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University of Castilla-La Mancha Faculty of Environmental Sciences and Biochemistry UNIVERSIDAD DE CASTILLA-LA MANCHA FACULTAD DE CIENCIAS AMBIENTALES Y BIOQUÍMICA Departamento de Ciencias Ambientales Área de Fisiología Vegetal Análisis funcional de genes cruciales para el desarrollo de sitios de alimentación inducidos por nematodos agalladores (Meloidogyne spp.) en arabidopsis Fernando Evaristo Díaz Manzano Doctorado en Ciencias Agrarias y Ambientales Tesis Doctoral Toledo, 2017 Fernando Evaristo Díaz Manzano UNIVERSITY OF CASTILLA-LA MANCHA ENVIRONMENTAL SCIENCES AND BIOCHEMISTRY FACULTY Department of Environmental Sciences Plant Physiology Area Functional analysis of genes crucial for the development of feeding sites induced by root-knot nematodes (Meloidogyne spp.) in arabidopsis Fernando Evaristo Díaz Manzano PhD in Agricultural and Environmental Sciences Doctoral Thesis Toledo, 2017 UNIVERSITY OF CASTILLA-LA MANCHA FACULTY OF ENVIRONMENTAL SCIENCES AND BIOCHEMISTRY Plant Physiology Area Functional analysis of genes crucial for the development of feeding sites induced by root-knot nematodes (Meloidogyne spp.) in arabidopsis AUTHOR: M.Sc. Fernando Evaristo Díaz Manzano DIRECTOR: Dr. Carolina Escobar Lucas CODIRECTOR: Dr. Carmen Fenoll Comes Doctoral Thesis Toledo, 2017 To all those who trusted, trust and will trust in me, Thank you, hugs, and kisses! A todos aquellos que confiaron, confían y confiarán en mi persona, ¡gracias, besos y abrazos! Humility, perseverance and honor... When you observe normality, avoid it; When you see frequency, elude it; When you sense singularity, pursue it. Humildad, perseverancia y honor… Cuando observes normalidad, evítalo; Cuando veas frecuencia, elúdelo; Cuando intuyas singularidad, persíguelo. INDEX OF CONTENTS - 7 - - 8 - Index of contents INDEX OF CONTENTS ........................................................................... - 7 - 1. - ACKNOWLEDGMENTS (AGRADECIMIENTOS) ........................... - 15 - 1.1. - ENGLISH (INGLÉS) .................................................................. - 17 - 1.2. - ESPAÑOL (SPANISH) .............................................................. - 19 - 2. - ABSTRACT (RESUMEN) ............................................................... - 21 - 2.1. - ENGLISH (INGLÉS) .................................................................. - 23 - 2.2. - ESPAÑOL (SPANISH) .............................................................. - 25 - 3. - INTRODUCTION ............................................................................. - 27 - 3.1. - PLANT PARASITIC NEMATODES ............................................. - 29 - 3.1.1. - ROOT KNOT NEMATODES, AN OVERVIEW ........................ - 32 - 3.1.2. – THE CONTROL OF ROOT KNOT NEMATODES .................. - 36 - 3.2. – PLANT DEVELOPMENTAL PATHWAYS ALTERED BY NEMATODES WITHIN THEIR FEEDING SITES: MOLECULAR HALLMARKS OF GALLS AND GIANT CELLS ................................... - 40 - 3.2.1. – PARALELLS BETWEEN LATERAL ROOT FORMATION AND RKNS FEEDING SITES ...................................................................... - 43 - 3.2.2. – GIANT CELLS, FLOWERING AND TUBER FORMATION: ARE THERE SIMILARITIES? ..................................................................... - 47 - 3.3. – GENE SILENCING IN GALLS AND GIANT CELLS ................... - 50 - 3.3.1. – SMALL RNAS IN GIANT CELLS ........................................... - 52 - 4. – OBJECTIVES (OBJETIVOS) ......................................................... - 55 - 5. - METHODOLOGY ............................................................................ - 61 - 5.1. – MATERIAL AND METHODS USED IN THIS THESIS ................ - 63 - 5.1.1. – IN VITRO CULTURE OF ARABIDOPSIS ............................... - 63 - 5.1.2. – PLANT MATERIAL ................................................................ - 63 - 5.1.3. – HOMOZYGOUS LINES SELECTION IN SOIL ....................... - 65 - 5.1.4. – LATE FLOWERING ASSAYS ................................................ - 65 - - 9 - - 10 - Index of contents 5.1.5. – ASSESING LR FOUNDER CELL NUMBER IN INFECTED VERSUS UN-INFECTED PLANTS ..................................................... - 66 - 5.1.6. – MAINTENANCE AND AMPLIFICATION OF NEMATODES ... - 67 - 5.1.7. – IN VITRO INOCULATION WITH NEMATODES ..................... - 68 - 5.1.8. – ANALYSIS OF REPRODUCTION PARAMETERS IN SOIL ... - 68 - 5.1.9. – NEMATODE PERFORMANCE IN POTATO MIR172 OVEREXPRESSOR LINES ............................................................... - 69 - 5.1.10. – GUS ANALYSIS AND GFP EXPRESSION .......................... - 70 - 5.1.11. – GCS & GALL TRANSCRIPTOMES IN SILICO ANALYSIS ... - 70 - 5.1.12. – IN SILICO ANALYSIS OF PLANT AUXIN CIS-ELEMENTS .. - 71 - 5.1.13. – PHARMACOLOGICAL TREATMENTS................................ - 71 - 5.1.14. – PLANT RNA ISOLATION AND QPCR ANALYSIS ............... - 72 - 5.1.15. – PLANT IN SITU HYBRIDIZATION ....................................... - 72 - 5.1.16. – BLASTN ANALYSIS IN CROPS ........................................... - 73 - 5.1.17. – DATA PROCESSING .......................................................... - 73 - 6. - RESULTS AND DISCUSSION ........................................................ - 75 - 6.1.- LONG-TERM IN VITRO SYSTEM FOR MAINTENANCE AND AMPLIFICATION OF RNKS IN CUCUMIS SATIVUS ROOTS ........... - 77 - 6.2.- PHENOTYPING NEMATODE FEEDING SITES: THREE‐DIMENSIONAL RECONSTRUCTION AND VOLUMETRIC MEASUREMENTS OF GIANT CELLS INDUCED BY ROOT‐KNOT NEMATODES IN ARABIDOPSIS ....................................................... - 88 - 6.3.- A RELIABLE PROTOCOL FOR IN SITU MICRORNAS DETECTION IN FEEDING SITES INDUCED BY ROOT-KNOT NEMATODES .... - 108 - 6.4. A COMPARATIVE STUDY OF LATERAL ROOT FORMATION AND THE DEVELOPMENT OF GALLS/GCS THROUGH AUXIN REGULATED PATHWAYS GOVERNING LATERAL ROOT INITIATION............... - 117 - 6.5. - THE GENE REGULATORY MODULE MIRNA172/TOE1/FT IS ACTIVE IN THE FEEDING SITES INDUCED BY MELOIDOGYNE JAVANICA IN ARABIDOPSIS AND HAS A ROLE DURING THE GALL AND GIANT CELLS DEVELOPMENT ............................................. - 147 - 7. - GENERAL DISCUSSION.............................................................. - 173 - 8. - GENERAL CONCLUSIONS (CONCLUSIONES GENERALES) .. - 183 - - 11 - - 12 - Index of contents 9. - SUPPLEMENTAL DATA .............................................................. - 193 - 10. - BOOK CHAPTERS ALREADY PUBLISHED ............................. - 207 - 10.1. - DEVELOPMENTAL PATHWAYS MEDIATED BY HORMONES IN NEMATODE FEEDING SITES......................................................... - 209 - 10.2. - A STANDARDIZED METHOD TO ASSESS INFECTION RATES OF ROOT-KNOT AND CYST NEMATODES IN ARABIDOPSIS THALIANA MUTANTS WITH ALTERATIONS IN ROOT DEVELOPMENT RELATED TO AUXIN AND CYTOKININ SIGNALLING ................... - 227 - 11. - BIBLIOGRAPHY ......................................................................... - 237 - - 13 - - 14 - 1. - ACKNOWLEDGMENTS (AGRADECIMIENTOS) - 15 - Egg mass of Meloidogyne javanica in cucumber root - 16 - Acknowledgments 1.1. - ENGLISH (INGLÉS) Thanks to Prof. Dr. Carolina Escobar, for teaching me within this wonderful world of plant-nematode interaction, I still remember the question that changed my fate the first day that I went to her office to ask if she wanted to lead my degree project: do you know what are nematodes? Carolina thank you very much for supporting me, encouraging me, helping me, talking to me, giving me advices, in brief, for sharing unforgettable moments that they have taught me how as extraordinary is the time on your side. It was not easy the way, but now we look at the fruit of patience, poise, humility and perseverance. Thanks for instilling me these values. Thanks to Prof. Dr. Carmen Fenoll for funding me after my FPU predoctoral grant ending and for her supervision of all my publications where her experience and wisdom has made to improve their contents thereof. Also, thanks to co-research group members Prof. Dr. Montaña Mena and Prof. Dr. Mar Martín and all our external collaborators. Thanks to my host director, Dr. Janice de Almeida-Engler, for endorsing me as a scientist in my early days, back in 2009, collaborating in several of my publications and for opening my mind to new thoughts. In addition, to Dr. Gilbert Engler for teaching me the wonderful world of microscopy with details of difficult understanding but with amazing visualization results. Finally, many thanks to Paulo, Mohammed and Natalia for supporting me in the solitude of the foreigner. Thanks to my village, Mascaraque, for showing me the true quality of life. I am especially grateful to my parents who gave me this wonderful life, and they made me grow in a delightful atmosphere of love and prosperity within the simplicity and humility that I am today. Thanks mom for giving me all your livelihood and love until the last breath. Surely, you are proud of that I have got today. - 17 - Acknowledgments To my father, for teaching me within the agriculture world, my first steps in agronomy. I still remember when we went every afternoon after elementary school to feed the lambs and sheeps at "Corchuelo". Thanks to my girlfriend for putting up with me, trying to understand what I do, explaining to her friends what I work in, filling me with happiness the days of grief and be as patient as science is. Thanks to my brothers, their peeks and support have always helped me to continue this hard and long highway. I would also like to thank to my “big family”, my career mates and my home friends for making me smile, for sharing other moments that perfectly complement scientist life.
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