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Strategies for Conservation of Rare and Endemic Strategies for Conservation of Rare and Endemic Species: Characterization of Genetic and Epigenetic Variation and Unusual Reproductive Biology of Coastal Species from Limonium ovalifolium and Limonium binervosum Complexes (Plumbaginaceae) TESE APRESENTADA PARA OBTENÇÃO DO GRAU DE DOUTOR EM BIOLOGIA ANA SOFIA DA SILVA VALBORDO RÓIS ORIENTADORA: Dr. Ana Cristina Delaunay Caperta COORIENTADOR: Dr. Timothy F. Sharbel Júri: Presidente: Reitor da Universidade de Lisboa Vogais: Doutora Maria Wanda Sarujine Viegas Professora Catedrática Instituto Superior de Agronomia da Universidade de Lisboa Doutor João Carlos Mano Castro Loureiro Professor Auxiliar Faculdade de Ciências e Tecnologias da Universidade de Coimbra Doutor Octávio Fernando de Sousa Salgueiro Godinho Paulo Professor Auxiliar Faculdade de Ciências da Universidade de Lisboa Doutor Jorge Henrique Capelo Gonçalves Investigador Auxiliar Instituto Nacional de Investigação Agrária e Veterinária Doutora Ana Cristina Delaunay Caperta Investigadora Auxiliar Instituto Superior de Agronomia da Universidade de Lisboa LISBOA 2014 Strategies for Conservation of Rare and Endemic Species: Characterization of Genetic and Epigenetic Variation and Unusual Reproductive Biology of Coastal Species from Limonium ovalifolium and Limonium binervosum Complexes (Plumbaginaceae) TESE APRESENTADA PARA OBTENÇÃO DO GRAU DE DOUTOR EM BIOLOGIA ANA SOFIA DA SILVA VALBORDO RÓIS ORIENTADORA: Dr. Ana Cristina Delaunay Caperta COORIENTADOR: Dr. Timothy F. Sharbel Júri: Presidente: Reitor da Universidade de Lisboa Vogais: Doutora Maria Wanda Sarujine Viegas Professora Catedrática Instituto Superior de Agronomia da Universidade de Lisboa Doutor João Carlos Mano Castro Loureiro Professor Auxiliar Faculdade de Ciências e Tecnologias da Universidade de Coimbra Doutor Octávio Fernando de Sousa Salgueiro Godinho Paulo Professor Auxiliar Faculdade de Ciências da Universidade de Lisboa Doutor Jorge Henrique Capelo Gonçalves Investigador Auxiliar Instituto Nacional de Investigação Agrária e Veterinária Doutora Ana Cristina Delaunay Caperta Investigadora Auxiliar Instituto Superior de Agronomia da Universidade de Lisboa LISBOA 2014 Ao meu eterno avô Zé… Strategies for conservation of rare and endemic species: characterization of genetic and epigenetic variation and unusual reproductive biology of coastal species from Limonium ovalifolium and Limonium binervosum complexes (Plumbaginaceae) “We do not even in the least know the final cause of sexuality; why new beings should be produced by the union of the two sexual elements... The whole subject is as yet hidden in darkness.” Charles Darwin (1862) The research presented in this thesis was carried out at the research group of Genetics Section, Centro de Botânica Aplicada a Agricultura, Instituto Superior de Agronomia (ISA), University of Lisbon, Portugal; in the Apomixis group at the Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben, Germany; and in the Institute of Biological Sciences, Edward Llwyd Building, at the University of Wales Aberystwyth, United Kingdom. LISBOA 2014 INDEX TABLE OF CONTENTS……………………………………………………………………..I LIST OF FIGURES………………………………………………………………………….IV LIST OF TABLES……………………………………………………………………………V LIST OF ABBREVIATIONS…………………………………………………………….....VI PUBLICATIONS AND PRESENTATIONS (during PhD study)……………………..VII ACKNOWLEDGEMENTS………………………………………………………………….IX ABSTRACT…………………………………………………………………………………..X RESUMO…………………………………………………………………………………….XI CHAPTER I - GENERAL INTRODUCTION AND LITERATURE REVIEW 1. Limonium Mill. genus…………………………………………………………………...2 1.1. General description…………………………………………………………………....2 1.2. Taxonomic complexity………………………………………………………………..3 1.3. Karyological polymorphisms………………………………………………………….6 1.4. Floral heteromorphies and mating systems………………………………………....6 1.5. Genetic diversity and differentiation ………………………………………………....8 2. Sexual reproduction versus apomixis……………………………………………..10 2.1. Tetraspory and apomixis……………………………………………………………..10 2.2. Origins of apomixis…………………………………………………………………...12 3. Conservation issues…………………………………………………………………..13 4. Aims of the dissertation……………………………………………………………....20 5. Literature cited………………………………………………………………………….21 CHAPTER II - GENERAL MATERIALS AND METHODS 1. Ethics statements………………………………………………………………………27 2. Field methods...………………………………………………………………………...27 2.1. Study species and population sampling…………………………………………....27 3. Laboratory methods…………………………………………………………………...28 3.1. Plant materials and growth conditions……………………………………………...28 4. Morphometric analysis………………………………………………………………..29 5. Cytometric analysis……………………………………………………………………29 5.1. Genome size estimations…………………………………………………………….29 6. Cytological, cytoembryological and cytohistological studies………………...30 6.1. Karyotyping…………………………………………………………………………..30 6.2. Reproductive biology analyses..