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Genetics of Resistance to Scab Caused by Venturia Inaequalis in 'Président Roulin' and 'Geneva' Apple Cultivars

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Genetics of Resistance to Scab Caused by Venturia Inaequalis in 'Président Roulin' and 'Geneva' Apple Cultivars COMMUNAUTE FRANÇAISE DE BELGIQUE UNIVERSITE DE LIEGE – GEMBLOUX AGRO-BIO TECH GENETICS OF RESISTANCE TO SCAB CAUSED BY VENTURIA INAEQUALIS IN 'PRÉSIDENT ROULIN' AND 'GENEVA' APPLE CULTIVARS Héloïse Bastiaanse Essai présenté en vue de l’obtention du grade de docteur en sciences agronomiques et ingénierie biologique Promoteurs : Marc Lateur et Philippe Lepoivre 2015 Copyright Aux termes de la loi belge du 30 juin 1994, sur le droit d’auteur et les droits voisins, seul l’auteur a le droit de reproduire partiellement ou complètement cet ouvrage de quelque façon et forme que ce soit ou d’en autoriser la reproduction partielle ou complète de quelque manière et sous quelque forme que ce soit. Toute photocopie ou reproduction sous autre forme est donc faite en violation de la dite loi et des modifications ultérieures. Héloïse Bastiaanse (2015). Genetics of resistance to scab caused by Venturia inaequalis in ‘Président Roulin’ and ‘Geneva’ apple cultivars. (PhD Dissertation in English). Gembloux, Belgium, Gembloux Agro-Bio Tech, University of Liège. Abstract Apple scab caused by Venturia inaequalis is the major constraint to apple production worldwide. Today, an intensive use of pesticide is required to protect commercial orchards planted with cultivars (cvs) highly susceptible to scab. This intensive use of pesticides costs, and has a detrimental impact on the consumer health and the environment, but could be largely reduced by the introduction of resistant or partially resistant scab cvs in the orchard. This thesis aims to provide new insights into the mechanisms of resistance of two cvs presenting contrasting resistance phenotypes and durability: the durable partial resistance in ‘Président Roulin’ and the non durable resistance in ‘Geneva’, harboring a complex of complete and partial effects R genes. Preliminary, phytopathological tests were used in both cvs to differentiate the resistance loci. Resistance in both cultivars were shown to be race-specific and governed by at least five resistance loci. Expression signature of the partially resistant ‘Président Roulin’ challenged by V. inaequalis revealed common but also different molecular pathways as compared to the susceptible ‘Gala’ and a completely resistance Rvi6 (Vf) ‘Gala’-transformed line. Thirteen candidate defense genes (CDGs) were identified and their expression characterized over a time-course experiment during pathogen infection. Co-localizations of CDGs with apple genomic regions known to carry resistance factors were found (QTLs, major scab genes, or analogues of resistance genes). Finally, contribution to their functional assessment was made by investigating correlations between their expression and the level of resistance in a progeny derived from the cross between ‘Gala’ and ‘Président Roulin’. Regulation of nine CDGs accounted for 46% of the phenotypic variance. In ‘Geneva’, five resistance loci (with dominant and more complex recessive control) were fine mapped in a region of 5 centimorgan (cM) located at the distal end of chromosome 4. This region corresponded to a 2 megabase pairs (Mbp) region containing nine CDGs encoding for nucleotide binding site-leucine rich repeat (NBS-LRR) family proteins on the ‘Golden Delicious’ apple reference genome. Overall this thesis contributed to better understand the genetic determinism of the resistance of apple against scab and its durability. Results were also at the basis of development of molecular marker tools to speed up the selection in a genome-informed breeding program. Héloïse Bastiaanse (2015). Déterminisme génétique de la résistance des variétés ‘Président Roulin’ et ‘Geneva’ à la tavelure du pommier cause par Venturia inaequalis (Thèse de doctorat en anglais). Gembloux, Belgium, Gembloux Agro-Bio Tech, University of Liège. Résumé La tavelure, causée par Venturia inaequalis, est la principale maladie présente dans les vergers commerciaux de pommiers. Aujourd’hui la plupart de ces vergers sont plantés de variétés extrêmement sensibles à la maladie. La lutte contre la tavelure requiert ainsi l’usage intensif de fongicides, ce qui a un impact tant sur le coût de production que sur l’environnement et la santé des consommateurs. Une méthode alternative à un tel usage de pesticides réside dans la plantation de variétés résistantes ou partiellement résistantes à la tavelure. Dans ce contexte, cette thèse a pour objectif d’étudier le déterminisme génétique de deux variétés de pommiers aux formes contrastées de résistance : ‘Président Roulin’, ancienne variété belge présentant une résistance partielle et durable à la tavelure, et ‘Geneva’, variété à chair rouge présentant un complexe de plusieurs gènes majeurs et mineurs de résistance, non durables en vergers. Premièrement, afin de différencier les loci de résistance au sein des deux variétés, des tests phytopathologiques ont été réalisés par l’inoculation de différentes races de V. inaequalis. Les deux formes de résistance ont démontré être spécifiques aux races de