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Francisca Rodrigues Dos Reis Universidade do Minho Escola de Ciências Francisca Rodrigues dos Reis Effect of mycorrhization on Quercus suber L. tolerance to drought L. tolerance to drought cus suber Quer corrhization on y fect of m Ef Francisca Rodrigues dos Reis Governo da República Portuguesa UMinho|2018 janeiro de 2018 Universidade do Minho Escola de Ciências Francisca Rodrigues dos Reis Effect of mycorrhization on Quercus suber L. tolerance to drought Tese de Doutoramento Programa Doutoral em Biologia de Plantas Trabalho efetuado sob a orientação da Profª Doutora Teresa Lino-Neto da Profª Doutora Paula Baptista e do Prof. Doutor Rui Tavares janeiro de 2018 Acknowledgements “Em tudo obrigada!” Quando um dia me vi sentada num anfiteatro onde me descreviam a importância da criação de laços e que o sentimento de gratidão deveria estar implícito no nosso dia-a-dia, nunca pensar que seria o mote de início da minha tese de Doutoramento. Quanto mais não seja por ter sido um padre jesuíta a dizer-mo numa reunião de pais. Sim, é verdade! Para quem acompanhou toda a minha jornada sabe que não fiz um doutoramento tradicional, que não sou uma pessoa convencional e que não encaixo nas estatísticas de uma jovem investigadora! Tudo isto me foi proporcionado graças à pessoa mais humana e à orientadora mais presente que poderia ter escolhido. A Profa. Teresa foi muito mais do que uma simples orientadora. Foi quem me incentivou quando a moral andava baixa, foi a disciplinadora quando o entusiasmo era desmedido, foi a amiga nos momentos de desespero. Apanhar amostras sob neve e temperaturas negativas, acordar de madrugada sob olhar atento de veados, e lama, lama e mais lama, são algumas das recordações que vou guardar para a vida! Obrigada por me proporcionar experiências de uma vida! Ao Prof. Rui Tavares, mais do que um co-orientador, foi um lutador pelas minhas causas. Desculpe se lhe roubei anos de vida! Mas obrigada por se ter batido, tal qual um gladiador na arena administrativa desta Universidade! À Profa. Paula Baptista, uma co-orientadora como poucas, daquelas que põe os pés ao caminho e as mãos na obra. Fui sempre recebida como uma filha da casa na Escola Agrária de Bragança e tratada como sendo da família! Obrigada por toda a dedicação e incentivos constantes! À Doutora Carolina Varela e à Doutora Teresa Valdiviesso, pelo trabalho de campo memorável! Pessoas como vocês ajudam qualquer um a desenvolver um gosto único pela floresta! Ao Prof. Pedro Santos e ao Pedro Castro, por toda ajuda no indecifrável mundo da Bioinformática! Vocês tiverem um papel fundamental no andamento dos trabalhos. Ao Doutor Frank Richard e ao Doutor Marc-André Selousse pela ajuda no delineamento experimental do trabalho e, por me darem a conhecer o muito da ecologia florestal. Um agradecimento à Dra. Maria do Céu Osório e ao vigilante Carlos Barroso Dias, do Instituto da Conservação da Natureza e Floresta, por todo o auxílio nas amostragens no Gerês. Ao Eng.o Pinto Moreira e ao Dr. Rafael Rodrigues pelo apoio na amostragem da Herdade da Contenda. Aos meus colegas de laboratório… Sem dúvida aqueles que mais me aturaram, nos dias bons mas sobretudo nos menos bons! Um agradecimento especial aos que deixaram o laboratório antes da conclusão desta tese, Herlânder, Humberto, Alexandre, Nuno, Sara Freitas, Telma, Joana, Eduarda, Juliana, João e Miguel obrigada por todo o conhecimento que me transmitiram e pela partilha durante os anos que privamos. Aos meus meninos, Hugo Alves, Hugo Olival, Rita e v João, obrigada por todos os momentos que o sobreiro nos proporcionou. À Daniela e à Eunice, que apesar de pouco convívio físico no laboratório também deram o seu contributo nesta jornada. À Profa. Manuela Costa não só pelos seus comentários enriquecedores, sobretudo nas apresentações (mesmo quando já as tinha ouvido uma dúzia de vezes) mas também pelos bons momentos off research. À Sara Laranjeira pela serenidade que trouxe ao laboratório e as palavras amigas no momento certo. A todos os técnicos, Magda, Manuela, Cristina, D. Isabel, Sr. Luís e Paula, obrigada por todo o apoio invisível. Aos Bragantinos, companheiros de congressos, Fátima, Teresa, Diogo e ao Eric, obrigada pela companhia e pelos bons momentos passados nas jornadas científicas fora do laboratório. Às minhas pedras filosofais do laboratório, Rómulo e Helena. Obrigada, obrigada e mais obrigada! Só desejo que todas as pessoas possam privar com amigos como vocês. Ao Rómulo, resta-me agradecer-lhe a palavra certa no momento oportuno. A ciência precisa de pessoas extraordinárias como tu! Obrigada por não me deixares ser a única louca a ter filhos durante o PhD! À Helena, minha amiga da linha da frente da batalha. Porque o doutoramento é muito mais do que uma tese: são as pessoas que conhecemos e que nós levamos para a vida! És muito mais forte e lutadora do que pensas, uma investigadora incrível e uma amiga fantástica! Aos meus pais por me terem proporcionado atingir este nível académico e, por me terem dado uma educação exemplar. Obrigada por me terem dado a cana para pescar! Aos meus