Divining Roots: uncovering how SUMO-mediated responses control developmental plasticity

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

Abstract

Food security represents a major global issue. Significant improvements in crop yields are urgently required to meet the increase in world population by 2050. The ability of a crop to efficiently absorb water and nutrients from soil is dependent on its root system responding to the availability of these resources. For example, roots preferentially form branches when in contact with water employing a mechanism called hydropatterning. Understanding the regulation of root branching is of vital agronomic importance.

This research project will investigate how hydropatterning works to position new root branches in response to water availability. Our research project attempts to 'fill in the gaps' between roots sensing water availability and then branching. To help our studies, we have already identified plant signals and genes such as auxin and ARF7 that are important for this process. Several promising processes will also be characterised including one that modifies ARF7 that switches on root branching. The knowledge gained from this study will provide new information about the key genes and processes controlling root branching in response to water availability, helping scientists design novel approaches to manipulate root architecture to enhance resource capture and yield in crops.

Technical Summary

Root branching is influenced by the soil environment to improve foraging efficiency. For example, lateral roots initiate and develop towards the availability of water employing a novel adaptive response termed hydropatterning. We recently identified the molecular mechanism regulating hydropatterning (Orosa et al, 2018, Science). In brief, this mechanism involves the SUMO-dependent post-translational modification of the lateral root regulator ARF7. SUMOylation of ARF7 is required to recruit the Aux/IAA repressor protein IAA3. Blocking ARF7 SUMOylation disrupts IAA3 recruitment and hydropatterning. We conclude that this new form of auxin regulation controls root branching pattern in response to water availability.

The new BBSRC proposal takes this research beyond ARF7 and addresses how SUMO-mediated environmental responses control hydropatterning. In objective 1, we initially address whether a hydropatterning stimulus modifies ARF7 SUMO status by altering the stability and/or activity of SUMO machinery components. Objective 2 will determine which root tissue ARF7 SUMOylation takes place to trigger hydropatterning. In objective 3, we will pinpoint the ARF7 gene targets required to be asymmetrically expressed to promote hydropatterning. Finally, objective 4 will explore whether IAA3 controls hydropatterning via just ARF7 or interacts with other SUMOylated transcription factors. By unravelling the SUMO mediated signal transduction pathway during hydropatterning we lay the foundations for understanding a major regulator of plant-environmental responses.

The knowledge generated about the new signals, genes and their regulatory pathways will underpin on going efforts to re-engineer root systems architecture and improve crop performance. The expertise, resources and tools that have been assembled for this project at Nottingham and Durham with our international collaborators uniquely position us to successfully complete this project.

Planned Impact

Who will benefit from this research?
Life science researchers
Agronomists and plant breeders
Industrial collaborators
Members of the public

How will they benefit from this research?
The project will generate a number of new and innovative experimental tools, data resources and models that a wide spectrum of researchers from other disciplines would be interested in employing. For example, Life Scientists could employ similar approaches to study SUMO-regulated processes in other biological systems; plant breeders and agronomists will use the information generated about SUMO and its target genes and processes in breeding studies and/or to design new approaches to manipulate root branching in crops, forestry and horticultural varieties. This award would also help establish a knowledge base that will allow by Industrial collaborators, to be explored, helping generate IP and new products with the information. Members of the public would gain access to images and movies of root systems via the web-based 'Hidden Half' interface as part of this project.

Data generated during the project will be stored in accordance with UKAS guidelines and published in peer-reviewed journals. All biological materials generated will be deposited at the Nottingham Arabidopsis Stock Centre (NASC); whilst light sheet movies will be deposited at https://mediaspace.nottingham.ac.uk/tag/tagid/the%20hidden%20half for public access.

The project will also help train researchers experienced with working as part of a multidisciplinary 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 and materials generated would be made publically available during the period of the award as outlined above and in accordance with our data release statement (see Data Management Plant for details). Staff would be available to enter the UK work force in 2022. 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-Is and PDRAs will disseminate their results at scientific conferences, through published journal articles, annual IP review with PBL and at our annual Nottingham Research Innovation and Impact Showcase with >100 commercial organisations.

Datasets providing light sheet microscopy images and movies of root systems will be added to the web-based 'Hidden Half' interface as part of this project.

Publications

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Title Hydro-signalling : How air gaps in soils alter the distribution of root water and hormones fluxes, thereby blocking root lateral branching 
Description EGU23 presentation 
Type Of Art Film/Video/Animation 
Year Produced 2023 
URL https://figshare.com/articles/presentation/Hydro-signalling_How_air_gaps_in_soils_alter_the_distribu...
 
Title Non-invasive water flow imaging in roots at cell resolution - FSPM2023 
Description Slides from FSPM2023 talk March 28th 2023 by Valentin Couvreur Abstract: A key impediment to studying water-related mechanisms in plants is the inability to non-invasively image water fluxes in cells at high temporal and spatial resolution. Here, we report that Raman microspectroscopy, complemented by hydrodynamic modelling, can achieve this goal - monitoring hydrodynamics within living root tissues at cell- and sub-second-scale resolutions. Raman imaging of water-transporting xylem vessels in Arabidopsis thaliana mutant roots reveals faster xylem water transport in endodermal diffusion barrier mutants. Furthermore, transverse line scans across the root suggest water transported via the root xylem does not re-enter outer root tissues nor the surrounding soil when en-route to shoot tissues if endodermal diffusion barriers are intact, thereby separating 'two water worlds'. 
Type Of Art Film/Video/Animation 
Year Produced 2023 
URL https://figshare.com/articles/presentation/Non-invasive_water_flow_imaging_in_roots_at_cell_resoluti...
 
Description The award provided new discoveries about how plants respond to environmental stresses using a protein modification system called SUMO.
The researchers also characterised a key plant protein called ARF7 (which regulates when roots branch) that is a target for SUMO modification
and the important role of a protein (termed OTS1) which removes SUMO from ARF7.
Exploitation Route The results have underpinned a £5M BBSRC sLOLA award to characterise the entire SUMO machinery and their targets.
Sectors Agriculture

Food and Drink

URL https://www.sumocode.org
 
Description SUMOcode: deciphering how SUMOylation enables plants to adapt to their environment
Amount £3,647,367 (GBP)
Funding ID BB/V003534/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 03/2021 
End 02/2026
 
Description SUMOcode: deciphering how SUMOylation enables plants to adapt to their environment (BB/V003534/1) 
Organisation Durham University
Department School of Biological and Biomedical Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution Plant Cell Biology, imaging and phenotyping
Collaborator Contribution Durham brings SUMO expertise complementing our own organisation's plant cell biology and phenotyping expertise
Impact sLOLA award just started
Start Year 2021
 
Description Science Fair (Nottingham) 
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 1500 members of the public (based on tickets issued for the event) attended the event.
Our project was presented in lay person terms and several exhibits provided of our work and its wider societal importance.
Year(s) Of Engagement Activity 2024
URL https://wollatonhall.org.uk/science-in-the-park/