The role of the oxylipin OPDA in the seasonal sensitivity of seed dormancy

Lead Research Organisation: University of York
Department Name: Biology

Abstract

Seasonal plant growth, typically initiated with the onset of bud burst or seed germination in the spring and terminated with the onset of dormancy in the progression through autumn to winter, is a well recognised natural phenomenon that can affect annual atmospheric gas exchange on a global scale. Environmental cues such as day-length and temperature are well known to directly affect plant growth and development, but much less is known about how such cues are used by plants to establish dormancy in advance of major seasonal change. There is a growing interest in understanding the underlying mechanism responsible for these predictive responses, not least because such knowledge will help us to predict how wild plants and crops will respond to environmental change. We have recently made two important discoveries that point to a lipid signalling molecule, OPDA, having a central role in controlling dormancy in seeds and being involved in the transfer of information governing seasonal growth control from one generation to the next. Both of these discoveries were made in the model plant species Arabidopsis thaliana, but knowledge gained will be applicable to other plant species. In the first discovery we found that elevated OPDA is responsible for increased seed dormancy in several Arabidopsis mutants. Exogenous OPDA application inhibits germination and we have evidence to show it involves at least one downstream target, a transcription factor protein called ABI5 that increases in abundance in the presence of OPDA and is essential for the OPDA imposed dormancy in beta-oxidation mutant seeds. In the second discovery we found that the day-length in which Arabidopsis plants are grown has a dramatic effect on the levels of OPDA in vegetative tissues and the dormancy state of seeds in the next generation. This effect on OPDA and seed dormancy is dependent on a protein called Flowering Locus T (FT) that is involved in regulating expression in vegetative tissues of a key gene involved in the synthesis of OPDA. A major question that now needs to be addressed is how the 'memory' of day-length in vegetative tissues is transmitted to the next generation and manifested in the dormancy status of seeds. Our preliminary studies indicate that OPDA plays a central role in the memory retention across generations from vegetative material to seeds. Furthermore, other recent work suggests a similar mechanism involving the FT protein controls dormancy in vegetative buds in perennial species such as poplar trees. The aim of our research is to establish the mechanism by which environmental signals influence seasonal growth by modification of the dormancy state of vegetative buds and seeds. To achieve this aim we will first establish how the FT protein regulates OPDA levels in vegetative tissues and establish the mechanism by which FT-dependent information is transferred from one generation to the next. The most likely mechanism is one involving epigenetic non-permanent modification of DNA that can affect gene expression and hence traits and phenotypes from one generation to the next. In parallel with this work we will establish how environmental signals during seed development influence dormancy state and OPDA levels. We will also elucidate the signal transduction pathway involved in the OPDA mediated control of seed dormancy. Finally, building on our remarkable observation that the environment experienced during seed set influences the growth rate of plants derived from that seed, we will investigate if an epigenetic OPDA-dependent memory of the seed maturation environment is involved. The outputs of this research will impact on the way we predict how plant ecosystems respond to environmental change. It may also impact on the development of improved agronomic practice for the production of seeds that are less dormant and/or give rise to crops that grow more vigorously.

Technical Summary

Our recent published data have led us to propose a new model for dormancy control in plants in response to seasonal cues that places the oxylipin intermediate 12-oxophytodienoic acid (OPDA) as a central player. To test this model we will first establish the mechanism by which the FT protein that we have shown to be important in regulating dormancy in seeds regulates OPDA levels in response to daylength in vegetative tissues. We also aim to establish how the FT-dependent 'memory' of environmental cues experienced in vegetative tissues is transferred to the next generation. We have preliminary data to suggest an epigenetic process and this will be investigated by analysis of candidate genes with altered expression in seeds. We have also shown that OPDA synthesised directly in developing seeds is responsible for the increased seed dormancy found in Arabidopsis mutants altered in lipid metabolism and we now need to establish the effect of environmental cues on OPDA levels in developing seeds by metabolite profiling. We have demonstrated that the ABI5 transcription factor is a downstream target involved in the OPDA inhibition of seed germination and we will elucidate the other components in this important, new signalling pathway. One other player appears to be MFT, a close relative of FT with a recently revealed role in integration of the ABA and GA- germination response of imbibed seeds and which directly regulates ABI5 expression. We will perform a series of molecular genetic and gene expression studies to elucidate this pathway. We will also perform a suppressor screen on one of the lipid metabolism mutants that is dormant because of elevated OPDA levels and select non-dormant seeds. We are confident of this strategy since double mutants that lack ABI5 are no longer dormant. Finally, we will investigate the remarkable observation that the environment during seed set influences growth rate of resulting plants and establish if an OPDA mediated process is also involved.

