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New Insights on Black Rot of Crucifers: Disclosing Novel Virulence Genes by in Vivo Host/Pathogen Transcriptomics and Functional Genetics

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New Insights on Black Rot of Crucifers: Disclosing Novel Virulence Genes by in Vivo Host/Pathogen Transcriptomics and Functional Genetics UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS New insights on black rot of crucifers: disclosing novel virulence genes by in vivo host/pathogen transcriptomics and functional genetics Doutoramento em Biologia Microbiologia Joana Costa Cardoso da Cruz Tese orientada por: Doutora Maria Leonor Pato da Cruz Professor Doutor Rogério Paulo de Andrade Tenreiro Documento especialmente elaborado para a obtenção do grau de doutor 201 7 UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS New insights on black rot of crucifers: disclosing novel virulence genes by in vivo host/pathogen transcriptomics and functional genetics Doutoramento em Biologia Microbiologia Joana Costa Cardoso da Cruz Tese orientada por: Doutora Maria Leonor Pato da Cruz Professor Doutor Rogério Paulo de Andrade Tenreiro Júri: Presidente: ● Doutor Rui Manuel Dos Santos Malhó, Professor Catedrático, Faculdade de Ci ências da Universidade de Lisboa Vogais: ● Doutor Pedro Miguel da Silva Albuquerque, Bolseiro Pós - Doutoramento, Instituto de Biologia Molecular e Celular ● Doutora Maria Teresa Ferreira de Oliveira Barreto Goulão Crespo, Responsável de Laboratório – Investigadora Nível 3, Instituto de Bio logia Experimental e Tecnológica (IBET); ● Doutora Amélia Maria Pereira Lopes, Investigadora Auxiliar, Instituto Nacional de Investigação Agrária e Veterinária (INIAV); ● Doutora Maria Leonor Pato da Cruz, Investigadora Auxiliar, Instituto Nacional de Inve stigação Agrária e Veterinária (INIAV) (Orientadora); ● Doutora Maria Helena Mendes da Costa Ferreira Correia de Oliveira, Professora Associada, Instituto Superior de Agronomia da Universidade de Lisboa ● Doutor Manuel Pedro Salema Fevereiro, Professor Aux iliar com Agregação, Faculdade de Ciências da Universidade de Lisboa; ● Doutora Margarida Henriques da Gama Carvalho, Professora Auxiliar, Faculdade de Ci ências da Universidade de Lisboa; Documento especialmente elaborado para a obtenção do grau de doutor Bolsa Individual de Doutoramento SFRH/BD/69787/2010 Fundação para a Ciência e a Tecnologia 201 7 Acknowledgments This thesis is the result of a life - changing experience , an adventure down a sinuous path that I would most certainly could not have walked alone. During this journey, I was always welcomed, encouraged and supported by all the people around me and for that I will be forever thankful . First and foremost, I would like to than k my supervisor, Dr. Leonor Cruz , head of the Phytobacteriology Lab (INIAV) , without whom this work would not have been achievable. I am t hankful for your scientific guidance, support and mentoring . F or allways inspiring me, believing in me and encouraging me to challenge myself. But above all, I am deeply grateful for your selfless dedication and true friendship, that led me every step of the way. I would also like to extend my profound gr atitude to my co - supervisor, Professor Rogério Tenreiro , head of the Microbiology & Biotechnology Group (BioISI/FCUL) , for his constant scientific leadership , constructive criticism and advice , pushing me to the limit and beyond, relentlessly motivating me to do more and better. For that, y ou will always be T he Professor . To both my supervisors, I would like to say that you have made me a better scientist and a better person. I hope our paths continue to cross. I would like to show my appreciation to t he head of UEIS - SAFSV, Dr. Amélia Lopes, for kindly welcoming me at INIAV ever since I was a MSc student , making this institution my home away from home. To the team of t he GMO Lab (INIAV), thank you for your support during the experimental work related to the last chapter of this thesis. To Dr. Raquel S á - Leão and Dr. Carina Va lente, at the Molecular Microbiology of Human Pathogens Lab (ITQB) , for their kind collaboration during the use of their Bioanalyzer System. To Dr. Margarida Gama - Carvalho and Dr. Andreia Fonseca, at the Gene Expressio n & Regulation Group (BioISI/FCUL), I would like to thank you f o r welcoming me and for your guidance and support during the bioinformatic analysis of the results presented in the last chapter of this thesis . You ha ve introduced me to a new world ! To Professor Ana Tenreiro, at the Microbiolog y & Biotechnology Group (BioISI /FCUL ), thank you for your kind collaboration and advice throughout this work. - i - To my colleagues at t he Phytobacteriology Lab (INIAV), Isaura Velez and Camila Fernandes , and to Márcia Santos, Ana Chegão and other colleagues: t h ank you for your friendship and kind words. And f or all the cakes and chocolates , they really kept me going. To my childhood and university