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Insights Into Lophotrochozoan Evolution and the Origin of Morphological Novelties from Brachiopod, Phoronid, and Nemertean Genomes

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Insights Into Lophotrochozoan Evolution and the Origin of Morphological Novelties from Brachiopod, Phoronid, and Nemertean Genomes Insights into lophotrochozoan evolution and the origin of morphological novelties from brachiopod, phoronid, and nemertean genomes Author Yi-Jyun Luo Degree Conferral 2017-08-14 Date Degree Doctor of Philosophy Degree Referral 38005甲第5号 Number Copyright (C) 2017 The Author Information URL http://doi.org/10.15102/1394.00000168 Okinawa Institute of Science and Technology Graduate University Thesis submitted for the degree Doctorate of Philosophy Insights into lophotrochozoan evolution and the origin of morphological novelties from brachiopod, phoronid, and nemertean genomes by Yi-Jyun Luo Supervisor: Noriyuki Satoh March, 2017 Declaration of Original and Sole Authorship I, Yi-Jyun Luo, declare that this thesis entitled “Insights into lophotrochozoan evolution and the origin of morphological novelties from brachiopod, phoronid, and nemertean genomes” and the data presented in it are original and my own work. I confirm that: • No part of this work has previously been submitted for a degree at this or any other university. • References to the work of others have been clearly acknowledged. Quotations from the work of others have been clearly indicated, and attributed to them. • In cases where others have contributed to part of this work, such contribution has been clearly acknowledged and distinguished from my own work. • None of this work has been previously published elsewhere, with the exception of the following: (*Corresponding author) Luo YJ*, Takeuchi T, Koyanagi R, Yamada L, Kanda M, Khalturina M, Fujie M, Yamasaki S, Endo K, Satoh N* (2015) The Lingula genome provides insights into brachiopod evolution and the origin of phosphate biomineralization. Nature Communications 6, 8301. Luo YJ*, Satoh N, Endo K (2015) Mitochondrial gene order variation in the brachiopod Lingula anatina and its implications for mitochondrial evolution in lophotrochozoans. Marine Genomics 24, 31-40. Signature: Date: March 23, 2017 i Insights into lophotrochozoan evolution and the origin of morphological novelties from brachiopod, phoronid, and nemertean genomes by Yi-Jyun Luo Submitted to the Graduate School in partial fulfillment of the requirements for the degree of Doctorate of Philosophy at the Okinawa Institute of Science and Technology Graduate University Abstract Brachiopods, phoronids, and nemerteans are closely related lophotrochozoans, yet they carry distinct feeding apparatuses and lifestyles. They are poorly studied despite their importance in ecology, evolution, and paleontology. As a result, the genetic basis of their evolutionary origins and body plans have been obscure. Since the Cambrian explosion ~540 million years ago, animal forms have greatly diversified. One fundamental question of animal evolution is how these diverse morphologies are formed. While animals share many developmental toolkit genes, they also possess novel genes and expansion of gene families in a lineage-specific manner. How lineage-specific genes and changes of genomic features contribute to morphological novelties is still a challenge in understanding animal evolution. Also, whether common toolkit genes are involved in patterning these novelties at the genomic level is not well understood. Here I present the genomes of the brachiopod Lingula anatina, the phoronid Phoronis australis, and the nemertean Notospermus geniculatus, together with multiple transcriptomes, providing a comparative platform to understand the evolution of animal genomes and the origin of lophotrochozoans. Using genomic, transcriptomic, and proteomic approaches, I show that although Lingula and vertebrates have superficially similar hard tissue components, Lingula lacks genes involved in bone formation, suggesting an independent origin of their phosphate biominerals. Several genes involved in Lingula shell formation are shared by molluscs. However, Lingula has independently undergone domain combinations to produce shell matrix collagens with epidermal growth factor domains and carries lineage-specific shell matrix proteins. Gene family expansion, domain shuffling, and co-option of genes appear to be the genomic background of Lingula’s unique biomineralization. Genome-based phylogenetic analyses place Nemertea sister to the group of Brachiopoda and Phoronida. Lophotrochozoans share many gene families with deuterostomes, suggesting that lophotrochozoans retain a core set of bilaterian gene repertoire rather than ecdysozoans or remaining spiralians. Comparative transcriptomics demonstrates that lophophores of brachiopods and phoronids have resemblance not only morphologically but also at the molecular level. Despite lophophores