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Coevolution of Plastid Genomes and Transcript Processing Pathways in Photosynthetic Alveolates

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Coevolution of Plastid Genomes and Transcript Processing Pathways in Photosynthetic Alveolates Coevolution of plastid genomes and transcript processing pathways in photosynthetic alveolates !"#$%&'()*+&,*(-+&&*../(0"1,23(4+..*,* Initial submission dated 31/05/2014 Corrected submission dated 08/08/2014 This dissertation is submitted for the degree of Doctor of Philosophy Declaration This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except where specifically indicated in the text. None of the material in this dissertation has been previously submitted for any other academic qualification. Some of the material within this dissertation has previously been published, in the following papers: Barbrook AC, Dorrell RG, Burrows J, Plenderleith LJ, Nisbet RER, Howe CJ. 2012. Polyuridylylation and processing of transcripts from multiple gene minicircles in chloroplasts of the dinoflagellate Amphidinium carterae. Plant Molecular Biology 79, 347-357. Dorrell RG, Howe CJ. 2012. What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses. Journal of Cell Science 125, 1865-1875. Dorrell RG, Howe CJ. 2012. Functional remodeling of RNA processing in replacement chloroplasts by pathways retained from their predecessors. Proceedings of the National Academy of Sciences USA. 109: 18879-18884 Dorrell RG, Butterfield ER, Nisbet RER, Howe CJ. 2013. Evolution: unveiling early alveolates. Current Biology 23, 1093-1096. Dorrell RG, Drew J, Nisbet RE, Howe CJ. 2014. Evolution of chloroplast transcript processing in Plasmodium and its chromerid algal relatives. PLoS Genetics 10, e1004008. Richardson E*, Dorrell RG* (joint first authors), Howe CJ. 2014. Genome-wide transcript profiling reveals the coevolution of chloroplast gene sequences and transcript processing pathways in the fucoxanthin dinoflagellate Karlodinium veneficum. Molecular Biology and Evolution, in press. All of the material from these publications that is included in this thesis was my own work, and was written by me. This dissertation is 51903 words length, excluding preface, abstract, figure legends, bibliography and appendices. !" " Thanks Thank you to Chris, for being such a generous and patient supervisor, and to members of the Howe Group for providing a warm and intellectually supportive research environment over the last four years. Particular thanks are due to Ellen Nisbet, for providing critical feedback on a great deal of the material in this thesis; to David Lea-Smith, Joanna McKenzie, Adrian Barbrook, and Davy Kurniawan, for training me in experimental techniques used in my PhD; and to Erin Butterfield, for reminding me to view everything with perspective. Thanks also to Martin Embley and to Ross Waller for a most enlightening viva examination, which I feel has made a very positive impact on this thesis. Thank you to the BBSRC for providing financial support for my work, and the British Phycological Society, British Society for Protist Biology, International Society of !"#$%&$#'#(%&$&)*+,-*.%,(/&*0#''1(1)*0+23"%-(1*4#"*1,+3'%,(*21*$#*+$$1,-*&#21*51"6* intellectually stimulating conferences. Thank you to my students- each and every one- for having provided me with a great deal to think about, challenging me on the assumptions that I make, and reminding me on a weekly basis of why I got into this job in the first place. Particular thanks to Beth Richardson, George Hinksman, and James Drew, who worked so hard and (I think) grew so much as research students under my supervision. Thank you to my parents, Mary and Peter Dorrell, for teaching me early on and continuing to teach me today to be inquisitive, limit myself only in the capacity of my imagination, and strive to be the kind of person that I want to see in the world. Finally, thank you to Anil: my love; the most beautiful person I know inside and out; for keeping me in one piece over the months spent writing this. OK, '1$/&*(#7 !!" " Abstract Following their endosymbiotic uptake, plastids undergo profound changes to genome content and to their associated biochemistry. I have investigated how evolutionary transitions in plastid genomes may impact on biochemical pathways associated with plastid gene expression, focusing on the highly unusual plastids found in one group of eukaryotes, the alveolates. The principal photosynthetic alveolate lineage is the dinoflagellate algae. Most dinoflagellate species harbour unusual plastids derived from red algae. The genome of this plastid has been fragmented into small, plasmid-!"#$%$!$&$'()%($*&$+%,&"'"-"*-!$)./% 0*1')-*"2()%34%(5")%6$'3&$%*$-$"7$%1%89%23!:;<=%(1"!%1'+>%"'%)3&$%)2$-"$)>%?'+$*63%$@($')"7$% sequence editing. Some dinoflagellates have replaced their original plastids with others, in a 2*3-$))%($*&$+%,)$*"1!