Planned Impact

Beneficiaries of this Research This research will provide new understanding of how a lipid based signalling molecule is used by plants to control whether or not they enter a dormant state in response to environmental factors such as day-length and temperature. These results will open up a new field of research activity on how plants use environmental signals to influence future growth state in the same or subsequent generation. Commercial Organisations As well as being of obvious interest to the relevant research community this research will also give rise to results that will have impact with organisations involved in commercial production of seed and possibly also commercial production of plants by vegetative propagation. Seed production companies that employ agricultural biotechnology such as Syngenta are one type of commercial organisation that could benefit from this research, since it will produce candidate gene targets that could be manipulated to alter dormancy state and growth vigour in both vegetative and seed material. Thus these companies could use the outputs of the research to develop improved crops that are not as subject as their predecessors to environmental conditions and are higher yielding. Such an approach to realising these benefits would involve the use of transgenic technology and due to the time it takes for development of the technology in crops plus regulatory approval we predict a 5 to 10 year time frame following the completion of this research before the benefits to the company are realised in terms of return on investment. We expect that there could also be a second path by which seed and vegetative production based companies could realise the benefits of this research that does not involve transgenic technology, and would have a much shorter timeline to realising benefits in the order of 2-3 years. This is because the results of the research could inform such companies of best environmental conditions for production of seed or vegetative materials. In addition, seed coating technology is an industry in itself for companies such as the UK based Germains Seeds (http://www.germains.com/). The results of this research could benefit such companies by assisting in the development of new treatments that improve seed performance and subsequent plant growth. The development and deployment of such technology is likely to occur within a 2-3 year time frame from proof of concept. The results of this research could therefore lead to an increase in the economic competitiveness of the UK. Public and third sector beneficiaries The Knowledge Based BioEconomy (KBBE) is now recognised as one of the main routes for the UK and other Western economies to recover from the current recession. The lead applicant, Ian Graham, has been involved in informing UK Government and EU policy with respect to how plant biology can impact on the KBBE. Most recently this has been through the Department of Business Innovation and Skills Horizon Scanning and Roadmapping Report for Industrial Biotechnology 2010-2025, which recognises the importance and impact of plant biology research. The results from the current research will be used to inform such policy forming documents, which in turn influence future government funding to research councils and other organisations. Third sector beneficiaries of the results outputs will include charities such as the Syngenta Foundation and the Bill and Melinda Gates Foundation, both of which are committed to improving developing world agriculture. CNAP has existing collaborative research programmes with both these organisations. The benefits described above for commercial organisations would also be of relevance to the aims of both these charities in terms of developing world agriculture. We will showpiece the results of this research to these organisations to gauge interest and attract additional funding for development work in relevant crops.

Publications

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Barros-Galvão T (2019) cis-12-Oxo-phytodienoic acid represses Arabidopsis seed germination in shade conditions. in Journal of experimental botany

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Chen M (2014) Maternal temperature history activates Flowering Locus T in fruits to control progeny dormancy according to time of year. in Proceedings of the National Academy of Sciences of the United States of America

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Vaistij FE (2018) represses seed germination under far-red light by modulating phytohormone responses in . in Proceedings of the National Academy of Sciences of the United States of America

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Vaistij FE (2013) Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. in Proceedings of the National Academy of Sciences of the United States of America

 
Description Timing of seed germination is crucial for survival of plants in the wild and is also important for commercial seed production where there is a need to ensure uniform growth. A cold environment can signal an imminent winter so the mother plant produces dormant seeds that will not grow until the following spring. A warmer environment can signal an early summer with the mother plant producing seeds that grow immediately allowing another generation to grow before winter.

As part of the work carried out in this grant we have discovered that a regulator/transcription factor encoding gene called SPATULA can control the expression of five other regulatory genes that are known to effect when a seed germinates.

Working in partnership with the Penfield lab in Exeter (now moved to JIC, Norwich) we have discovered that the temperature experienced by the mother plant is transduced to the seed by the FT protein. In so doing FT controls seed dormancy through inhibition of proanthocyanidin synthesis in fruits. Transport of proanthocyanidin to seeds promotes dormancy by increasing seed coat tannin content. Thus maternal temperature history is integrated through FT in the fruit to modulate a metabolic signal that entrains the behaviour of progeny seeds according to time of year.

Building on our previous findings that the oxylipin OPDA acts along with ABA to regulate seed germination in Arabidopsis, we go on to demonstrate here that OPDA acts through the ABA-sensing ABI5 protein and the GA-sensing RGL2 DELLA protein. We further demonstrate that OPDA also acts through another dormancy-promoting factor MOTHER-OF-FT-AND-TFL1 (MFT). These results confirm the central role of OPDA in regulating seed dormancy and germination in Arabidopsis.
Exploitation Route This work represents a significant advance in our understanding of what controls seed dormancy and germination. We have demonstrated that an oxylipin signal plays a significant role in dormancy control and does this through a complex interaction with various other regulators of germination. Controlling seed dormancy remains a top priority for seed companies. Because the level of dormancy can vary in commercial batches of seeds a better understanding of what causes this variability is required. This new knowledge can and is being used by seed companies to better understand what environmental factors (such as temperature and light) impact on dormancy, the objective being to develop seed production conditions that result in less variable seed batches in terms of dormancy status.
Sectors Agriculture, Food and Drink

URL http://www.york.ac.uk/news-and-events/news/2013/research/germinating-seeds/
 
Description This research has provided a new understanding of how a lipid based signalling molecule is used by plants to control whether or not they enter a dormant state in response to environmental factors such as day length and temperature. These results are opening up a new field of research activity on how plants use environmental signals to influence future growth state in the same or subsequent generation.
First Year Of Impact 2016
Sector Agriculture, Food and Drink
Impact Types Economic

 
Description BBC Radio 4 Material World programme interview 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact The project PI, Professor Ian Graham, was interviewed by Quentin Cooper in the BBC Radio 4 'Material World' programme about the new insights in plant dormancy control described in the then newly published 2013 PNAS paper linked to this project, and wider implications of the research.
Year(s) Of Engagement Activity 2013
URL http://www.bbc.co.uk/programmes/b02qp1sm#programme-broadcasts
 
Description Press release: To germinate or not to germinate, that is the question 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact The press release was widely circulated across the media in both the UK and overseas.

The project PI, Professor Ian Graham, was interviewed on the BBC Radio 4 Material World programme about this research work as a result of the press release.
Year(s) Of Engagement Activity 2013
URL http://www.york.ac.uk/news-and-events/news/2013/research/germinating-seeds/