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Conservation and Function of COOLAIR Long Non-Coding Rnas in Brassica Flowering Time Control

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Conservation and Function of COOLAIR Long Non-Coding Rnas in Brassica Flowering Time Control Conservation and function of COOLAIR long non-coding RNAs in Brassica flowering time control Emily Jane Hawkes Thesis submitted for the degree of Doctor of Philosophy University of East Anglia John Innes Centre September 2017 © This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived there from must be in accordance with UK Copyright Law. In addition, any quotation or extract must include full attribution. This page is intentionally left blank. 2 Abstract Since their discovery long non-coding RNAs (lncRNAs) have in turn been described as essential genomic regulators or as transcriptional noise. Examples of lncRNAs with experimentally-validated function are limited, with poor nucleotide sequence conservation calling apparent functionality into question. COOLAIR lncRNAs are transcribed in the antisense direction at the Arabidopsis thaliana floral repressor gene, Flowering Locus C (FLC). Previous work has revealed a role for COOLAIR antisense RNAs in regulation of the FLC protein-coding sense transcript and, consequently, flowering time. FLC homologues are wide-spread in flowering plants, but nucleotide sequence conservation of COOLAIR-specific regions is low. COOLAIR has a complex secondary structure, and covariant base-pair mutations predict strong conservation of this secondary structure across flowering plants. Syntenic transcription of COOLAIR was confirmed in vivo for several species within the family Brassicaceae, including three commercially important Brassica crops: B. rapa, B. oleracea and B. napus. COOLAIR transcription was detected from at least three of four ancient FLC clades within the latter three polyploid and paleopolyploid species. Each FLC homologue has distinct nucleotide sequence, expression patterns, and COOLAIR isoforms. Further variation in COOLAIR was identified between winter and spring cultivars. It was hypothesised that this could affect cis-regulation of FLC. Correlation between COOLAIR modifications and flowering time was tested by introducing antisense splice site mutations into Brassica FLC transgenes in A. thaliana. These experiments suggested that a shorter COOLAIR isoform with a disrupted structural motif was a weaker negative regulator of FLC. This work supports conservation of COOLAIR expression, structure and function in Brassica crop plants, and a role for RNA structure in COOLAIR function. We propose an evolutionarily conserved lncRNA that is neither essential regulator nor transcriptional noise, but rather adapts with the environment to fine-tune the transition to flowering. 3 Acknowledgements First and foremost, I would like to thank my supervisors, Judith Irwin and Caroline Dean, for their support and guidance over the last four years. Thank you not only for helping to develop and progress this project, but for your encouragement and enthusiasm throughout. I acknowledge the BBSRC and my iCASE partner, Bayer CropScience, for funding this work. Thank you to my iCASE supervisors, Chikako Shindo, Pieter Ouwerkerk and Mark Davey, for your guidance and scientific support. Further, thank you to the above and to the Genetics team for making me feel so welcome during my visits to the Gent site in Belgium, and to Freya Lammertyn for technical assistance during my first placement. I acknowledge our collaborators at Los Alamos National Laboratory, New Mexico, U.S.A. Thank you to Karissa Sanbonmatsu, Scott Hennelly, Irina Novikova and team for introducing me to the chemical-probing of RNA secondary structures, for solving the in vitro COOLAIR secondary structures, and for working with us to produce a paper in this field. Thank you, Karissa, for many fascinating discussions on secondary structure and for explaining your methods of secondary structure prediction and covariation analysis. I thank members of the Dean lab, past and present, who have provided technical assistance, project advice and many useful discussions. Thank you especially to Qianwen Sun for your supervision at the beginning of this project and to Zhe Wu for technical assistance with 3’RACE. I would further like to thank Rebecca Bloomer, Julia Qüesta and Peijin Li for useful discussions on COOLAIR secondary structure and splicing. Thank you all for being a supportive, inspiring and fun group to be a part of. I thank all members of the ‘Brassica group’ (Irwin, Morris and Penfield labs, Martin Trick and Rachel Wells) who have provided scientific and technical advice, useful discussions [and cake]. Thank you to Rachel Wells for sharing Brassica plant materials, and to Chantelle Burrowes for all your hard work threshing Arabidopsis seeds. Thank you to William Hawkes for assisting with the collection of flowering time data, bagging, and harvesting plants, and for many hours spent threshing seeds, and to Sibyl Batey for giving up your time to help me bag hundreds of plants the day before Christmas Eve 2016. 4 Most of all, I would like to thank Eleri Tudor, fellow PhD student and friend. Thank you for your support and advice, for sharing plant materials and methods (and photos of Reggie!), for discussions about FLC in Brassica, and for always being there for a chat. A special commendation to the support services at the NBI; they have been invaluable during my time here. Thank you to Lionel Perkins and the rest of the Horticultural Services team, who have done a fantastic and diligent job looking after my plants. I would also like to thank the security staff who go above and beyond their duty to make late-night workers feel safe and less alone. I would like to acknowledge those who have commented on and proofread drafts of this thesis submission. First and foremost, thank you to Judith Irwin for your feedback and comments. Also, thank you to Caroline Dean, Jonathan Cocker and Jeanette Hawkes for your comments and/or proofreading. Finally, thank you to my family and friends for their love and support over the last four years. Thank you to Jon for being my closest friend and for lifting my spirit. Thank you to my mum, dad, Becki, Will and Annie, without whom I could not be; to my grandads, who were there at the beginning; and to Mystique and Bilbo, for being entirely yourselves. Thank you to each of my friends for making life fun and to Sibyl, Dash and Mabon, who can make even a PhD fun. Lastly, thank you to Grey Cat, Sammy and Eeyore, without whom I would not have got this far. 5 Contents Abstract .............................................................................................................................................................. 3 Acknowledgements ............................................................................................................................................ 4 Contents ............................................................................................................................................................. 6 Illustrative material ............................................................................................................................................ 8 Abbreviations ................................................................................................................................................... 10 1 Introduction ............................................................................................................................................. 11 1.1 Overview ........................................................................................................................................ 11 1.2 The role of FLC in flowering time control ..................................................................................... 13 1.2.1 Flowering and vernalization ................................................................................................... 13 1.2.2 Key genes in flowering time control ...................................................................................... 14 1.2.3 FLC is an important floral repressor ...................................................................................... 16 1.2.4 FRIGIDA upregulates FLC .................................................................................................... 17 1.2.5 The autonomous pathway downregulates FLC ...................................................................... 18 1.2.6 The vernalization pathway epigenetically silences FLC ........................................................ 21 1.2.7 Natural variation in Arabidopsis flowering times .................................................................. 27 1.3 Mechanisms for COOLAIR regulation of FLC ............................................................................... 29 1.3.1 Long non-coding RNAs ......................................................................................................... 29 1.3.2 FLC sense and antisense transcripts are transcribed from the same locus ............................. 29 1.3.3 Antisense regulation through the RNAi pathway................................................................... 30 1.3.4 Antisense regulation through transcriptional interference ..................................................... 31 1.3.5 Sense and antisense in a self-regulatory circuit...................................................................... 31 1.3.6 Antisense regulation through protein recruitment .................................................................. 33 1.3.7 COOLAIR is regulated
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