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FLOWER ABSCISSION and FRUIT SET on TABLE GRAPES (Vitis Vinifera L.): UNRAVELING PHYSIOLOGICAL and MOLECULAR MECHANISMS

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FLOWER ABSCISSION and FRUIT SET on TABLE GRAPES (Vitis Vinifera L.): UNRAVELING PHYSIOLOGICAL and MOLECULAR MECHANISMS FLOWER ABSCISSION AND FRUIT SET ON TABLE GRAPES (Vitis vinifera L.): UNRAVELING PHYSIOLOGICAL AND MOLECULAR MECHANISMS SARA NOBRE GONÇALVES DOMINGOS ORIENTADORA: Doutora Cristina Maria Moniz Simões Oliveira COORIENTADOR: Doutor Luís Filipe Sanches Goulão TESE APRESENTADA PARA OBTENÇÃO DO GRAU DE DOUTOR EM ENGENHARIA AGRONÓMICA Presidente: Doutora Maria Helena Mendes da Costa Ferreira Correia de Oliveira, Professora Associada do Instituto Superior de Agronomia, Universidade de Lisboa. Vogais: Doutor Hernâni Varanda Gerós, Professor Associado com Agregação da Escola de Ciências da Universidade do Minho; Doutora Sara Barros Queiroz Amâncio, Professora Associada com Agregação do Instituto Superior de Agronomia da Universidade de Lisboa; Doutora Cristina Maria Moniz Simões de Oliveira, Professora Associada com Agregação do Instituto Superior de Agronomia da Universidade de Lisboa; Doutor João Manuel Mota Barroso, Professor Associado da Escola de Ciências e Tecnologia da Universidade de Évora; Doutora Ana Margarida da Costa Macedo Fortes, Investigadora Auxiliar da Faculdade de Ciências da Universidade de Lisboa. Fundação para a Ciência e Tecnologia 2016 Agradecimentos Este espaço é dedicado às inúmeras contribuições que permitiram a realização deste trabalho, a todos um muito obrigado com o mais profundo reconhecimento. Aos meus orientadores Professora Cristina Oliveira e Doutor Luís Goulão, pela oportunidade que me deram para a realização do doutoramento, pelo apoio e orientação do trabalho ao longo destes anos, pela amizade, por me inspirarem e desafiarem a fazer sempre melhor. Ao Doutor Pietro Scafidi e ao Professor Rosario Di Lorenzo, da Universidade de Palermo, pelas ideias que contribuíram para melhorar este trabalho, pelo convite para realizar parte dele na Sicíla, pelo apoio e carinho com que me receberam. A toda a equipa da Herdade Vale da Rosa, especialmente ao Doutor António Silvestre, pelo apoio a este projecto, pela disponibilidade e amizade que tiveram para comigo ao longo destes anos. À Joana Fino e ao Professor Octávio Paulo, da Faculdade de Ciências, pelas análises bioinformáticas indispensáveis para a realização do trabalho e pelo apoio e sugestões que permitiram melhorá-lo. Aos Doutores José Cochico e Eduardo Leitão, do IICT, pelo apoio nos procedimentos e determinações fisiológicas e bioquímicas, bem como pela leitura e crítica de partes do trabalho. Às Doutoras Cláudia Sanchez e Carmen Serrano, do INIAV, e Doutor Robert Larcher, da Fondazione Edmund Mach em Itália, pelo apoio nas determinações bioquímicas. A todos os colegas, principalmente Vânia Cardoso, Hugo Nóbrega, Isabela Soares, Ana Raposo e Carlos Correira pela ajuda preciosa nos ensaios e determinações, pela amizade, pelas sugestões e pelo espírito de equipa ao longo de todo o trabalho. À minha família, especialmente à minha mãe, ao meu pai, ao Jorge, à minha irmã e aos meus avós, a quem devo o que sou hoje, por todo o amor e apoio incondicional, pela constante ajuda e incentivo ao longo do todo o percurso académico. Ao Vasco, pela ajuda e o amor dedicados, por estar ao meu lado todos dias, por me transmitir calma e fazer rir nos momentos de maior nervosismo. A realização de todo este trabalho só foi possível através do financiamento da bolsa individual de doutoramento (SFRH/BD/69076/2010) e do projecto VitiShade: PTDC/AGR- GPL/116923/2010 pela Fundação para a Ciência e Tecnologia, e do projecto ProDeR Medida 4.1 - Cooperação para a Inovação: PROdUVA 23921/2/3/4. i Abstract Despite the importance of grapevine (Vitis vinifera L.) as one of the most cultivated species, the molecular events occurring during the critical period of fruit set, are far from elucidated. Aiming at providing a new insight on flower-to-fruit transition and flower abscission regulation, transcriptomic (RNA-Seq) and metabolomic analyzes were performed in the inflorescences and vine physiological alterations were investigated. Regarding flower-to-fruit transition regulation the results showed involvement of nutrient transport regulation and alterations on carbohydrates, secondary and hormone metabolism. In particular, induction of indole-3-acetic acid accumulation and activation of ethylene and sugar signaling were hypothesized to induce bioactive gibberellins biosynthesis, stimulating cell division within inflorescences. Assays with gibberellic acid (GAc) spraying and reduction of light interception during bloom allowed to promote flower abscission and suggested that growth regulator application and C-starvation resulted in distinct effects on inflorescence metabolism. GAc response involved stimulation of photosynthetic and