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PHOTONET-C4 Report Summary

Project ID: 637765
Funded under: H2020-EU.1.1.

Periodic Reporting for period 1 - PHOTONET-C4 (Characterising the Gene Regulatory Networks Governing Photosynthesis: From Basic Understanding to Targeted Engineering)

Reporting period: 2015-11-01 to 2017-04-30

Summary of the context and overall objectives of the project

Photosynthesis is the primary energy source for life on earth. While the biochemistry and cell biology of photosynthesis are well understood, little is known of how the genes that mediate photosynthesis are regulated. Our research aims to address this knowledge gap by identifying the molecular regulators and mechanisms that control the expression of photosynthesis genes in the world’s most important food crops, the grasses. This work combines comparative genomics, evolutionary biology, high-throughput assays and genetic engineering.


Understanding and manipulating the gene regulatory network governing photosynthesis is one way in which engineer food and fuel crops for increased productivity. This may help contribute to future food security through enhanced sustainable agricultural production.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

The following is a list of the major results that have been achieved so far. The publications describing the result are listed after the result.

We have developed a novel computational method to identify missing genes in genome assemblies. This has allowed us to identify several transcription factor genes that were previously un-annotated in multiple grass genomes. (This is the completion of WP 1.1)
Dunne, M.P., Kelly, S. (2017) OrthoFiller: utilising data from multiple species to improve the completeness of genome annotations. BMC genomics 18:390.

We have mapped the evolution of all plant transcription factor gene families to enable cross-species identification of orthologous transcription factor genes.
Catarino, B., Hetherington, A.J., Emms, D.M., Kelly, S. Dolan, L. (2016) The stepwise increase in the number of transcription factor families in the Precambrian predated the diversification of plants on land. Molecular Biology and Evolution 33 (11): 2815-2819.

We have identified key transcription factor and transporter gene families that have been recruited to facilitate the partitioning of photosynthesis between two cell types in C4 species
Emms, D.M., Covshoff, S., Hibberd, J.M., and Kelly, S. (2016) Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species. Molecular Biology and Evolution 33 (7): 1796-1806.

We have developed a novel computational method that allows us to improve our transcriptome assemblies and thus improve our analysis of transcription factor gene families in grass species lacking reference genomes
Smith Unna, R., Boursnell, C.R., Patro, R., Hibberd, J.M., and Kelly, S. (2016) TransRate: reference free quality assessment of de novo transcriptome assemblies. Genome Research 26: 1134-1144.

We have identified the key developmental stage in the rice leaf development where photosynthesis becomes active and used this to inform our computational models of photosynthesis gene expression regulation
van Campen, J., Yaapar, M.N., Narawatthana, S., Lehmeier, C., Wanchana, S., Thakur, V., Chater, C., Kelly, S., Rolfe, S.A., Quick, W.P., Fleming, A.J. (2016) Combined Chlorophyll Fluorescence and Transcriptomic Analysis Identifies the P3/P4 Transition as a Key stage in Rice Leaf Photosynthetic Development. Plant Physiology 170 (3): 1655-1674.

We have identified differences in gene expression of plants doing C3 and C4 photosynthesis in a paddy field to provide insight into the gene expression differences that C4 photosynthesis might induce in a rice crop
Covshoff, S., Szecowka, M., Hughes, T.E., Smith-Unna, R., Kelly, S., Bailey, K.J., Sage, T.L., Pachebat, J.A., Leegood, R.C., Hibberd, J.M. (2016) C4 photosynthesis in the rice paddy: insights from the noxious weed Echinochloa glabrescens. Plant Physiology 170 (1): 57-73.

We have developed mathematical models to understand the role of transcription factors in promoting higher genome organisation
Brackley, C.A., Johnson, J., Kelly, S., Cook, P.R., Marenduzzo, D. (2016) Simulated binding of transcription factors to active and inactive regions folds human chromosomes into loops, rosettes and topological domains. Nucleic Acids Research 44 (8): 3503-3512.

We have developed mathematical models to understand how changes in metabolism impact on the evolution of gene and genome sequences
Seward, E.A., and Kelly, S. (2016) Dietary nitrogen alters codon bias and genome composition in parasitic microorganisms. Genome Biology. 17: 226.

We have used our bioinformatic technology to identify new transcription factors and transporters important for fundamental plant processes.
Honkanen, S., Jones, V.A.S., Morieri, G., Champion, C., Hetherington, A.J., Kelly, S., Proust, H., Saint-Marcoux, D., Prescott, H., Dolan, L. (2016) The Mechanism Forming the Cell Surface of Tip-Growing Rooting Cells Is Conserved among Land Plants. Current Biology 26 (23):3238-3244.
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Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

We have delivered beyond the state of the art in multiple ways. For example our work on identifying missing genes in gene families has been generalized and released as a generic method for improving the genome annotation of any species.
Dunne, M.P., Kelly, S. (2017) OrthoFiller: utilising data from multiple species to improve the completeness of genome annotations. BMC genomics 18:390.

We have adapted our transcriptome analysis method to provide a general method that can be usses to assess any transcriptome.
Smith Unna, R., Boursnell, C.R., Patro, R., Hibberd, J.M., and Kelly, S. (2016) TransRate: reference free quality assessment of de novo transcriptome assemblies. Genome Research 26: 1134-1144.

Our search for transcription factors has lead to the unanticipated discovery of families of transporters that are potentially important for C4 photosynthetic function
Emms, D.M., Covshoff, S., Hibberd, J.M., and Kelly, S. (2016) Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species. Molecular Biology and Evolution 33 (7): 1796-1806.

To further help go beyond the state of the art, we have authored two reviews that place our research program in the broader context of transcriptional control of photosynthesis and plant metabolic engineering. The first review provides a global overview of the successes and challenges in metabolic engineering in plants. This review pays particular attention to the successes that have been obtained from engineering expression of transcription factors to modulate biological production.
O’Neill, E., and Kelly, S. (2016) Engineering biosynthesis of high value compounds in photosynthetic organisms. Critical Reviews in Biotechnology 4: 1-24.
The second review places our understanding of the transcriptional regulation of photosynthesis in Arabidopsis thaliana in an evolutionary context, to provide new insight into transcriptional regulatory networks that control photosynthesis gene expression in grasses. This review reveals the striking differences between the grass and Arabidopsis networks and identifies avenues that may be exploited for engineering photosynthesis in the future.
Wang, P., Hendron, R.W., Kelly, S. (2017) Transcriptional control of photosynthetic capacity: Conservation and divergence from Arabidopsis to rice. New Phytologist (in press)
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