friends, thank you for your long - lasting and steady presence in my life, for sharing with me those life - giving laughs and for putting up with me during venting moments. Last, but definitely not least, I would like to dedicate this thesis t o my family . Thank you for everything, y ou are my reason for living. - ii - Abstract Xanthomonas campestris belongs to th e gamma subdivision of Proteobacteria and is the type species of a genus comprising 28 species of plant pathogenic bacteria, affecting 124 species of monocotyledonous and 268 species of dicotyledonous plants. Identified for the first t ime in 1895 in the United States of America, this species has undergone several taxonomic reclassifications, and currently comprises pathovars X. campestris pv. campestris ( Xcc ) , X. campestris pv. raphani ( Xcr ) and X. campestris pv. incanae ( Xci ), causing distinct diseases in vegetables, ornamentals and spontaneous plants belonging to Brassica ceae family, as well as some vegetable crops belonging to the Solanaceae family. Black rot disease , caused by Xcc , is the most important bacterial disease of Brassica cea e , affecting crops and weeds worldwide. After penetration through hydathodes on leaf margins, bacterial multiplication causes t ypical V - shaped lesions on leaf margins, followed by darkening of the veins that evolve to necrosis of the affected tissue, ulti mately leading to plant death. Short - distance dispersal through plant - to - plant contact, human manipulation, wind, insects, aerosols and irrigation water or rain, associated with long distance di spersal through infected seeds and plantlets following commercial routes across the globe are responsible for the worldwide distribution of this disease . Studies on the interaction of Xcc with B. oleracea have identified several virulence genes, however no resistance genes have been successfully cloned in Brassica ceae crops and there is still a lack of effective black rot disease control measures, which continues to cause severe economic losses worldwide. Despite the growing body of work on this subject, mo lecular mechanisms of host - pathogen interaction have been mostly inferred using in vitro approaches, resulting in a knowledge gap concerning the in vivo behavior of this pathogen during its interaction with plant hosts. In Portugal, an important centre of Brassica ceae domestication, Xcc has long been identified and Portuguese Xcc strains have already been described as a unique sub - population of this pathogen. In this context, with the goal of bringing new insights on the molecular mechanisms of host/pathog en interaction, a set of 33 X. campestris strains collected in the country was characterized, in terms of pathogenicity, virulence, population structure and phylogenetic diversity. Furthermore, the in planta transcriptomes of the Xcc strains representing the extremes of the virulence spectrum during the infection process on two selected hosts were profiled, in a total of four pathosystems. A high level of phenotypic diversity, supported by phylogenetic data, was found among X. campestris isolates, allowing the identification of Xcc closely related pathovars Xcr and Xci for the first time in Portugal. Moreover, a mong Xcc isolates, presence of races 4, 6 and 7 was recorded , and - iii - two novel races of this pathovar, race 10 and race 11, were also described. Contra stingly, the partial virulence profiles determined by the presence of known virulence genes were highly conserved among the set of X. campestris strains. The integration of Portuguese strains in a global dataset comprising a total of 75 X. campestris strai ns provided a snapshot of the worldwide X. campestris phylogenetic diversity and population structure , correlating the existing pathovars with three distinct genetic lineages . The identification of an intermediate link between Xcc and Xcr , suggests that t hese pathovars are more closely related to each other than to Xci . This gradient of genetic relatedness seems to be associated to the host range of each pathovar. While Xci appears only to be pathogenic on ornamental Brassica ceae, Xcc and Xcr have a partia lly overlapping host range: Xcc affects mostly Brassica ceous hosts, whereas Xcr , while affecting the same hosts, is also pathogenic on Solanaceous hosts. These findings suggest that instead of causing a host shift, the genetic divergence between Xcc and Xcr conferred the latter strains the ability to explore additional hosts , resulting in a broader host range . Although population displayed a major clonal structure, the presence of recombinational events that may have driven the ecological specialization o f X. campestris and distinct host ranges was highlighted. Portuguese X. campestris strains provided a significant input of genetic diversity, confirming this region as an important diversification reservoir, most likely taking place through host - pathogen c o - evolution. Virulence assessment
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