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Systems analysis of tapetal regulatory networks required for pollen development

Reference	BB/J001295/1
Principal Investigator / Supervisor	Professor Zoe Wilson
Co-Investigators / Co-Supervisors	Dr Leah Band, Professor John King, Dr Caiyun Yang
Institution	University of Nottingham
Department	Sch of Biosciences
Funding type	Research
Value (£)	513,883
Status	Completed
Type	Research Grant
Start date	18/11/2011
End date	17/11/2014
Duration	36 months

Abstract

Pollen development is fundamental to plant fertilisation and seed formation, and is thus vital for food production. Controlling pollen fertility is critical in plant breeding and in hybrid production, with hybrid crops frequently out-yielding selfed lines by 20-30%. Developing a greater understanding of pollen development and the means to manipulate this for selective breeding, maximising fertilization and hybrid production are essential for increased productivity and sustainable agriculture. One of the most important anther tissues involved in pollen formation is the tapetum, which is in direct contact with the developing microspores and plays a major role in meiotic progression, microspore maturation and pollen wall formation. A number of transcription factors that are involved in regulating gene expression and function of the tapetum have been identified; one key transcription factor is ABORTED MICROSPORES (AMS). AMS expression is prolonged, from meiosis until tapetal degeneration during Pollen Mitosis II (PMII), implying multiple roles for AMS during anther development. We have identified ams transcriptional changes and confirmed late AMS targets, including an ABC transporter that is critical for pollen wall deposition and viable pollen formation, however AMS is also involved in additional earlier events in pollen development. We will conduct functional analyses of the AMS expression network to gain a greater insight on events occurring throughout tapetal development and aid understanding on the regulation and transfer of factors between the tapetum and developing microspores. Network inference and functional testing, combined with cell-specific mathematical modelling will be used to identify the principal players in the network and explore their regulatory relationships. This will facilitate a greater understanding of the relationship between the tapetum and developing microspores and of pollen formation in dicots and monocots.

Summary

Pollen development is fundamental to plant fertilisation and seed formation, and is vital for the production of most of the food that we eat. It also plays a critical role in plant breeding and the production of hybrid plants. Hybrids (results of crossing two separate plant lines) tend to be more vigorous, with 20-30% higher yields, compared to self-fertilised lines. An example of how important this can be is seen with hybrid rice in China, where growing hybrid lines provides additional food for 60 million people/annum. However, the production of hybrids is both time-consuming and costly. We are becoming increasingly aware of population increases and the need for sustainable, effective agricultural systems, with increased yield but less environmental impact. Understanding the process of pollen formation is a vital step in such strategies since it provides an opportunity for selective breeding, maximising fertilization and hybrid production. Over recent years significant progress has been made towards understanding pollen development, much of this has come from studying mutants that fail to produce viable pollen (male steriles) in the model plant Arabidopsis. However recent advances, mean that information on pollen regulatory networks from Arabidopsis can now be applied to crops. We have shown that the pathways for pollen development between Arabidopsis and rice and barley are highly conserved; therefore such data can directly impact on strategies for crop breeding and hybrid production. One of the most important anther tissues for pollen production is the tapetum and many male sterile mutants show tapetal abnormalities. It plays a key secretory role in events associated with meiosis, pollen wall formation and in the development of microspores to pollen grains. However, little is known about the relationship between the tapetum and the developing pollen, although the tapetum has been shown to be essential. ABORTED MICROSPORE (AMS) is a key regulatory gene in the tapetum, which shows prolonged expressed during pollen development, which appears to have multiple roles during pollen formation, including early events associated with meiosis and later stages when synthesis and secretion of the pollen wall materials occurs. Our analysis of AMS during pollen wall formation has identified AMS regulated targets, including an ABC transporter, which is involved in the transport of pollen wall materials from the tapetum to the pollen and recently lipid biosynthesis for the pollen wall. However, it is also involved in earlier events, for example in the progression of meiosis and tapetal Programmed Cell Death. Although we have data that AMS regulates additional targets, there has been no characterisation of these other roles. In this proposal we want to build on our existing data and analyse the function of AMS throughout tapetal development. We will also analyse the expression of key components in the network using inducible AMS constructs and test them for their role in pollen development. We will use mathematical modelling of this pathway to help understand the cellular specificity of the network and determine components of the network, which are functioning in the communication between the tapetum and developing pollen. We will also determine how AMS regulates the expression of its targets and whether this is via a change in the status of the chromatin to make it accessible for expression. This work will provide a greater understanding of how the tapetum and the AMS regulatory network function to control pollen formation. It will provide valuable information about pollen development, which will be useful to facilitate control of fertility for breeding, and for the development of hybrid lines for increased yield. The regulatory networks found in Arabidopsis are conserved in the monocots rice and barley, thus the comparative analysis of these networks will directly impact onto crop research in the UK and worldwide.