tavelure et être sous le contrôle d’au moins cinq loci de résistance. Une analyse de données transcriptomiques semble démontrer que l’expression de la résistance partielle de ‘Président Roulin’ empreinte des voies métaboliques communes mais aussi différentes de celles observées dans le cas d’une réaction compatible (variété sensible ‘Gala’) ou incompatible (ligne ‘Gala’ transformée par le gène majeur de résistance Rvi6 (Vf)). Treize gènes candidats de défense (GCD) ont été sélectionnés, et leur expression respective a été caractérisée après différentes périodes de temps au cours de l’infection par V. inaequalis. Certains GCD semblent être localisés dans des régions génomiques du pommier porteuses de facteurs de résistance déjà connus (gènes majeurs, loci de caractères quantitatifs et analogues de gènes de résistance). Enfin, la fonction de ces GCD dans les mécanismes de résistance partielle à la tavelure de ‘Président Roulin’ a été évaluée par l’estimation des corrélations existant entre la régulation de ces gènes et l’expression de la résistance dans une population en ségrégation dérivée du croisement entre ‘Gala’ et ‘Président Roulin’ : 46% de la proportion de la variance phénotypique a pu être expliquée par la régulation de neuf GCD. Chez ‘Geneva’, cinq loci de résistance (avec un contrôle dominant, ainsi qu’un contrôle récessif plus complexe) ont pu être finement cartographiés dans une région de 5 centimorgans (cM) située à l’extrémité du chromosome 4 du pommier. Cette région correspond à 2 mégabases dans le génome de référence de ‘Golden Delicious’ et contient neuf GCD encodant des protéines de résistance de la famille ‘nucleotide binding site-leucine rich repeat’ (NBS-LRR). En conclusion, cette thèse contribue à une meilleure compréhension à la fois du déterminisme génétique et des mécanismes biologiques de résistance à la tavelure du pommier. Cette thèse a de plus contribué au développement d’outils de marqueurs moléculaires visant à accélérer le processus de sélection dans des programmes modernes d’amélioration du pommier. Acknowledgment My PhD has been an epic journey, across a wide diversity of offices, labs, orchards and greenhouses across Belgium, New Zealand, and even the USA from where I am writing the present lines. This provided me the opportunity to meet a great number of people to whom I would like to express my sincerest gratitude. Without your help, your support, your knowledge and advice, I would not have achieved this work. First, I would like to acknowledge my advisors, Dr. Marc Lateur (Walloon Agricultural Research Center, CRA-W) and Prof. Philippe Lepoivre (Gembloux Agro-Bio Tech, GxABT, University of Liège), for their guidance through this work. Mr. Lateur, I particularly appreciated your contagious enthusiasm for the genetics and breeding of fruit trees. From the close scrutiny of apple scab resistance symptoms in the orchard to the excitement of the spring time cross pollinations and the tasting of the very first fruits of our new born accessions, I could not have had a better advisor than you. I have now the audacity to confess your nickname, ‘Monsieur Pomme’, when I mentioned you to my friends and family… I quit our work in the cherished apple orchards at the CRA-W to meet up the next challenges in my scientific carrier, but I made the tree genetics my favorite topic of research! I would like to extend my sincerest gratitude to my jury members: Prof. Marie-Laure Fauconnier (President of the jury, GxABT, University of Liège), Prof. Haïssam Jijakli (GxABT, University of Liège), Prof. Hervé Vanderschuren (GxABT, University of Liège) and Prof. Wannes Keulemans (Katholieke Universiteit Leuven) for their valuable comments on my work. I am also grateful to Prof. Patrick du Jardin (GxABT, University of Liège), Prof. Franck Dequiedt (GxABT, University of Liège) and Dr. Dominique Mingeot (CRA-W) as members of my thesis committee. I would like to thank all the colleagues that I met during the first part of my PhD journey at the CRA- W and the Phytopatholy Unit at GxABT for helping me through the various challenges I experienced during this thesis. Special thanks to: - My Jedi Masters, Yordan Muhovsky (CRA-W) and Olivier Parisi (GxABT, University of Liège) for sharing with me, the young and innocent ‘padawan’ I was, your knowledge (and wisdom! ;o) for the molecular biology techniques. Without your precious help, I would not have made my way through the (very technical) pouring and transfer of the giant AFLP gels as well as the very diverse and numerous days troubleshooting the RNA extractions, purifications, amplifications and visualizations. Thank you guys for your expertise in the lab, your time and your patience! - The ‘RGF’ team at the CRA-W, aka ‘les garçons’: Thibaut, Pascal, Laurent D., ‘Stris’, Alain, Bertrand and Patrick, as well as Bruno and Laurent J. and for the most feminine part of the team, Audrey, Anne, Isabelle and Joanna! Thank you for your help and advice, notably in the grafting, and raising of the apple trees used in this PhD. Thank you also for our relaxing lunch time, playing cards under the loud exclamations of our favorite ‘Godu’. I was often the perfect candidate for your playful little tricks and it always created the opportunity to share a good laugh.
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