are dissimilar from head structures, lophophores highly express vertebrate head organizer and neuronal marker genes, probably indicating a common origin of bilaterian head patterning. Together, this study reveals a dual nature of lophotrochozoans in which bilaterian-conserved and lineage-specific features shape the evolution of their genomes. ii Acknowledgments I am indebted to my supervisor, Noriyuki Satoh, for providing me excellent resources, absolute freedom, and trust in my scientific ability. In retrospect, those are essential factors that allow me to pursue my graduate training in a whole new field—bioinformatics and genomics of marine invertebrates. Without his insights and his emphasis on a creative environment, I would not have learned so such along this genomic adventure. I thank my collaborator, Kazuyoshi Endo, for bringing me into the Lingula study and for teaching me sampling and artificial spawning. I also thank my collaborators, Takeshi Takeuchi and Lixy Yamada, for their help in proteomic analysis. Thanks also to the collaborators, Tadashi Akiyama, Hirotaka Sakamoto, and Tatsuya Sakamoto, for sampling phoronid and nemertean specimens. I would like to thank the technical staff, Ryo Koyanagi, Miyuki Kanda, Makiko Tanaka, Mariia Khalturina, Manabu Fujie, and Shinichi Yamasaki, for their assistance in DNA and RNA sequencing. Thanks to Kanako Hisata for preparing genome browsers. I appreciate the support and stimulating discussion from the Satoh lab members. Mainly thanks to Chuya Shinzato, Yuuri Yasuoka, Kostya Khalturina, Eiichi Shoguchi, Jun Inoue, and Tsai-Ming Lu. I thank my classmates, roommates, and labmates, Ken Baughman and Keita Ikegami, for their continued friendship as well as sharing our experiences in science and daily life as the pioneer class at OIST. During my graduate work, I am grateful to have the discussion with Dan Rokhsar, Chris Lowe, Bernie Degnan, Peter Holland, Mark Martindale, and Andy Hejnol. Thanks for their suggestions in the specific studies as well as advice in the scientific career in general. I wish to thank the administrative staff, Tomomi Teruya and Shoko Yamakawa, for their assistance in daily life and lab-related matters. I thank Steve Aird for English editing and fruitful discussion on scientific writing. Thanks to Jeff Wickens for providing constructive feedback on the first draft. iii List of Abbreviations AP anterior–posterior BBH bidirectional best hits BLAST basic local alignment search tool BMP bone morphogenetic protein BSA bovine serum albumin CHS chitin synthase DAPI 4’,6-diamidino-2-phenylindole EGF epidermal growth factor EST expressed sequence tag FACS fluorescence-activated cell sorting FGF fibroblast growth factor FPKM fragments per kilobase of transcript per million mapped reads GAG glucosaminoglycan gel GC guanine-cytosine GO gene ontology GRN gene regulatory network LRR leucine-rich repeats LSU large subunit MHD myosin-head-domain ORF open reading frame PBS phosphate-buffered saline SCPP secreted calcium-binding phosphoproteins. SMP shell matrix protein SPARC secreted proteins acidic and rich in cysteine SSU small subunit TGF transforming growth factor TIR toll/interleukin-1 receptor TLR toll-like receptor TMM trimmed mean of M-values URF unassigned open reading frame iv Table of Contents 1 Introduction ................................................................................................................................... 1 1.1 Animal phylogeny .................................................................................................................. 1 1.2 Lophotrochozoan relationships .............................................................................................. 2 1.3 Lophotrochozoan phylogeny and debates .............................................................................. 3 1.4 Marine invertebrate genomics ................................................................................................ 5 1.5 Deep homology and gene regulatory networks ...................................................................... 8 1.6 Hox genes and morphological novelties ................................................................................. 9 1.7 Morphological novelties and similarities in genomic and transcriptomic perspectives ....... 10 1.8 Biomineralization in shells and bones .................................................................................. 12 1.9 The brachiopod Lingula anatina and debates on ‘living fossil’ ........................................... 14 1.10 The phoronid Phoronis australis .......................................................................................... 15 1.11 The nemertean Notospermus geniculatus ............................................................................. 16 1.12 Concluding remarks ............................................................................................................
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