Elucidating Signalling Networks in Plant Stress Responses

Lead Research Organisation: University of Essex
Department Name: Biological Sciences

Abstract

We are dependent on the productivity of plants for all the food that we eat, either directly or to feed animals that we then consume. A major challenge for scientists is to understand how plants grow and develop in order to produce plants better suited to the role that we demand of them. When grown as crops plants face many environmental stresses that limit their ability to produce at their maximum potential. Such environmental limitations are caused by climatic pressures, such as high temperatures, lack of rain causing drought conditions and high light intensities. Conditions such as these are becoming more frequent as the consequence of global warming becomes more extreme worldwide (Intergovernmental Panel on Climate Change Working Group Fourth Assessment Report, 6th April 2007; http://www.ipcc.ch/). However, it is not only the physical world that plants must contend with but also the biological. Many organisms grow on plants as pathogens (causing disease) and using the plant as a food source they reduce the yields of crops. To cope with these stresses plants have developed a whole range of responses many of which are common irrespective of the type of stress. The plant responses are very complex involving changes in use of many genes and alterations in the levels of many hormones. Although biologists have identified several components of these response pathways it has become clear that to understand how they are all interlinked, new approaches are needed. Recently, the study of biology has been changing as biologists and mathematicians have begun to combine their expertise to produce mathematical models of biological systems, producing the new field of Systems Biology. Systems Biology holds out the promise of linking the data that biologists have been producing for many years in terms of genetics, biochemistry and physiology to produce models of plant behaviour that allow predictions to be made as to how a plant will respond to environment changes and how this response will affect plant growth. In this project we will take a Systems Biology approach to model the plant's response to several environmental stresses. The novel models that we will produce will allow us to predict how a plant will respond to a particular stress. Our long term goal is to use these models to select for plants that are more robust in their response to the increasing environmental pressures that they face to sustain our production of food.

Technical Summary

Plants respond to biotic and abiotic stress using a range of transcriptional and physiological response pathways many of which are shared between different stress stimuli. A crucial question is how plants switch between different stress responses and the balance of these response pathways when multiple stresses are perceived. In this project using systems modelling we propose to integrate the response pathways from three biotic (infection by Pseudomonas syringae, Hyaloperonospora parasitica, Botrytis cinerea) and two abiotic (drought and high light) stress responses in the leaf. Initially we will produce high resolution time course transcript profiles of our stress responses. We will cluster genes based on their temporal expression profiles. Using these data and prior information we will use state space modelling to create course grain network models. Networks common to more than one stress or containing key genes with different targets will be analysed further. A reiterative process will be used to verify the models by producing mutations or overexpression constructs for the nodal genes and measuring their consequence on gene expression and host plant phenotype. Promoter motif modelling will be used to aid in identification of gene regulatory networks. As the project develops we will focus on 2-4 networks to model at a higher resolution where we will identify and confirm the linkages between genes using a range of experimental techniques. We aim to produce a linking course grain network that models plant leaf responses to environmental stress and detailed models of 2-4 networks involved in switching between different stress responses.

Publications

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Alvarez-Fernandez R (2021) Time-series transcriptomics reveals a BBX32-directed control of acclimation to high light in mature Arabidopsis leaves. in The Plant journal : for cell and molecular biology

 
Description We have monitored changes in the expression of thousands of genes in the leaves of the model plant Arabidopsis during their exposure to the onset of drought (over 13 days) to high light (over 6 hours). This generates large data sets that show responses in time and we can use highly specialised modelling techniques to identify novel genes that influence these responses to the environment. In both the example we did exactly this and have identified genes hitherto that have not been implicated in responses to drought or high light. These genes have profound effects on these responses and are now the focus of further research to see how these can be used in crop breeding to ensure the resilience of plant productivity. These datasets are available for any scientist to analyse and gain further insights. Further transcriptomics datasets have been added to accommodate responses to referees as part of preparing a re-submission of the high light research for publication.
Exploitation Route Continued funding will be sought to transfer the research and methods to crops.
Sectors Agriculture, Food and Drink,Environment