%$'+3):&A"3)")./%05$%&1B3*%'3'-photosynthetic alveolates are the apicomplexans, which include the malaria parasite Plasmodium. Apicomplexans are descended from free-living algae and possess a vestigial plastid, which originated through the same endosymbiosis as the ancestral red dinoflagellate plastid. This plastid has lost all genes involved in photosynthesis and does not possess a poly(U) tail addition pathway. I have investigated the consequences of the fragmentation of the red algal dinoflagellate plastid genome on plastid transcription. I have characterised non-coding transcripts in plastids of the dinoflagellate Amphidinium carterae, including the first evidence for antisense transcripts in an algal plastid. Antisense transcripts in dinoflagellate plastids do not receive poly(U) tails, suggesting that poly(U) tail addition may play a role in strand discrimination during transcript processing. I have additionally characterised transcript processing in dinoflagellate plastids that were acquired through serial endosymbiosis. I have shown that poly(U) tail addition and editing occur in the haptophyte-derived serial endosymbionts of the fucoxanthin-containing dinoflagellates Karenia mikimotoi and Karlodinium veneficum. This is the first evidence that plastids acquired through serial endosymbiosis may be supported by pathways retained from previous symbioses. Transcript editing constrains the phenotypic consequences of divergent mutations in fucoxanthin plastid genomes, whereas poly(U) tail addition plays a central role in recognising and processing translationally functional fucoxanthin plastid mRNAs. I have additionally shown that certain genes within fucoxanthin plastids are located on minicircles. This demonstrates convergent evolution in the organisation of the fucoxanthin and red algal dinoflagellate plastid genomes since their endosymbiotic acquisition. Finally, I have investigated transcript processing in the algae Chromera velia and Vitrella brassicaformis. These species are closely related to apicomplexans but are still !!!" " photosynthetic and apply poly(U) tails to plastid transcripts, as with dinoflagellates. I have shown that poly(U) tails in these species are preferentially associated with translationally functional mRNAs of photosynthesis genes. This is the first plastid transcript processing pathway documented to target a specific functional gene category. Poly(U) tail addition may direct transcript cleavage and allow photosynthesis gene transcripts to accumulate to high levels. The loss of this pathway from ancestors of apicomplexans may have contributed to their transition from photosynthesis to parasitism. !"# # Contents Chapter One: Thesis Introduction...................................................................................1-24 -The origins of photosynthesis in the eukaryotes.....................................................................1 -Taxonomic distribution of plastid lineages..............................................................................3 -Identifying model systems for studying plastid evolution........................................................5 -Evolutionary diversity of the alveolates...................................................................................5 -Alveolates possess highly unusual plastids............................................................................8 -Thesis aims...........................................................................................................................10 -Theme 1: Genome reduction in plastid evolution..................................................................10 -Theme 2: Post-endosymbiotic changes to plastid genome organisation..............................14 -!"#$#%&'%(#)*+,%#-./01$2*/0*0%+-.%3"#%40"/55*-6%2+67%$/.#,...........................................15 -Transcript processing in plastids...........................................................................................18 -Outline of thesis chapters......................................................................................................21 Chapter Two: Materials and Methods............................................................................25-38 Chapter Three: Processing of core-containing and antisense transcripts generated from plastid minicircles in the peridinin dinoflagellate Amphidinium carterae........39-70 -Rolling circle transcription occurs in A. carterae plastids......................................................42 -Multi-copy transcripts can receive poly(U) tails.....................................................................45 -Multi-8/51%3)+-08)*530%8+-%5/00#00%$+39)#%:;%#-.0<..............................................................46 -Short core-containing transcripts are present in dinoflagellate plastid transcript
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