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Genetics and Genomics of Cultivated Eggplants and Wild Relatives

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Genetics and Genomics of Cultivated Eggplants and Wild Relatives Genetics and genomics of cultivated eggplants and wild relatives PhD dissertation by Pietro Gramazio Advisors Jaime Prohens Tomás Santiago Vilanova Navarro Valencia, February 2018 “Nothing in life is to be feared, it is only to be understood. Now is the time to understand more, so that we may fear less.” Maria Salomea Skłodowska-Curie Agradecimientos Aunque parezcan mucho menos, ya siete son los años que llevo en el COMAV. Los años pasan volando cuando el ambiente de trabajo es estimulante, constructivo, apasionante, gratificante, motivador, intrigante, creativo, integrador, cooperativo, productivo, positivo, divertido…, familiar. Todo empezó aquella tarde del 10 de noviembre del 2010, cuando Lola Raigón, a quien va mi eterna gratitud, me presentó la persona que iba a cambiar mi vida, Jaime Prohens. Jaime, la admiración, el respeto y la gratitud que siento por ti no se pueden expresar en unas pocas frases. Eres la persona que más me ha enseñado, motivado y animado en estos años. Has conseguido sacar de mí unas cualidades que ni siquiera había imaginado tener. Tu inteligencia, sabiduría, humildad, paciencia, hacen de ti un verdadero líder. Gracias por estar pendiente en cada momento, espero colaborar contigo durante muchos años más. Eres un ejemplo a seguir y fuente de inspiración y guía para mi y muchas personas. Mi formación doctoral no sería completa si no hubiera sido por tí, Santi. Intelligente, simpatíco, caótico, siempre de buen humor y "runner". Gracias por todo el conocimiento, las buenas ideas, las clases de Génomica, las risas y los videos "frikis" que has compartido conmigo. Gracias por alegrar nuestros días. Mariola, aunque burocráticamente no has podido ser mi co-directora, te agradezco el apoyo, motivación y alegría de estos años. Aunque ahora pasamos todo el día en los despachos, echo de menos los primeros años de laboratorio, cuando pasábamos horas y horas hablando de lo que fuera. Junto a Jaime y Santi, eres un pilar de "Los Berenjen@s". Gracias a mi "hermano mayor" Javi, por los muchos momentos de amistad pasados juntos, por tu inteligencia, por compartir tus experiencias, por tu buen gusto musical, tu escepticismo, por ser un gran amigo. "Los Berenjen@s" se han ido multiplicando y muchas son las entradas que hemos recolectado en estos años alrededor del mundo. Me hubiera gustado escribir algo sobre cada uno de vosotros, pero necesitaría otro capítulo de tesis, así que os agradeceré de forma conjuntas. Gracias Abou, Adriana, Agustín, Alba E., Alba L., Alessio, Andrea, Arantxa, Arunika, Bianca, Brice, Camil, Carolina, Celia, Celine, Cristina, Dani, David, Dionís, Dora, Edgar, Elena C., Elena R., Elisa, Francesco, Giulio, Gloria, Ioana, Irene, Isa, Juan, Juan Pablo, Judith, Lahiru, Lara, Laura, Loles, Maria, Marieta, Michael, Muditha, Nacho, Nadia, Nirasha, Noelia, Orsi, Pelin, Prashant, Ramses, Ranil, Rory, Silia, Sorin, Trong, por haber aportado vuestro granito de arena para la realización de esta tesis y de colaboraciones varias. Todos, los que todavía estáis por aquí y los que se han ido, habéis dejado una huella en el laboratorio y en mí (Pido disculpa si se me ha olvidado alguien, sois muchos los que se han pasado por el labo). Gracias también a todos mis compañeros del COMAV, grandes profesionales que han contribuido a mi formación doctoral y personal y por haber compartido tantas horas, sobretodo en los almuerzos y comidas. Muchos de vosotros sois muy buenos amigos. Especialmente quiero agradecer a los bioinformáticos (Peio, Jose, Ximo y Pau) por los consejos, explicaciones y paciencia cuando tenía dudas y me salían errores en la terminal y a MªJosé Díez por ser tan buena persona e investigadora y por dejarme colaborar en la asignatura de Mejora Genética Vegetal. I also would like to thanks to all the colleagues and collaborators that strongly contributed to this thesis: Sandra Knapp, the Global Crop team (Hannes Dempewolf and Benjamin Kilian), the Italian team (Sergio Lanteri, Ezio Portis, Lorenzo Barchi, Alberto Acquadro and Cinzia Comino), Rachel Meyer and Aureliano Bombarely. Un ringraziamento speciale a mia madre, per essere stata una donna cosí forte nei momenti difficili, per avermi cresciuto con dei valori sani, per avermi sostenuto e spronato in ogni mia scelta, per essere lí sempre quando c'è ne bisogno. Alle mie sorelle, i miei cognati e i miei nipoti, per l'affetto che mi dimostrano giornalmente nonostante la lontananza. A mio padre. Ad Antonella, alla compagna di questo lungo viaggio, alla persona piú importante della mia vita, la quale mi sopporta tutti i giorni da ormai tanti anni, dedico questa tesi. So Long, and Thanks for All the Fish Abstract Feeding the future burgeoning population