Dynamics and evolution of a halogenated auxin - a seed-derived signal for pea pod growth

In the history of life on Earth, the evolution of flowering plants (angiosperms) is arguably one of the most impactful events that has shaped the world of today. More than 95% of extant plants belong to the angiosperm phylum and domesticated flowering plants are essential sources of protein and energy in food consumed by humans. A major reason for the success of angiosperms is the formation of carpels in the centre of the flowers that develop as fruits after pollination harbouring the seeds for the next generation. The proposed research capitalises on recent advances into the dynamics and evolution of a novel hormone variant and its role in inter-generational signalling.
Pea (Pisum sativum) is a crop plant species with an extensive history in genetics research, and a useful model for legume crops in general. In contrast to the model plant Arabidopsis thaliana, which produces bicarpellate (two-chambered) fruit with many small seeds, pea produces monocarpellate (single-chambered) fruit (or pods) with comparatively larger but fewer seeds. Deciphering the seed/pod molecular conversation that regulates pea reproductive development may therefore lead to the discovery of alternative signalling systems. Moreover, given the important role of legume crops in the provision of plant-based protein and in achieving low-input agriculture, the improvement of legume crops has wide environmental and health implications.
Auxin is a versatile hormone functioning in practically all aspects of plant development, including fruit formation. Pea (along with other species in the Fabeae and Trifolieae (F/T) tribes of the legume family) produces a chlorinated variant of auxin, 4-Cl-IAA, which is enriched in fruit and seed. Deseeding a young pea pod leads to little or no further growth of the pod and application of exogenous IAA has no effect on this. In contrast, exogenously applied 4-Cl-IAA promotes growth leading to full elongation of the deseeded pods. 4-Cl-IAA may therefore fulfil the role that fertilised ovules/seeds ordinarily play in stimulating fruit growth by providing a mobile seed-to-pod signal to communicate that fertilisation has taken place. In this proposal, we will elucidate synthesis, signalling and evolution of this auxin variant revealing the formation of a novel signalling pathway. Given the significant strategic potential of the proposed work, the impact objectives aim to exploit the obtained knowledge to advance legume agronomy and explore potential for drug development in the medical industry.
With a focus on the molecular mechanism of signal diversification, the proposal will investigate the impact of 4-Cl-IAA biosynthesis and signalling on reproductive organ growth in the F/T tribes of the legume family. Over and above the fundamental understanding of how modification of an existing hormone can generate a novel signal for growth, results from this project have immediate potential to impact disciplines as far apart as crop improvement and drug discovery.

Auxin (3-indoleacetic acid or IAA) affects a wide variety of biological processes controlling plant growth and development. A subclade within the legume family, including Pisum sativum (pea) produces a chlorinated variant of auxin, 4-Cl-IAA, which is predominantly found in young seeds and able to stimulate pea pod growth after fertilisation. In this context, 4-Cl-IAA has been suggested as an inter-generation messenger providing a seed-derived signal perceived by maternally-derived tissue.
The aim of this proposal is to decipher the molecular mechanism by which, 4-Cl-IAA, controls pod growth from synthesis to signalling and reveal the origin of this novel plant signalling mechanism.
Using pea as a model system, we will identify the enzyme responsible for chlorination of position 4 of the indole ring - a unique activity not before identified in nature - and study its requirement for reproduction in pea. Since a substantial proportion of drugs and agrichemicals are halogenated to promote their function, this work may also provide a valuable halogenation tool in both drug discovery and agriculture. Moreover, by understanding the molecular signalling mechanism we will discover the key components that allow 4-Cl-IAA to be distinguished from that of regular auxin and characterise the specific 4-Cl-IAA response machinery. Finally, in a cross-genus transcriptomic effort, we will elucidate the dynamic changes in target gene expression that led to the evolution of 4-Cl-IAA-mediated signalling.
Given the significant strategic potential of the proposed work, the impact objectives aim to exploit the obtained knowledge to advance legume agronomy and explore potential for drug development in the medical industry. To this end, we will both alert stakeholders to the huge potential of the resources we have available to improve legume crop performance and initiate collaborations with the drug industry to explore the potential for 4-Trp halogenation in drug discovery.