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Gene Expression Reprogramming During the Formation of Feeding Sites Induced by Plant Endoparasitic Nematodes

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Gene Expression Reprogramming During the Formation of Feeding Sites Induced by Plant Endoparasitic Nematodes UNIVERSIDAD DE CASTILLA LA MANCHA FACULTAD DE CIENCIAS AMBIENTALES Y BIOQUÍMICA DEPARTAMENTO DE CIENCIAS AMBIENTALES Gene expression reprogramming during the formation of feeding sites induced by plant endoparasitic nematodes TESIS DOCTORAL JAVIER CABRERA CHAVES (TOLEDO, 2016) UNIVERSIDAD DE CASTILLA LA MANCHA FACULTAD DE CIENCIAS AMBIENTALES Y BIOQUÍMICA DEPARTAMENTO DE CIENCIAS AMBIENTALES ÁREA DE FISIOLOGÍA VEGETAL Gene expression reprogramming during the formation of feeding sites induced by plant endoparasitic nematodes Javier Cabrera Chaves 2016 UNIVERSIDAD DE CASTILLA LA MANCHA FACULTAD DE CIENCIAS AMBIENTALES Y BIOQUÍMICA DEPARTAMENTO DE CIENCIAS AMBIENTALES ÁREA DE FISIOLOGÍA VEGETAL Gene expression reprogramming during the formation of feeding sites induced by plant endoparasitic nematodes Memoria presentada por el licenciado Javier Cabrera Chaves para optar al grado de Doctor por la Universidad de Castilla- La Mancha. Trabajo dirigido por la Dra. Carolina Escobar Lucas de la Universidad de Castilla- La Mancha Toledo, 2016 Vº Bº del Director de Tesis El Doctorando Dra. Carolina Escobar Lucas Javier Cabrera Chaves INDEX INDEX CONCEPTUAL GRAPH SUMMARY CHAPTER 1: Introduction Purpose of the chapter Overview of Root-Knot Nematodes and Giant Cells Developmental Pathways Mediated by Hormones in Nematode Feeding Site The Power of Omics to Identify Plant Susceptibility Factors and to Study Resistance to Root-knot Nematodes AIMS AND OBJECTIVES CHAPTER 2: Holistic analyses on plant- nematode interactions Purpose of the chapter Distinct and conserved transcriptomic changes during nematode- induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression Differentially expressed small RNAs in Arabidopsis galls formed by Meloidogyne javanica: a functional role for miR390 and its TAS3-derived tasiRNAs NEMATIC: a simple and versatile tool for the in silico analysis of plant–nematode interactions CHAPTER 3: Molecular parallelisms between lateral roots and giant cell and gall formation Purpose of the chapter A role for LATERAL ORGAN BOUNDARIES-DOMAIN 16 during the interaction Arabidopsis–Meloidogyne spp. provides a molecular link between lateral root and root-knot nematode feeding site development Genes co-regulated with LBD16 in nematode feeding sites inferred from in silico analysis show similarities to regulatory circuits mediated by the auxin/cytokinin balance in Arabidopsis CHAPTER 4: A new method for the phenotyping of the giant cells Purpose of the chapter Phenotyping nematode feeding sites: three-dimensional reconstruction and volumetric measurements of giant cells induced by root-knot nematodes in Arabidopsis INTENGRATED DISCUSSION CONCLUSIONS CONCEPTUAL GRAPH SUMMARY Chapter 1: Introduction Chapter 2: Holistic Studies A general overview of the plant nematode interaction Chapter 3: LBD16 & Lateral Roots and the research Chapter 4: 3D Reconstruction performed in this field Developmental pathways Holistic studies performed mediated by hormones in the susceptible and and altered during the resistant interactions with plant- nematode root- knot nematodes interactions A method for the 3D phenotping of the giant cells. Insights into their volumes and morphological features Transcriptomic and The transcriptomes of molecular mechanisms are early developing giant cells common between lateral from tomato and root and giant cells and arabidopsis showed a gall formation. LBD16 is a common massive and key gene in both functional gene repression processes A tool to facilitate the selection of genes frm the data generated on trasncriptomes from plant- nematode interactions and other fields miRNA and tasiRNA Regulation of LBD16 co- pathways for gene regulated genes differs silencing are functional in between giant cells and galls and the rasiRNAs are syncytia. Differences in highly induced. Molecular the balance parallelisms with lateral Auxins/Cytokinins between roots both feeding cells Chapter 1: Introduction Chapter 2: Holistic Studies A general overview of the plant nematode interaction Chapter 3: LBD16 & Lateral Roots and the research Chapter 4: 3D Reconstruction performed in this field Developmental pathways Holistic studies performed mediated by hormones in the susceptible and and altered during the resistant interactions with plant- nematode root- knot nematodes interactions A method for the 3D phenotping of the giant cells. Insights into their volumes and morphological features Transcriptomic and The transcriptomes of molecular mechanisms are early developing giant cells common between lateral from tomato and root and giant cells and arabidopsis showed a gall