Cell-type-specific environmental signal integration networks controlling a binary developmental switch during the life cycle of plants

A growing human population is placing increasing demands on agriculture, with current production needing to double by the year 2050. Compounding this challenge are the effects of climate change which are limiting the yields we have previously come to expect. The need to develop crop varieties resistant to the yield-limiting effects of environmental change is urgent. The information generated by this project will be vital to the successful development of new crop varieties with sustainably high yields across a range of environmental conditions.
In order to ensure their survival and reproductive success, plants have evolved the ability to alter the timing of decisions during their life cycle in response to a wide variety of signals from their environment. Key choices during plant development include the decision to reproduce, or start flowering, and the decision to commence growth, which begins with the germination of their seeds. Both of these transitions are influenced by more than one cue from the environment, including light, temperature and nutrients. The process of signal integration describes the incorporation of multiple pieces of information into a single verdict. This amalgamation of information occurs in plants through a complex series of interactions between various molecules. This project will use seed germination as a model system to understand how diverse environmental signals are integrated into a single binary decision, to terminate dormancy and start germination.
Many individual factors mediating seed responses to the environment have been uncovered previously. What is not known is how these individual components interact with one another to form a signal integration network. This proposal will fill this gap in our understanding by defining the molecular network which plants use to merge diverse environmental cues into a single decision to commence their growth. The project will as well define previously uncharacterized components of the signal integration process, and explain how information from the environment is passed onto the final molecular targets that drive the final decision.
It is well known that plants use multiple pieces of information to guide their developmental transitions, yet it much less clear in which cells this decision-making process occurs. The proposal will investigate the role of a specialized sub-group of cells within the plant embryo that we have recently uncovered as a site where diverse signals are integrated into a single decision. The way the environment controls the signal integration network within each of these cells will be determined, characterizing a cellular decision-making centre in plants.
The information derived from this project will represent a step change in our ability to develop crop plants with robust yields across a wide range of environmental conditions. Previous attempts to modify plant response to the environment using individual components have been met with limited success, largely due to the lack of understanding of how these isolated factors exert their influence through a complex series of interactions within molecular signal integration networks. In order to accurately and robustly modify plant response to the environment, we must first understand what these networks are, and how they function to control plant responses. This knowledge can be used to tactically perturb key interactions, rather than individual components, to achieve a desired output.
Another factor limiting the success of modifying plant response to the environment is a lack of understanding of the spatial control of these processes. Distinct decisions are made within distinct sites. The ability to target modifications to interactions present within specific cells that are making key decisions will greatly enhance our ability to modify plant behaviour in response to the environment.

Plants as sessile organisms have evolved the ability to modulate their developmental programs based on a wide range of environmental cues to ensure their survival and successful reproduction. The process of signal integration describes the information processing system by which multiple perceived environmental cues are integrated by a complex network of molecular interactions into a single binary developmental output. Key gaps in our understanding of this process in plants are a lack of knowledge of the signal integration network topology at a molecular level, and the cellular sites where this information merger occurs.
This proposal will address these gaps in our knowledge by defining the molecular network underlying the integration of diverse signals in seeds. The passage of each light, temperature and nutrient signal through this network and their convergence upon the promoters of two GA3-oxidase gene promoters, representing the downstream targets of an integrated signal, will be uncovered. The quantitative dynamics of this network will be determined within individual cell types of the newly described signal integration centre in plant embryos using a novel computational 3D quantitative image analysis pipeline. This work will collectively provide a multi-scale link between environmental cues, and the quantitative dynamics of the molecular networks mediating the merger of diverse information within specialized cell types.

There is currently an urgent need to develop crops resistant to climate change. The information generated in this project will be of great value to both crop breeders and industry who are seeking to modulate plant response to the environment and enhance crop productivity despite environmental fluctuations. The project will uncover both new components involved in mediating plant response to the environment in addition to understanding how these pieces fit together to generate responses. Both these new components and their newly identified functional interactions provide novel targets to develop new technologies for climate change-resistant crop development, Understanding the role of individual cell types in the control of plant environmental responses represents an additional level of information and understanding that can be used to control individual environmental responses through the development of new technologies using cell type specific promoters.
This project will result in the training of a PDRA who will develop a range of molecular biology skills in addition to imaging and novel quantitative computational analyses of these images. This will result in a highly qualified research scientist who will contribute to the competitive UK research. The technician will obtain additional skills and research experience over the duration of this project and contribute to UK research over a longer term.
A wider public interest in this work will also be generated as it related to mitigating the negative impacts of climate change on our food supply. Both the rising cost of food and the impact that a changing climate is having on the agricultural industry is of increasing interest to the media and general public. The notion of the capacity of plants to make decisions and the role of the specialized subgroup of cells within the embryo can also stimulate a philosophical general interest in biological processes outside of the animal kingdom.

Impact activities and publications will be undertaken and written by Dr. George Bassel. Computational aspects of this project will include an informal collaboration to further develop the open-source software package MorphoGraphX with Professor Richard Smith (Max Planck Insitute, Cologne) (see letter of support for this application), and webpage development will be undertaken by all members of the proposal. Pathways to Impact will be monitored and evaluated every six months. Web site impact will be monitored by collecting website statistics.