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Auxin in transcription factor complex controls polarity in plant organogenesis

Reference	BB/M004112/1
Principal Investigator / Supervisor	Professor Lars Ostergaard
Co-Investigators / Co-Supervisors
Institution	John Innes Centre
Department	Crop Genetics
Funding type	Research
Value (£)	536,459
Status	Completed
Type	Research Grant
Start date	15/02/2015
End date	14/02/2018
Duration	36 months

Abstract

Auxin comprises the most important intercellular signal in plant development and functions in organogenesis and patterning through biosynthesis, transport and signalling. Auxin signalling occurs through binding of the auxin molecule to a TIR1/AFB F-box protein allowing interaction with Aux/IAA transcriptional repressor proteins. These are subsequently degraded via the 26S proteasome leading to derepression of auxin response factors (ARFs). Different combinations between members of the ARF, Aux/IAA and AFB families are believed to provide cell and tissue specificity to the auxin response. Moreover, auxin signalling also occurs through the auxin-binding protein 1 (ABP1), which - in the presence of auxin - inhibits endocytosis of PIN auxin efflux carriers to regulate directional transport. From experiments carried out in yeast and plants, we have identified a protein-protein interaction between two key regulators of polarity establishment during Arabidopsis gynoecium development. These are the auxin response factor ETTIN (ETT) and the bHLH protein IND. Interestingly, this protein complex can bind the natural auxin, indole-3-acetic acid (IAA) and our preliminary data suggest that binding of IAA changes the ETT/IND target gene set. This suggests the existence of an alternative signalling pathway for auxin, and since ETTIN is involved in the initiation and patterning of other organs, this pathway may be widespread throughout plant development. Here we will carry out studies to reveal the significance, mechanism and conservation of this novel IAA-controlled module, which is distinctly different from previously established modes of auxin action.

Summary

Multicellular organisms including plants and animals develop specialised organs, which are composed of different types of tissues. The structure - or pattern - of organs is determined by the polarity within tissues along axes of symmetry. In order to coordinate polarity across a tissue or organ, multicellular organisms use mobile substances such as hormones. The plant hormone auxin was one of the first hormones ever to be studied and the effect of auxin on light-regulated plant growth (phototropism) was investigated by Charles Darwin and his son Francis in the 1880s. It was, however, not until the 1930s that the auxin molecule was isolated and its molecular structure determined as indole 3-acetic acid (IAA). In plants, auxin plays an essential role in initiating organ formation and in patterning the organs in specific tissue types, including for example lateral roots, young leaves and those of the female reproductive organ, the gynoecium. Control of auxin dynamics is achieved at the levels of biosynthesis, transport and signalling. The auxin molecule was previously shown to mediate the interactions between specific proteins thereby causing the degradation of repressors of gene expression. It has also been established that auxin can influence its own transport via inhibiting internalisation of PIN auxin transporters. Although these mechanisms of auxin signalling can explain many processes of auxin action, other transcriptional signalling pathways are likely to exist to account for the plethora of processes in which auxin plays a role. We have identified an interaction between two proteins found in the model plant Arabidopsis, which both are key regulators of polarity in the gynoecium of the flower. They have been named ETTIN and IND and both act as transcription factors (i.e. directly control the expression of genes). From experiments carried out in yeast we know that together these proteins can physically bind auxin in a so-called receptor complex, and our preliminary data suggest that the target gene set of ETT and IND changes when they bind auxin. This suggests the existence of an alternative signalling pathway for auxin. ETTIN controls the initiation and patterning of other plant organs, and in accordance with this, we identified other transcription factors that ETT can interact with in a similar auxin-sensitive manner. It is therefore likely that this new pathway is conserved in plant development. Through experiments described in this proposal, we aim to reach a mechanistic and developmental understanding of this newly discovered auxin-signalling module, which may be particularly well suited to facilitate precise switches in polarity throughout plant development.

Impact Summary

Who will benefit from this research and how? The Brassica genus includes important crop plants such as oilseed rape (B. napus). The close evolutionary relation between members of the Brassica genus and the model plant Arabidopsis provides a potential goldmine for exploiting fundamental discoveries to improve crop performance. Indeed such a model-to-crop pipeline has already been successfully achieved in the Ostergaard laboratory through the transfer of knowledge on fruit opening in Arabidopsis to address seed loss related to pod shatter in oilseed rape. The results expected from this proposal provides the first step in a similar pipe line and will point out directions for improving crop performance through regulation of auxin dynamics. In this way, the work directly addresses the BBSRC strategic priorities on Crop Science to tackle the challenge of Food Security. The agricultural industry: The industry will benefit from technology development to improve crop performance with respect to yield and sustainability. Given the wide function of auxin and demonstrated role of the transcription factor ETT in root development and leaf initiation, it is likely that the results can also be used in aspects of plant development in addition to gynoecium development to improve e.g. seedling establishment, plant architecture and nutrient uptake. These processes are not restricted to oilseed rape, and the results may therefore be transferable to other crops. Public: The public would benefit from greater predictability of yields, through greater stability in production costs, which would impact on prices in the shops. There are also obvious environmental benefits if yield could be improved through the discoveries that will come out of this proposal. Oilseed rape has emerged as the second largest oilseed crop with an annual worldwide production of 38 million tons of oil and demand is increasing. For this to be sustainable, seed yield needs to be dramatically increased through more efficient breeding programmes while at the same time minimising the amount of fertiliser input in order to protect the environment. I believe that the data obtained here has the potential to set out strategies to optimise fertility, plant architecture and nutrient uptake and thus contributing significantly towards such a goal. What will be done to ensure that they have the opportunity to benefit from this research? Publications: Results will be published in high-impact scientific journals and the breeding/farming press in a timely fashion. It will also be presented at national and international conferences and trade shows. Collaborations: The PI has strong connections to the international auxin research community. This is reflected in the access to the novel and unique resources described in Case for Support, part 2. We also have strong links to the breeding industry and Brassica crop improvement programmes. The data that we obtain will be of immediate use to these interest groups for example via the BBSRC-funded Crop Improvement and research Club (CIRC) and the Defra-funded Oilseed Rape Genetic Improvement Network (OREGIN). Both networks bring together academic researchers and breeding companies to discuss ongoing projects as well as to establish new interdisciplinary collaborations. Commercialisation: We are dedicated to promote the use of our results for crop improvement purposes. Informal contacts with industrialists, biotechnologists and related stakeholders will be made as soon as any exploitable results are generated. We have tight links with relevant industries and will present results to them either when they visit JIC, at joint meetings or when visiting the companies. Such events and opportunities include the UK Brassica Research Community annual meetings, the OREGIN meetings and the 6-monthly dissemination events for grant holders within the BBSRC CIRC initiative.

Committee	Research Committee C (Genes, development and STEM approaches to biology)
Research Topics	Plant Science, Structural Biology
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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