Impact Summary

Food Security is now a key global issue and the realisation that we will need to find food to meet a 50% population increase by 2050 provides major focus for the need for strategies to increase agricultural production, but not at the expense of environmental impact. Pollen development is fundamental to plant fertilisation and is vital for the production of most of the food that we eat, therefore understanding pollen development and the means to manipulate this for selective breeding, maximising fertilization and hybrid production are an essential basis for these advances. Providing detailed understanding of the pathway of pollen development is fundamental to the future development of hybrid lines and for selective breeding strategies. The observations that the pathway of pollen development is highly conserved between dicots (Arabidopsis) and monocots (rice and barley) (Wilson and Zhang, 2009; Fernandez-Gomez and Wilson unpublished) provides a valuable asset since the information obtained from distinct species can be compared and used to facilitate developments in crops. Outputs from this research provide opportunities for improving crop performance and help deliver food security, a strategic priority area supported by the BBSRC. WHO WILL BENEFIT FROM THE RESEARCH? - This project will generate important data on the regulatory networks for pollen development in higher plants, which will have direct impact in this field of developmental biology and will provide valuable information for plant breeders and biotechnologists. This will provide opportunities for F1 seed production, targeted breeding and for environmental issues relating to the limitation of gene flow and the release of genetically manipulated crops. - The data will provide basic information on the pathways and processes of gene regulation for plant development and aid understanding of this key stage, which is currently lacking. This is likely to have impact at all levels from specialised researchers, through to schools and textbooks. - The approaches being adopted will facilitate new technical developments linked to Systems Biology, both in the application and development of algorithms for Network Inference, but also in the cell-specific modelling of regulatory networks and comparative analysis of data between dicots and monocots. - International collaborations will benefit, in particular by our links with China. This has proved to be a very efficient way of developing new resources, technical developments and providing opportunities for staff exchange, development and networking, with has massive benefits for Reproductive Research specifically in the UK and China, but also in a worldwide context. HOW WILL THEY BENEFIT? - By basic information on the pathways and processes of gene regulation for plant development. - By understanding mechanisms of gene regulation within the tapetum and anther during pollen formation. - By the development of tools and resources for systems research, image analysis, mathematical modelling and reproductive biology. - By enabling basic research to be applied to strategies for manipulating fertility in crops. - Data generated will be stored in accordance with UKAS guidelines published in peer-reviewed journals. IMPACT STRATEGY: Our work and significance of our data will be imparted in a variety of ways: - By publications in Internationally significant journals, the presentation of data at National and International Conferences and the filing of patents. - Information will also be imparted through web sites to provide progress in the research areas. - By workshops and discussion forums with colleagues in the UK and China to ensure transfer of ideas and adoption of best practices. - Information and ideas linked to Plant Reproduction and GM will also be imparted to Schools, by talks, visits and placements within the PI's group. This provides opportunities to cultivate interests in young people in plant biology.

Committee	Research Committee B (Plants, microbes, food & sustainability)
Research Topics	Plant Science
Research Priority	Systems Approach to Biological research
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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