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Origem E Evolução Das Algas Eucarióticas E De Seus Cloroplastos Com Ênfase Nas Algas Vermelhas (Rhodophyta)

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Origem E Evolução Das Algas Eucarióticas E De Seus Cloroplastos Com Ênfase Nas Algas Vermelhas (Rhodophyta) Mariana Cabral de Oliveira Origem e evolução das algas eucarióticas e de seus cloroplastos com ênfase nas algas vermelhas (Rhodophyta) Texto apresentado ao Instituto de Biociências da Universidade de São Paulo para concurso de Livre-Docência no Departamento de Botânica São Paulo 2005 1 "Nothing in biology makes sense except in the light of evolution". Dobzhansky Para Pedro e Lucas 2 Agradecimentos Ao Departamento de Botânica e Instituto de Biociências da Universidade de São Paulo. Este trabalho não seria possível sem o apoio financeiro de diversas entidades, agradeço: à FAPESP; ao CNPq; ao DAAD (Alemanha); ao STINT (Suécia); à IFS (Suécia) e à Pró- Reitoria de Pesquisa-USP pelo apoio aos projetos de pesquisa e bolsas. Ao Eurico Cabral de Oliveira Filho pela revisão do texto e pelo apoio fundamental na minha carreira acadêmica. Este trabalho foi realizado com a colaboração de alunos e pesquisadores, co-autores dos trabalhos incluídos. Agradeço à: Alexis M. Bellorin, Carlos F. M. Menck, Daniela Milstein, Debashish Bhattacharya, Eurico C. de Oliveira, João P. Kitajima, João C. Setubal, Jonas Collén, Jonathan C. Hagopian, Kirsten M. Müller, Marcelo Reis, Marianne Pedersén, Pio Colepicolo, Robert G. Sheath e Suzanne Pi Nyvall. Agradeço o apoio e a colaboração dos alunos e pesquisadores: Alessandro M. Varani, Angela P. Tonon, Cíntia S. Coimbra, Estela M. Plastino, Flávio A. S. Berchez, Fungyi Chow Ho, Maria do Carmo Bittencourt-Oliveira, Marie-Anne Van Sluys, Mônica M. Takahashi, Mutue T. Fujii, Nair Yokoya, Orlando Nechi Jr., Sônia M. B. Pereira, Vanessa R. Falcão, e Yocie Yoneshigue. Agradeço a toda equipe do Laboratório de Algas Marinhas Edison J. de Paula (LAM) e do Laboratório de Biologia Molecular de Plantas (LBMP) pelo apoio prestado e pela amizade e companheirismo. Agradeço o apoio técnico imprescindível de Rosario Petti e Silvia R. Blanco, e do pessoal da secretaria do Departamento de Botânica: Carlos, Cezario e Norberto. Agradeço a Vanessa Sato pela ajuda com o Memorial. Agradeço a Alexis Bellorin pela figura da capa. À minha família e ao Lalo, sem os quais esse trabalho não seria possível. 3 Índice: Lista dos Anexos 5 Abreviaturas 6 Abstract 7 Resumo 9 Apresentação 11 1. As diferentes linhagens filogenéticas de algas eucarióticas 13 2. Origem e diversificação dos cloroplastos 17 2.1. Endossimbiose secundária: origem dos plastos complexos 21 2.2. Plastos secundários da linhagem vermelha 22 3. O genoma dos plastos 24 3.1. Seqüenciamento e análise do genoma do plasto de Gracilaria tenuistipitata 25 4. A linhagem filogenética das Rhodophyta 26 4.1. As subclasses Bangiophycidae e Florideophycidae 27 4.2. Filogenia das ordens de Bangiophycidae 27 4.3. Filogenia de espécies de Bangiales (Bangiophycidae) baseada no seqüenciamento do gene SSU rDNA 29 4.4. Introns do grupo I e biogeografia de Porphyra spiralis var. amplifolia 32 4.5. Filogenia de espécies de Gracilariaceae (Florideophycidae) baseada no seqüenciamento do gene SSU rDNA 36 5. Genômica 37 5.1. Seqüenciamento de ‘Expressed Sequence Tags’ (EST) de G. tenuistipitata 38 6. Perspectivas 39 6.1. Caracterização do genoma mitocondrial e banco de dados genéticos para Gracilaria tenuistipitata 39 6.2. Obtenção de transformantes estáveis de Gracilariales 40 6.3. Filogenia molecular de algas 40 6.4. Introns do grupo I e biogeografia de Porphyra spiralis var. amplifolia 41 Referências 42 4 Anexos1 Oliveira M.C. & Bhattacharya D. 2000. Phylogeny of the Bangiophycidae (Rhodophyta) and the secondary endosymbiotic origin of algal plastids. American Journal of Botany 87: 482- 492. (Anexo 1) Bhattacharya D. & Oliveira M.C. 2000. The SSU rDNA coding region of a filose amoeba contains a group I intron lacking the universally conserved G at the 3'-terminus. Journal of Eukaryotic Microbiology 47: 585-589. (Anexo 2) Oliveira M.C. & Menck C.F.M. 2001. O mundo de RNA e a origem da complexidade da vida. In Matioli S.R. (ed.), Biologia Molecular e Evolução. Holos Editora, Ribeirão Preto. pp: 15-26. (Anexo 3) Oliveira M.C. 2001. Estudios de la macro y micro biodiversidad de las algas. Secuenciamiento del DNA ribosomal (rDNA). In Alveal K. & Antezana T. (eds), Sustentabilidad de la Biodiversidad, un Problema Actual. Bases Cientifico-Técnicas, Teorizaciones Y Proyecciones. Univ. de Concepción, Concepción, Chile, 85-96. (Anexo 4) Müller K.M., Oliveira M.C., Sheath R.G. & Bhattacharya D. 2001. Ribosomal DNA phylogeny of the Bangiophycidae (Rhodophyta) and the origin of secondary plastids. American Journal of Botany 88: 1390-1400. (Anexo 5) Bellorin A.M., Oliveira M.C. & Oliveira E.C. 2002. Phylogeny and systematic of Gracilariaceae (Rhodophyta) revisited: ribosomal gene sequencing. Journal of Phycology 38: 551-563. (Anexo 6) Hagopian J.C., Nyvall P. & Oliveira M.C. 2002. Purification of plastid DNA from an enriched rhodoplast fraction of the red alga Gracilaria tenuistipitata. Plant Molecular Biology Reporter 20: 399-406. (Anexo 7) Hagopian J.C., Reis M., Kitajima J.P., Bhattacharya D. & Oliveira M.C. 2004. Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights on the evolution of rhodoplasts and their relationship to other plastids. Journal of Molecular Evolution. 59: 464-477. (Anexo 8) Bellorin A.M., Oliveira M.C. & Oliveira E.C. 2004. Gracilaria vermiculophylla: A western Pacific species of Gracilariaceae (Rhodophyta) first recorded from the eastern Pacific. Phycological Research 52: 69-79. (Anexo 9) 1 para esse trabalho foram incluídas apenas publicações selecionadas a partir de 2000, publicações anteriores estão citadas como referências 5 Milstein D. & Oliveira M.C. 2005. Molecular phylogeny of Bangiales (Rhodophyta) based on small subunit rDNA sequencing: Emphasis on Brazilian Porphyra species. Phycologia, 44: 212-221. (Anexo 10) Bellorin A.M. & Oliveira M.C. Plastid origin: a driving force for the evolution of algae. In Sharma A.K. & Sharma A. (eds.), Plant Genome, Biodiversity and Evolution, Volume 2B. Capítulo de livro aceito. (Anexo 11) Nyvall P., Collén J., Reis M.S., Pedersén M., Setubal J.C., Colepicolo P. & Oliveira M.C. 2005. Assessment of gene diversity in the red alga Gracilaria tenuistipitata (Rhodophyta) based on expressed sequences tags (EST). Manuscrito em preparação para publicação. (Anexo 12) Abreviaturas EST - ‘Expressed Sequence Tags’ ou etiquetas de seqüências expressas. Indel – inserção/deleção ITS - ‘Internal Transcribed Spacer’ ou espaçador transcrito interno. Kb - kilo base (1 Kb = 1000 nucleotídeos). mRNA - RNA mensageiro. nt - nucleotídeos. ORF - ‘Open Reading Frame’ ou quadro de leitura aberto. pb - pares de bases PCR - ‘Polymerase Chain Reaction’ ou reação em cadeia de polimerase. rbcL - gene que codifica para o a subunidade grande da RuBisCO RuBisCo - Ribulose-1,5-bifosfato carboxilase/oxigenase rRNA - RNA ribossômico. SSU rDNA - gene que codifica para o RNA da subunidade pequena do ribossomo. tRNA - RNA transportador. 6 Origin and evolution of eukaryotic algae and their chloroplasts with emphasis on red algae (Rhodophyta) Abstract Chlorophyll a is present in all organisms that release oxygen during the photosynthesis. The development of this molecule altered the earth atmosphere causing a great impact in the history of the planet, redirecting the evolution of life. The oxygenic photosynthesis was developed early in the history of life by a group of prokaryotes, the cyanobacteria. This ability was later laterally transferred to the eukaryotic realm by the acquisition of photosynthetic organelles (plastids) through the engulfment and retention of formerly free living cyanobacteria by an ancient eukaryotic cell. Such kind of cellular merging, called primary endosymbiosis, likely occurred only once. Three lineages of extant algae (including the ancestors of land plants) vertically evolved from the cells which first acquired plastids. Later on, the photosynthetic apparatus was laterally transferred to other unrelated eukaryotic lineages through independent secondary endosymbiosis, i.e., the acquisition of plastids by engulfing an eukaryote, already equipped with plastids. This gave rise to the ‘second-hand’ or secondary plastid-containing algae, a diverse assemblage including disparate organisms such as euglenoids, dinoflagellates and kelps. Thus, the history of photosynthesis acquisition by eukaryotes is extremely complex, making very difficult to briefly define algae and to discriminate them from other organisms. Current data support the view that plastid acquisition is a rather rare event and, accordingly, a single primary endosymbiosis followed by a few very ancient secondary endosymbiosis probably account for all extant plastid diversity. The Rhodophyta is one of three extant lineages which arose from the primary endosymbiosis and one of the main monophyletic groups within the eukaryotes. Traditionally the Rhodophyta has been divided in two subclasses, the paraphyletic Bangiophycidae and the monophyletic Florideophycidae. The Bangiophycidae are the ancestral pool for the more morphologically complex taxa in the Florideophycidae and from which the chromist algae chloroplasts have originated through secondary endosymbiosis. Besides their evolutionary relevance, the Rhodophyta present great economic importance, especially as human feed and phycocolloid production. Even so, the knowledge about their genome and metabolism is very restricted. DNA sequencing has significantly contributed to a better understanding of the origin and evolution of algae and their plastids, besides providing information
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