respiratory machinery, nucleotide biosynthesis and carbon metabolism. Conversely, shading repressed photosynthesis, induced carbon/nitrogen imbalance and comprehensive alterations on hormone-related pathways, resulting in repression of cell division and induction of senescence. Candidates as common pathways leading to abscission were putrescine catabolism regulation, auxin biosynthesis induction, gibberellin biosynthesis repression and ROS signaling/detoxification although often through changes on specific transcripts and metabolites levels. Aiming at optimizing thinning methods, mandatory on table grapes production for guarantee bunch quality, GAc spray and shading during bloom were tested in seedless and seeded cultivars growing under field and greenhouse conditions. 'Thompson Seedless' showed to be sensitive to both thinning methods resulting in increased flower drop and reduced bunch compactness, but only GAc spray enhanced berry quality. Both treatments induced flower abscission in 'Black Magic' growing in late cycle on greenhouse production system, whereas during early cycle, only shade enhanced flower drop, bunch aspect and berry quality, resulting in an effective thinning method. Key-words: abscission, fruit set, grapevine, gibberellic acid, shade ii Resumo Apesar da importância da videira (Vitis vinifera L.) como umas uma das espécies mais cultivadas, os mecanismos moleculares que ocorrem durante o período do vingamento, continuam por esclarecer. Análises do transcritoma (RNA-Seq) e metaboloma das inflorescências e das alterações fisiológicas da videira permitiram clarificar alguns mecanismos de regulação da transição de flor para bago e abscisão de flores. Relativamente ao vingamento, foram observadas alterações na regulação do transporte de nutrientes, no metabolismo secundário, dos hidratos de carbono e hormonal. A acumulação de ácido indol-3-acético e activação das vias de sinalização dos açúcares e do etileno podem induzir a síntese de giberelinas, estimulando a divisão celular. As análises realizadas após a pulverização com ácido giberélico (GAc) e redução da radiação incidente durante a floração, promovendo a queda de flores, sugeriram que estes dois estímulos provocam efeitos opostos no metabolismo das inflorescências. A resposta ao GAc envolveu um reforço do metabolismo energético e indução da biossíntese de nucleótidos. Pelo contrário, a sombra inibiu a fotossíntese, induziu a um desequilíbrio C/N e uma alteração global do metabolismo hormonal. As vias metabólicas comuns conduzindo à abscisão foram o catabolismo da putrescina, indução da biossíntese de auxinas, repressão da biossíntese de giberelinas e activação de mecanismos antioxidantes, por transcritos e metabolitos específicos. Para optimizar métodos de monda indispensáveis na produção de uva de mesa, a aplicação de GAc e do sombreamento durante a floração foram testados em diferentes cultivares. A 'Thompson Seedless' mostrou ser sensível a ambos os métodos em condições de campo, no entanto apenas a aplicação de GAc melhorou a qualidade dos bagos. Os dois tratamentos induziram a queda de flores na 'Black Magic' durante o ciclo de produção tardio em estufa, enquanto que no ciclo precoce apenas o sombreamento melhorou a qualidade dos cachos e bagos, sendo efectivo como método de monda. Palavras-chave: abscisão, ácido giberélico, sombreamento, videira, vingamento. iii Resumo alargado Abscisão de flores e vingamento em uva de mesa (Vitis vinifera L.): estudo dos mecanismos fisiológicos e moleculares Na videira (Vitis vinifera L.), o vingamento e a abscisão de flores ocorrem simultaneamente, após a queda das caliptras, determinando o número final de bagos, o seu calibre e a productividade. Apesar da importância da espécie cultivada, os mechanismos moleculares que regulam estes processos na videira foram pouco estudados. Este trabalho pretendeu caracterizar as alterações fisiológicas, metabólicas e transcritómicas que ocorrem durante a fase de transição de flor para bago e durante a indução de abscisão das flores, recorrendo a técnicas de transcritómica (RNA-Seq com a tecnologia Illumina) e metabolómica (plataforma que conjuga UHLC/MS/MS2 e GC/MS) em larga escala, integradas com análises cromatográficas de metabolitos específicos, determinações das trocas gasosas e teor de clorofila nas folhas e medição do crescimento vegetativo, ao longo do tempo. Estas técnicas foram aplicadas nas análises realizadas com a cultivar apirénica Thompson Seedless em condições de campo e com a cultivar com semente Black Magic em condições controladas em estufa, à excepção do RNA- Seq na Black Magic. Foram analisadas inflorescências da 'Thompson Seedless' recolhidas a 3, 5 e 7 dias após 100% da queda das caliptras. Os nossos resultados mostraram que o processo de vingamento requer a indução da divisão celular, inibição da transcrição de genes relacionados com a senescência e com a regulação do transporte molecular,
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