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Plant Derived Cyclic Peptides: from Discovery to Biotechnological Applications Haiou Qu Bsc, Msc

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Plant Derived Cyclic Peptides: from Discovery to Biotechnological Applications Haiou Qu Bsc, Msc Plant derived cyclic peptides: from discovery to biotechnological applications Haiou Qu BSc, MSc A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2019 Institute for Molecular Bioscience Abstract Plant-derived cysteine-rich cyclic peptides are a class of small peptides that range from 14-37 amino acids in size and are characterised by a head-to-tail cyclized backbone. Their unique cyclized and disulfide-constrained structures make them exceptionally stable molecules. Members include the six-cysteine containing cyclotides, which have been detected in species spanning five plant families, and the two-cysteine PawS-derived cyclic peptides found in sunflower. The sequences between cysteines residues are tolerant to residue substitutions in both of these examples, thus making them promising scaffolds for grafting and stabilizing bioactive epitopes. Indeed, a number of pharmaceutical protein-engineering applications based on cyclic peptides have been demonstrated in recent years. Chemical synthesis has been the dominant approach in the past for producing cysteine-rich cyclic peptides, with native chemical ligation being the most commonly used to generate the cyclic backbone. However, production using this approach can be expensive, especially upon scale-up production, and not all cyclic peptides are amenable to synthesis and correct folding. Furthermore, the large amounts of chemical reagents required for synthesis has impacts for the environment. To overcome this issue, an alternative strategy is to produce cyclic peptides in plants, as some plant species are naturally efficient at cyclic peptide production. Other advantages of developing plant-based production systems include reduced production costs, reduced chemical waste, and the possibility of developing innovative oral delivery drugs by the packaging of peptides in edible plant products. The overall goal of this thesis is to explore the potential of plant-based production of cyclic peptides. Chapter 1 provides a comprehensive background of plant-derived cysteine-rich cyclic peptides and the current synthesis approaches. The first aim was to develop rice as a production system to produce cyclic peptides (Chapter 2). Rice was selected as a candidate biofactory host as it has been proven to be efficient for the recombinant production of complex proteins, especially for those with disulfide bonds. Moreover, rice does not naturally produce cyclic peptides, which eliminates the possible interference of native cyclic peptides during separation and purification. A stable transformation platform was set up to produce cyclic peptides in rice suspension cells and seeds. Transgenes encoding prototypical cyclic peptides and engineered analogues were co-expressed with asparaginyl endopeptidases (AEPs) which are enzymes required for peptide backbone cyclization. The yields and structures of rice-derived cyclic peptides and transcript expression levels of AEPs were characterized. The second aim was to investigate the diversity and cyclization capability of cyclotide-like peptides in monocots (Chapter 3). To date, no native cyclic peptides have been identified in any monocot species, and only genes encoding linear cyclotide-like peptides have been identified. The essential residues known to be required for backbone cyclization are missing in these precursors. To investigate this further, monocot ii lineages were explored for cyclotide-like gene sequences using transcriptome analysis of monocots spanning the breadth of the taxonomic group. When expressing cyclotide-like genes in planta, a pyroGlu modification at the N-terminus was observed. Additionally, it was observed that some monocot cyclotide-like genes could be engineered with minimal residue changes to allow backbone cyclization both in vitro and in planta. These results will aid efficient cyclic peptide production in monocot cereal plants (e.g. rice, maize). The third aim was to define the plasticity of seeds for the production of diverse cyclic peptides (Chapter 4). Some cyclic peptides are naturally produced in seeds, which suggests that plant seeds may provide a beneficial environment for the production of heterologous cyclic peptides. To investigate this hypothesis, a number of cyclic peptide genes were expressed in Arabidopsis seeds. Furthermore, the cyclization efficiencies of three different sunflower AEPs were determined. To circumvent the low efficiency of co-transformation of cyclic peptide precursors and AEP genes, a homozygous AEP transgenic line exhibiting high expression was created. This stable AEP expressing line with cyclic peptide gene stacking experiments would shed light on the production of cyclic peptides in seeds. Throughout my PhD, a range of plants, tissues and cell types has been investigated for their plasticity to produce cyclic peptides. Rice suspension cells and seeds were developed to produce cyclic peptides in continuous production or stable long term storage respectively. Arabidopsis seeds were developed as a simple platform for the seed production of cyclic peptides. Furthermore, the diversity of monocot cyclotide-like genes was investigated, as well as their capability to be engineered for backbone cyclization using a transient leaf expression system. All in all, these studies provide valuable information on the selection of biofactory hosts, tissue specificity and the genetic modifications required to produce cyclic peptides efficiently in plants. iii Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, financial support and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my higher degree by research candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co-authors for any jointly authored works included in the thesis. iv Publications included in this thesis Haiou Qu, Bronwyn J. Smithies, Thomas Durek, and David J. Craik. Synthesis and protein engineering applications of cyclotides. Australian Journal of Chemistry, 2017, 70(2):152-161. Partially incorporated in Chapter 1 Contributor Statement of contribution Haiou Qu Wrote and edited paper (70%) Prepared figures (20%) Bronwyn J. Smithies Wrote and edited paper (30%) Prepared figures (40%) Thomas Durek Refined writing (50%) David J. Craik Refined writing (50%) Prepared and edited the figures (40%) Submitted manuscripts included in this thesis No manuscripts submitted for publication Other publications during candidature Research article Mark A. Jackson, Kuok Yap, Aaron G. Poth, Edward K. Gilding, Joakim E. Swedberg, Simon Poon, Haiou Qu, Thomas Durek, Karen Harris, Marilyn A. Anderson and David J. Craik, 2019. Rapid and scalable plant based production of a potent plasmin inhibitor peptide. Frontiers in plant science 10, 602. Conference abstracts Haiou Qu, Mark A. Jackson, Edward K. Gilding and David J. Craik. Developing rice as a biofactory for cyclic therapeutic peptides. EMBL Australia PhD Symposium, Nov 2016, Adelaide, Australia. Oral presentation. Haiou Qu, Mark A. Jackson, Edward K. Gilding and David J. Craik. Developing rice as a production system for cyclic therapeutic peptides. ComBio, Oct 2016, Brisbane, Australia. Poster and short talk presentation. Haiou Qu, Mark A. Jackson, Edward K. Gilding and David J. Craik. Developing rice as a production system for cyclic therapeutic peptides. 3rd Congress of the International Society for Plant Molecular Farming, June 2018, Helsinki, Finland. Poster presentation. v Haiou Qu, Edward K. Gilding, Mark A. Jackson, Kuok Yap, Olivier J. Cheneval and David J. Craik. Surveying a diverse set of monocots for cyclotides: are these cyclic peptides restricted to dicots? IMB EMCRA Mini-Symposium, Dec 2018, Brisbane, Australia. Poster presentation. Haiou Qu, Edward K. Gilding, Mark A. Jackson, Kuok Yap, Olivier J. Cheneval and David J. Craik. Surveying a diverse set of monocots for cyclotides. 4th International Conference on Circular Proteins and Peptides, Nov 2018, Kawasaki, Japan. Poster and short talk presentation. Contributions by others to the thesis Dr. Mark A. Jackson and Dr. Edward K. Gilding contributed to the research project design, discussion and editing of the
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