URL https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE87755
 
Description A US patent was awarded on the the use of the transcription factor HSFA1b to drive increased yield under a range of watering regimes. This led to a licensing agreement with DupOnt/Pioneer who evaluated the gene in maize. However, renewal of the agreement was not forthcoming because yield data for maize did not show a convincing increase. The effect may be confined to the Brassicaceae since we have seen the effect in Brassica juncea and Brassica napus.
First Year Of Impact 2008
Sector Agriculture, Food and Drink
Impact Types Economic

 
Description THEME [KBBE.2011.1.1-02] [Integrated approach to studying effects of combined biotic and abiotic stress in crop plants]
Amount € 432,400 (EUR)
Funding ID 289562 
Organisation European Commission 
Sector Public
Country European Union (EU)
Start 01/2012 
End 01/2017
 
Title Drought time series microarray data 
Description An extensive microarray data set for a highly replicated time series of the leaf 7 of Arabidopsis plants undergoing a 13 day transition from fully watered progressing to moderate drought stress just at the point of loss of leaf turgor. 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes  
Impact Too early to say because the database in GEO is embargoed until February 29th 2016. But forms the basis of the analysis in the Bechtold et al 2016 Plant Cell paper 
URL http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE65046
 
Title HL time series microarray data 
Description This data set is a highly replicated microarray time series (4 biological replicates with 4 technical replicates of leaf 7 of Arabidopsis exposed to high light from 0 - 6h and plants sampled at 0.5h intervals. The changes in gene expression reflected in time over this experiment established an important link between immediate responses to high light and subsequent acclimation to raise photosynthetic capacity in response to increased light intensities. The dataset is lodged with NCBI GEO. 
Type Of Material Database/Collection of data 
Provided To Others? No  
Impact At the moment the database is embargoed until 20th February 2017. This is so that we can publish an accompanying paper, which has just been submitted to Plant Cell at the time this submission. Once a manuscript gains acceptance and is published we will release the database to public access. 
URL http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE78251
 
Title high light and raised temprature comparisons with controls in Arabidopsis 
Description GSE87755 Arabidopsis Col0 5 week-old plants: control vs 30 minutes of exposure to high light stress (1000 umol m-2 s-1) GSE87756 Arabidopsis Col0 5 week-old plants: control vs 25 minutes of exposure to mild heat stress 27 degrees Celsius 
Type Of Material Database/Collection of data 
Provided To Others? No  
Impact None yet, since not due for release until 1/3/2017 
URL http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE87755
 
Title Increasing Photosynthetic Capacity in Plants 
Description The invention relate to the finding that manipulating the cryptochrome 1 (CRY1)-directed signalling pathway promotes the maximum photosynthetic capacity that mature fully expanded 20 leaves (so-called photosynthate source leaves that drive plant productivity) can achieve when challenged with an increased light intensity. In certain embodiments, the invention relates to the unexpected finding that Suppressor of PhyA-105 (SPA) proteins are negative regulators of photosynthetic capacity. Moreover, the 25 inventors have shown that Constitutively Photomorphogenic 1 (COP1) proteins, that interact with SPA proteins, also constrain maximum photosynthetic capacity in plants. The inventors' have also shown that B-BOX DOMAIN CONTAINING PROTEIN32 (BBX32) is a negative regulator of photosynthetic capacity and works in tandem with a second gene, 30 LONG HYPOCOTYL5 (HY5), which is a positive regulator of this process. Furthermore, elucidation of the gene regulatory networks controlling dynamic acclimation to high light also reveals that Cryptochrome 1 (CRY1) and Phytochrome B (PHYB) are positive regulators of photosynthetic capacity. 
IP Reference 2020158.8 (P050339-GB) 
Protection Patent application published
Year Protection Granted 2020
Licensed No
Impact Too early - initial filing, now looking to interest commercial partners to go to PCT and develop further.
 
Title PLANT RESPONSES 
Description The present invention relates to methods and uses for improving traits in plants which are important in the field of agriculture. In particular, the metho ds and uses of the invention use a plant Hsf to increase plant productivity, water use efficiency, dro ught or pathogen resistance. 
IP Reference WO2008110848 
Protection Patent granted
Year Protection Granted 2008
Licensed Yes
Impact The patent is being evaluated under the terms of an evaluation licence issued by Plant Bioscience Ltd to Pioneer Hi-Bred