formation. LBD16 is a common massive and key gene in both functional gene repression processes A tool to facilitate the selection of genes frm the data generated on trasncriptomes from plant- nematode interactions and other fields miRNA and tasiRNA Regulation of LBD16 co- pathways for gene regulated genes differs silencing are functional in between giant cells and galls and the rasiRNAs are syncytia. Differences in highly induced. Molecular the balance parallelisms with lateral Auxins/Cytokinins between roots both feeding cells CHAPTER 1: Introduction Chapter 1: Introduction Chapter 2: Holistic Studies A general overview of the plant nematode interaction Chapter 3: LBD16 & Lateral Roots and the research Chapter 4: 3D Reconstruction performed in this field Developmental pathways Holistic studies performed mediated by hormones in the susceptible and and altered during the resistant interactions with plant- nematode root- knot nematodes interactions A method for the 3D phenotping of the giant cells. Insights into their volumes and morphological features Transcriptomic and The transcriptomes of molecular mechanisms are early developing giant cells common between lateral from tomato and root and giant cells and arabidopsis showed a gall formation. LBD16 is a common massive and key gene in both functional gene repression processes A tool to facilitate the selection of genes frm the data generated on trasncriptomes from plant- nematode interactions and other fields miRNA and tasiRNA Regulation of LBD16 co- pathways for gene regulated genes differs silencing are functional in between giant cells and galls and the rasiRNAs are syncytia. Differences in highly induced. Molecular the balance parallelisms with lateral Auxins/Cytokinins between roots both feeding cells Aim of the chapter. This introductory chapter is composed by three different review articles with the aim of offering an insight into the current state of the art of the plant- nematode interaction research. It is mainly centred in the root-knot nematodes and particularly in molecular aspects of the interaction. The first review article entitled “Overview of Root-Knot Nematodes and Giant Cells” discusses general aspects of the morphology, the life cycle including the reproduction of the nematodes of the genus Meloidogyne spp., as well as the impact of this plague in the agriculture worldwide. Moreover, an overview of the present knowledge on the morphological and molecular changes occurring during the development of the root- knot nematode feeding cells, the giant cells, is also shown. The article gives a hint of the research on giant cells and galls biology and development based largely on microscopy and molecular biology techniques. This overview is followed by a more detailed description of those plant developmental pathways mediated by hormones that could be contributing to the formation of the giant cells induced by Meloidogyne spp. or to the syncytia induced by cyst nematodes. This review entitled “Developmental Pathways Mediated by Hormones in Nematode Feeding Sites” discusses the parallelisms found at the gene regulation level between the processes of the development of different plant tissues or organs such as the root apical meristem or the lateral roots and the formation of the nematode feeding sites, and how nematode secretions should interfere with hormone- regulated developmental pathways in the roots to establish their feeding sites. Under the title of “The Power of Omics to Identify Plant Susceptibility Factors and to Study Resistance to Root-knot Nematodes (RKNs)”, the last section of this introductory chapter reviews the approaches based on omic techniques for the study of the RKNs interaction. The vast data generated in this holistic studies helped to a better understanding of the giant cells and galls development, and to the identification of putative plant susceptibility factors; some of them helpful to the development of biotechnological tools for nematode control. Moreover, this introduction makes reference to some of the results obtained during the experimental work of this thesis, highlighting some of the main conclusions obtained. In this way, the results obtained during my PhD have been incorporated to the state of the art of the research on this field, helping to placing them in context and to understand their significance. CHAPTER ONE Overview of Root-Knot Nematodes and Giant Cells Carolina Escobar1,a, Marta Barcalaa, Javier Cabrera, Carmen Fenoll Laboratory of Plant Physiology, Department of Environmental Sciences, Universidad de Castilla-La Mancha, Toledo, Spain 1Corresponding author: E-mail: [email protected] Contents 1. Introduction to Plant Parasitic Nematodes 2 2. General Aspects of Root-Knot Nematodes (RKNs) 5 3. The Morphology and Reproduction of RKNs 8 4. The Life Cycle of RKNs 12 5. Giant Cells (GCs): From Vascular Cells to Nourishing
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