in a climate change scenario demands new breeding approaches and tools to develop new resource- efficient and resilient crop varieties. Among vegetable crops, eggplant (Solanum melongena) is recognized as an important food crop and as such is included in the Annex 1 of the International Treaty on Plant Genetic Resources for Food and Agriculture, which includes 34 crops considered as most relevant for mankind. Before the start of this thesis, few genetic and genomic tools and resources for eggplant breeding, which are reviewed in an introductory chapter, were available. We have recognized the importance of wild eggplant relatives, which have been barely used in eggplant breeding. In this respect, in order to make a more efficient use of wild relatives in plant breeding, we proposed an ambitious approach, called "introgressiomics", consisting of a systematic and massive development of materials carrying introgressions from crop wild relatives (CWRs), which usually are an unexplored and unexploited source of genetic variation for breeding traits. The works done in this thesis are related to the application of the introgressiomics approach to eggplant. In this framework, the general objectives of the thesis are the development of genetic and genomic information and tools in eggplant genepool, using a multidisciplinary and multi-pronged approach to assist eggplant breeding in the development of new improved and resilient varieties using eggplant relatives as a source of variation. Specifically, in the first chapter of this thesis, we sequenced the transcriptome of two eggplant related species, the wild Solanum incanum and the cultivated S. aethiopicum, that have a great interest in eggplant breeding. The transcriptomes were assembled in 83,905 and 87,084 unigenes for S. incanum and S. aethiopicum respectively, which were extensively structurally and functionally annotated. The variant call analysis identified tens of thousands intraspecific and interspecific polymorphisms, as well as around a thousand of SSRs in each species. In the second chapter, a subset of those markers (11 SSRs and 35 SNPs) was tested for confirming their usefulness for genetic fingerprinting, diversity evaluation and the establishment of relationships in cultivated eggplant (common, scarlet and gboma) genepools. We observed that SSRs and SNPs provided different results in the establishment of the relationships, suggesting that each marker type sampled different levels of genetic variation. However, although both markers provided a similar level of information, SNPs seem to provide a better resolution than SSRs for materials phylogenetically more distant. In the third chapter, in order to broaden the estimation of the genetic diversity and genetic relationships among and within wild and cultivated species belonging to eggplant complexes, we performed a massive genotyping, by a genotype-by-sequencing approach, of 76 accessions belonging to 17 species from the primary, secondary and tertiary genepool of common eggplant. Out of 75,399 polymorphic sites identified, 12,859 were associated to CDS regions and used to establish an exhaustive and detailed evaluation of the natural allelic diversity and genetic relationships in eggplant genepool using three different approaches (hierarchical population structure, UPGMA-based dendrogram, and PCoA analysis). In the four chapter, we developed an interspecific genetic map between S. incanum and S. melongena, linked to four previous eggplant maps and to one tomato map. A total of 243 molecular markers were successfully mapped consisting of 42 COSII, 99 SSRs, 88 AFLPs, 9 CAPS, 4 SNPs and one morphological polymorphic markers encompassed 1085 cM distributed in 12 linkage groups. Based on the syntheny with tomato, the candidate genes involved in the core chlorogenic acid synthesis pathway in eggplant (PAL, C4H, 4CL, HCT, C3′H, HQT), five polyphenol oxidase genes (PPO1, PPO2, PPO3, PPO4, PPO5), as well as two genes involved in fruit shape (OVATE, SISUN1), were mapped. Finally, in the fifth chapter, we developed the first introgression line population (IL) in eggplant using S. incanum as a donor parent. A set of 73 selected advanced backcross materials were developed, which covered 99% of the S. incanum genome. Also, 25 fixed immortal ILs were obytained, each carrying a single introgressed fragment in homozygosis, altogether spanning 61.7% of the S. incanum genome. Sixty-eight candidate genes involved in drought tolerance were identified in the set of ILs. In summary, in this thesis we have provided tools, knowledge, approaches and advanced breeding materials to develop enhanced and resilient eggplant varieties using the valuable genetic diversity of CWRs and the precision and efficiency of high-throughput techniques. We consider that the information presented in this work will be useful for the eggplant
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