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Copping with Extreme Dehydration: a Physiological, Biochemical and Molecular Study on the Aquatic Bryophyte Fontinalis Antipyretica

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Copping with Extreme Dehydration: a Physiological, Biochemical and Molecular Study on the Aquatic Bryophyte Fontinalis Antipyretica Universidade de Lisboa Faculdade de Ciências Departamento de Biologia Vegetal Copping with Extreme Dehydration: A Physiological, Biochemical and Molecular Study on the Aquatic Bryophyte Fontinalis antipyretica Ricardo Filipe Duarte da Cruz de Carvalho Doutoramento em Biologia Especialidade de Fisiologia e Bioquímica 2013 Universidade de Lisboa Faculdade de Ciências Departamento de Biologia Vegetal Copping with Extreme Dehydration: A Physiological, Biochemical and Molecular Study on the Aquatic Bryophyte Fontinalis antipyretica Ricardo Filipe Duarte da Cruz de Carvalho Tese orientada pela Professora Doutora Cristina Branquinho e pelo Professor Doutor Jorge Marques da Silva, especialmente elaborada para a obtenção do grau de doutor em Biologia (Fisiologia e Bioquímica). 2013 Part of the experimental work leading to this dissertation was performed in collaboration with UNIVERSITAT DE VALÈNCIA Departamento de Biología Vegetal València, Spain Under the supervision of Professor Eva Barreno UNIVERSIDAD REY JUAN CARLOS Madrid, Spain Under the supervision of Professor Myriam Catalá INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA Oeiras, Portugal Under the supervision of Professor Ana Varela Coelho This Doctor of Philosophy Dissertation was supported by Fundação para a Ciência e a Tecnologia (Scientific Doctoral Grant no. SFRH/BD/31424/2006). In addition to the supervision of Professor Cristina Branquinho and Professor Jorge Marques da Silva, part of the results in this Dissertation also involved the collaboration with other Researchers. Para os devidos efeitos no n.º 2 do Art. 8º do Decreto-Lei 388/70, o autor da Dissertação declara que participou na execução do trabalho experimental descrito, bem como na análise e interpretação dos resultados e na redacção dos textos e manuscritos submetidos para publicação. Ricardo Filipe Duarte da Cruz de Carvalho Novembro 2013 Publications – Chapter 2 – Planta (2011) 234, 195–205 (http://www.springerlink.com/content/u4l6m30m250t2571/) – Chapter 3 – Annals of Botany (2012) 110, 1007–1016 (http://aob.oxfordjournals.org/content/110/5/1007) Submissions – Chapter 6 – Submitted and under review in Plant, Cell and Environment Conferences – Cruz RD, Branquinho C, Marques da Silva J, 2007. Oxygen evolution and chlorophyll fluorescence under extreme desiccation in the aquatic bryophyte Fontinalis antipyretica. In: 14th International Congress on Photosynthesis, Society for Experimental Biology (SEB), Glasgow, Scotland – Poster Presentation; and In: Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis, Chapter 7 (2008), Allen JF, Gantt E, Golbeck JH, Osmond B (eds). Springer, Berlin, Germany, pp 1425–1430. – Cruz RD, Branquinho C, Marques da Silva J, 2007. Stress indicators in the aquatic bryophyte Fontinalis antipyretica under different levels of desiccation. In: XVI Simposio Botánica Criptogámica, León, Spain – Poster Presentation. – Cruz de Carvalho R, Branquinho C, Marques da Silva J, 2008. Respiratory burst and hydrogen peroxide production upon rehydration in Fontinalis antipyretica. In: SEB Annual Main Meeting, Marseille, France – Poster Presentation. – Cruz de Carvalho R, Branquinho C, Marques da Silva J, 2008. Desiccation caused respiratory burst upon rehydration in Fontinalis antipyretica. In: The 6th IAL Symposium and ABLS, Asilomar, USA – Poster Presentation. – Cruz de Carvalho R, Catalá M, Barreno E, Branquinho C, Marques da Silva J, 2009. Desiccation in the aquatic bryophyte Fontinalis antipyretica. In: XVII Simpósio Botânica Criptogâmica, Tomar, Portugal – Oral Presentation. – Cruz de Carvalho R, Silva AB, Branquinho C, Marques da Silva J, 2010. Sucrose content increases only during fast desiccation in an aquatic bryophyte. In: 4th International Symposium on “Signals, Sensing and Plant Primary Metabolism”, Humboldt-Universität zu Berlin, Potsdam, Germany – Poster Presentation. – Cruz de Carvalho R, Soares R, Silva AB, Almeida A, Coelho AV, Marques da Silva J, Branquinho C, 2013. Desiccation tolerance induced during slow drying of Fontinalis antipyretica: a differential proteomic evaluation. In: XIII Congresso Luso-Espanhol de Fisiologia Vegetal, Lisbon, Portugal – Poster Presentation. Acknowledgements / Agradecimentos Acknowledgements / Agradecimentos I am very grateful to Fundação para a Ciência e a Tecnologia (Portugal) for the financial support (Scientific Doctoral Grant no. SFRH/BD/31424/2006), to Faculdade de Ciências da Universidade de Lisboa (FCUL) (Portugal), to Universitat de València (Spain) and Instituto de Tecnologia Química e Biológica (ITQB) (Portugal) for receiving me and providing the conditions to develop the work here presented. Professora Cristina Branquinho pela sugestão do tema deste trabalho, pela orientação e supervisão do trabalho. Por nunca ter deixado de acreditar em mim. Agradeço-lhe a amizade, o carinho e todas as lições de vida. Por me lembrar para apontar sempre para