sogros, por todo o apoio com toda a logística familiar que me possibilitou abraçar este projecto do início ao fim. Aos meus amigos, por todas as gargalhadas que me fizeram dar nos momentos certos, e também nos menos certos, mas que ainda me souberam melhor! À minha família! Sim, aquela que quando começou este doutoramento estava resumida a dois elementos e que já vai em quatro. Estes anos foram a loucura total! Se fazer um doutoramento já é uma tarefa ambiciosa, fazê-lo com duas recém-nascidas pelo meio é algo surreal! Por isso, tenho muito que agradecer à pessoa que esteve ao meu lado, dia após dia, semana após semana, mês após mês, ano após ano… Toda esta jornada só fez sentido porque ele a fez comigo. Obrigada por tudo e por nada em especial! Talvez mais por me ter mantido com a sanidade mental necessária para prosseguir o caminho. O que não foi tarefa nada fácil! O nosso amor é incondicional, um amor para a vida toda! Aos maiores e melhores outputs deste doutoramento, as nossas filhas: a Margarida e a Teresa! Vocês foram e são o melhor que me aconteceu neste doutoramento! Espero que um dia, quando forem crescidas, se sintam orgulhosas de mim! Porque eu todos os dias me orgulho de ser vossa mãe! Este foi o caminho que escolhi. É preciso muita força de vontade, sim; é preciso muita determinação, sim; é preciso muito espirito de sacrifico, sim; mas sobretudo é preciso muito amor! vi This work was funded by FEDER funds through the Operational Competitiveness Program - COMPETE and by National Funds through FCT (Fundação para a Ciência e a Tecnologia) under the project FCT/COMPETE/FEDER with a project grant ref PEst- OE/BIA/UI4046/2014; UID/MULTI/04046/2013 and with the PhD grant, ref. FRH/BD/86519/2012. vii Abstract Mediterranean temperate forests have been identified as major biodiversity hotspots. These ecosystems are currently threatened by long term drought imposition, which will be further enhanced by the predicted climate changing. Cork oak (Quercus suber L.) is an evergreen species typically distributed within the Mediterranean Basin that has an important economic and social impact for the Iberian Peninsula. Q. suber forests can comprise different forest systems, ranging from forests with high tree density (400 trees/ha, sobreirais) to savannah-like landscapes with 60–100 trees/ha (montados). Although, well adapted to summer drought season, increasing of temperature and decreasing of precipitation is endangering the sustainability of cork oak forests. A key role for cork oak adaptation and tolerance to drought could be played by the microbial community, namely ectomycorrhizal fungi and bacteria. In the present PhD project, seven cork oak forests from five different geographic locations, at different landscapes and gradient of water availability, were sampled. Ectomycorrhizal (ECM) community was assessed by barcoding of root tips present in soils samples, whereas the bacterial community of the same cork oak soils samples was assessed by metabarcoding using Illumina MiSeq sequencing. ECM community was predominantly dominated by Basidiomycota whereas bacterial community was highly enriched in Proteobacteria, Actinobacteria and Acidobacteria. A core microbial community was identified as belonging to all cork oak forests, namely Tomentella for ECM community and Acidothermus, Afipia and Sphingomonas for bacterial community. Both microbiomes clustered according to three bioclimate groups, humid, sub-humid and semi-arid/arid climates, although clustering was more evident for bacterial communities. When considering individual climate variables, bacterial and ECMF communities presented an opposite behavior. While ECMF occurrence was promoted by precipitation and impaired by temperature, bacteria presented the exact opposite trend. Correlations between ECM and mycorrhiza helper bacteria (MBH) communities revealed that Russula/Bacillus and Russula/Streptomyces interaction could play a potential role for cork oak drought stress acclimation. To the best of our knowledge, this work comprises the most complete survey of cork oak microbiomes at different landscapes. A set of microbial interactions were suggested that could push forward future research on cork oak forests for preventing further drought stress consequences. Keywords: cork oak, forest soil, ectomycorrhizal community, bacterial community, symbiotic interactions; Mediterranean bioclimates ix Resumo A floresta Mediterrânica está classificada como um dos principais pontos de conservação de biodiversidade. Estes ecossistemas estão atualmente ameaçados por períodos de seca prolongada, que serão intensificados com as alterações climáticas previstas. O sobreiro (Quercus suber L.) é uma espécie arbórea, de folhagem persistente, distribuída na bacia do Mediterrâneo, que tem um importante impacto socio-económico na Península Ibérica. As florestas de Q. suber estão distribuídas em diferentes sistemas florestais que variam, desde florestas com alta densidade de árvores (400 árvores/ha, sobreirais), até paisagens tipo-savana com 60-100 árvores/ha (montados).
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