……………………………………………………30 6.2.1. Male sporogenesis and gametogenesis…………………………………………31 6.2.2. Female sporogenesis and gametogenesis……………………………………...31 6.3. Seed analysis………………………………………………………………………...32 7. Floral heteromorphies analyses, pollen exclusion tests and crossing experiments………....................................................................................................32 8. Molecular analysis……………………………………………………………………..33 8.1. Epigenetic assessment: the MSAP technique…………………………………….33 8.2. Genetic analyses: cpDNA marker analysis………………………………………..34 9. Literature cited………………………………………………………………………….37 I CHAPTER III - SPECIES DISTRIBUTION IN CONTINENTAL PORTUGAL 1. Abstract………………………………………………………………………………….41 2. Introduction……………………………………………………………………………..41 3. Material and methods…………………………………………………………………44 3.1. Study species………………………………………………………………………...44 3.2. Studied area…………………………………………………………………………..45 3.3. Plant material…………………………………………………………………………45 4. Results…………………………………………………………………………………...45 5. Discussion………………………………………………………………………………48 6. Literature cited………………………………………………………………………….69 CHAPTER IV - MALE FERTILITY VERSUS STERILITY, CYTOTYPE, AND SEED PRODUCTION IN DIPLOID AND TETRAPLOID LIMONIUM REVEAL DIVERSITY IN REPRODUCTION MODES 1. Abstract………………………………………………………………………………….72 2. Introduction……………………………………………………………………………..73 3. Material and methods…………………………………………………………………75 3.1. Plant materials and growth conditions……………………………………………...75 3.2. Chromosome preparation and karyotyping………………………………………..76 3.3. Genome size estimations……………………………………………………………76 3.4. Cytological analyses of microsporogenesis………………………………………..77 3.5. In vitro pollen viability tests………………………………………………………….77 3.6. In vitro pollen germination…………………………………………………………...78 3.7. Optical microscopy analysis and imaging………………………………………….78 3.8. Electron microscopy pollen and seed analyses…………………………………...78 3.9. Cytohistological analysis of mature seeds………………………………………....79 3.10. Flow cytometric screening of seeds………………………………………………79 4. Results…………………………………………………………………………………...80 5. Discussion………………………………………………………………………………84 6. Literature cited………………………………………………………………………....97 CHAPTER V - EPIGENETIC RATHER THAN GENETIC FACTORS MAY EXPLAIN PHENOTYPIC DIVERGENCE BETWEEN DIPLOID AND TETRAPLOID LIMONIUM 1. Abstract...............................................................................................................101 2. Introduction........................................................................................................101 3. Material and methods........................................................................................105 3.1. Study species....................................................................................................105 3.2. Morphometric analysis.......................................................................................105 3.3. DNA isolation.....................................................................................................106 3.4. Genetic/Epigenetic analysis - MSAP procedure...............................................106 3.5. Data analyses....................................................................................................107 3.6. Analysis of Genetic/Epigenetic Variance...........................................................108 4. Results...............................................................................................................109 4.1. Morphological differentiation between diploid and tetraploid species..............109 4.2. MSAP profiles analysis.....................................................................................110 II 4.3. Genetic/epigenetic divergence of diploid and tetraploid Limonium species....110 4.4. Tetraploid species compensate lower genetic variability with higher epigenetic variability…………………………………………………………………………………………111 5. Discussion…………………………………………………………………………….112 6. Literature cited………………………………………………………………………..132 CHAPTER VI - SEX AND APOMIXIS SHAPE CHLOROPLAST DNA VARIATION PATTERNS IN DIPLOID AND TETRAPLOID LIMONIUM 1. Abstract.............................................................................................................138 2. Introduction.......................................................................................................138 3. Material and methods.......................................................................................141 3.1. Study species and population sampling...........................................................141 3.2. DNA isolation, PCR amplification and sequencing..........................................142 3.3. Data analyses..................................................................................................142
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