o céu: “O céu é o limite!” Professor Jorge Marques da Silva pela orientação e supervisão do trabalho, pela liberdade que sempre me deu para enveredar por novos caminhos mas por ter sempre a frontalidade e disponibilidade para discutir todos os aspetos do trabalho. Pela amizade e imensa paciência que tem tido para comigo ao longo de todos estes anos. Professor Eva Barreno for receiving me at Universitat de València. For all the friendship, guidance and support and for making me part of the Spanish family. Professor Myriam Catalá for receiving me at Universidad Rey Juan Carlos. Thank you for all the friendship, support and help throughout my Spanish adventure. A todos os que me receberam de braços abertos no ITQB. À Dra. Ana Varela Coelho, ao Dr. André Almeida e à Dra. Renata Soares por toda ajuda que me ofereceram na pesquisa proteómica dos meus musgos. Todos os Professores do Departamento de Biologia Vegetal da FCUL, em particular os de Fisiologia Vegetal. Professora Anabela Bernardes da Silva, por toda a amizade e carinho ao longo destes anos, por me ter dado sempre uma palavra de ânimo nos momentos mais críticos. Professor João Arrabaça pela amizade e constante estímulo à investigação e sempre me lembrar de ser um “jovem cientista”. Professora Ana Rita Matos por partilharmos as aulas de Fisiologia Vegetal e as histórias das aventuras das nossas crianças. À Professora Otília Correia e Professora Cristina Máguas por me receberem de braços abertos nos laboratórios de Ecologia. Professora Lia Ascensão pela ajuda na Microscopia e sugestões sobre os “musguitos”. Acknowledgements / Agradecimentos Maria Manuela Lucas, Manelita, a minha “mãe” da faculdade, por estar sempre pronta a ajudar e principalmente a escutar. Obrigado por tornares sempre o impossível, possível! A todos os amigos que partilharam comigo todo este longo percurso na FCUL. Aos meus fisiólogos! A Ana Sofia Soares, embora tenhas seguido outro rumo a tua amizade sempre me acompanha. A Ana Elizabete por toda a amizade e inspiração. À Cátia Nunes por ter sempre um sorriso. Ao André “Kokas” pela boa disposição e tornar o laboratório num lugar menos cinzento. À Cláudia “escalamocada”, obrigado por todos os cafés e conversas que partilhámos. Ao André Alcântara e à Susana por toda a boa disposição e por tratarem dos meus musgos sempre que precisei. Aos meus ecólogos! Por me terem recebido tão bem, de um modo especial à Rute, Sofia, Pedro, Sónia, Lena, Silvana, Andreia! Obrigado por me ajudarem a ver o mundo noutra perspetiva! Um especial agradecimento à Leena Luis pelas palavras de encorajamento ao longo da escrita da Dissertação e pela revisão final do manuscrito. To my good friends in València! To Paco Gasulla who helped me settle and introduce me to everyone. To Guillermo, Fernando, Carol and Santi, who welcomed me so well in the lab and made my stay so wonderful. I will take you always in my heart! To Sonia Priego for all the long hours in front of the Confocal Microscope and for being so patient with me. A toda a minha família por todo o apoio e compreensão ao longo de todos estes anos. Pai, mãe, tudo o que fizeram por mim não consigo colocar em palavras! À minha mana por ter sempre palavras bem-dispostas que me aliviam o stresse. Aos meus avós e tio que sempre me perguntavam com carinho como ia a escola… Aos meus sogros por todo o apoio especialmente quando os pequenos estavam doentes e precisava escrever… À minha esposa Leonor… Obrigado por me amares e por todo o apoio em todos os momentos, mesmo naqueles mais difíceis… Aos meus filhos Maria Inês e Santiago por sempre me lembrarem o que é importante… À minha família da fé, a minha comunidade, a toda a oração que sempre me acompanhou… OBRIGADO! . “I am the resurrection. Anyone who believes in me, even though that person dies, will live, and whoever lives and believes in me will never die.” John 11, 25-26 Table of Contents Table of Contents Page Abstract 1 Sumário 5 Chapter 1 - Introduction 9 1.1. Desiccation tolerance 11 1.2. Physiological, biochemical and molecular responses to desiccation 14 1.2.1. The drying process 14 1.2.2. Recovery upon rehydration 16 1.2.3. Constitutive and induced desiccation tolerance 18 1.3. Studying desiccation tolerance 19 1.3.1. Primary metabolism: photosynthesis and respiration 19 1.3.2. Oxidative stress 19 1.3.3. Membrane leakage 20 1.3.4. Water content and dehydration rates 21 1.3.5. Differential proteomics 22 1.4. The aquatic bryophyte Fontinalis antipyretica 22 1.5. Aims and Outline of the Thesis 23 1.6. References 25 Chapter 2. Physiological consequences of desiccation in Fontinalis antipyretica 35 2.1. Abstract 37 2.2. Introduction 38 2.3. Material and Methods 40 2.3.1. Plant material and culture conditions 40 2.3.2. Dehydration and recovery treatments 41 2.3.3. Gross photosynthesis and chlorophyll a fluorescence analysis 41 2.3.4. Statistical analysis 42 2.4. Results 42 2.4.1. Relative water content and relative water loss 42 2.4.2. Effects of desiccation on the recovery of gross photosynthesis and 43 chlorophyll a fluorescence 2.4.2.1. Short-term recovery 43 2.4.2.2. Long-term recovery 47 2.5. Discussion 49 2.5.1. Fontinalis antipyretica shows partial desiccation tolerance 49 . Table of Contents 2.5.2.
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