based mechanisms. in Proceedings of the National Academy of Sciences of the United States of America

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Davies WJ (2015) Achieving more crop per drop. in Nature plants

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Fozard JA (2013) Vertex-element models for anisotropic growth of elongated plant organs. in Frontiers in plant science

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Fozard JA (2013) Modelling auxin efflux carrier phosphorylation and localization. in Journal of theoretical biology

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Jensen OE (2015) Multiscale models in the biomechanics of plant growth. in Physiology (Bethesda, Md.)

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Mairhofer S (2017) X-Ray Computed Tomography of Crop Plant Root Systems Grown in Soil. in Current protocols in plant biology

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Morris EC (2017) Shaping 3D Root System Architecture. in Current biology : CB

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Muller L (2018) Root Development

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Tardieu F (2017) Plant Phenomics, From Sensors to Knowledge. in Current biology : CB

 
Description Roots employ environmental signals to guide their growth and explore the soil to find sources of nutrients and water. Gravity is employed by roots to direct their growth downwards using a mechanism called gravitropism. Other signals like water causes roots' to redirect their growth towards its source using a mechanism called hydrotropism.

We developed a new CT (X-ray) imaging approach to see these important root adaptive responses occurring directly in soil.

We have also discovered that roots changes their direction of growth in response to gravity or water signals using plant hormones called auxin or ABA, respectively.

We were able to see for the very first time that roots form a gradient of auxin at the bottom (versus top) side of a root. This accumulation of auxin causes cells at the bottom (but not top) side of the root to stop growing, resulting in roots to bend downwards.

In contrast, the hormone ABA accumulates on the dry side of a root, causing cells to prematurely expand, resulting in the root growing towards the water source.

ABA and auxin control the direction of root growth by targeting different layers of cells.

The information generated will contribute to developing new approaches to improve crop performance.
Exploitation Route Academic route: our findings have obvious educational, agricultural and environmental value.
Non-academic route: The CT imaging approach we developed is being used to characterize movement of agrichemicals in soil by industry
Sectors Agriculture, Food and Drink,Education,Environment

URL https://www.cpib.ac.uk/research/projects/satnav/
 
Description The hormone reporters developed as part of this project have been widely used in the science community. For example, seed for the auxin reporter DII-VENUS was the most highly ordered line in the history of the International Arabidopsis Stock Centre. The image analysis software tools and mathematical models generated as part of this project have been widely used in the community. For example, a special graphic user interface (GUI) was developed for non-specialists to explore changing parameters in the models. This GUI was highlighted for special mention in Plant Cell, the highest impact factor plant journal in which it was published in 2014.
First Year Of Impact 2012
Sector Agriculture, Food and Drink,Education,Environment
Impact Types Economic