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ASSESSMENT of Verticillium Dahliae Kleb. and SOIL FUNGAL COMMUNITIES ASSOCIATED with STRAWBERRY FIELDS

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ASSESSMENT of Verticillium Dahliae Kleb. and SOIL FUNGAL COMMUNITIES ASSOCIATED with STRAWBERRY FIELDS ASSESSMENT OF Verticillium dahliae Kleb. AND SOIL FUNGAL COMMUNITIES ASSOCIATED WITH STRAWBERRY FIELDS MAASIKA PATOGEENI Verticillium dahliae Kleb. JA MULLA SEENEKOOSLUSTE ISELOOMUSTAMINE MAASIKAPÕLDUDEL SEYED MAHYAR MIRMAJLESSI A Thesis for applying for the degree of Doctor of Philosophy in Agriculture Väitekiri filosoofiadoktori kraadi taotlemiseks põllumajanduse erialal Tartu 2017 Eesti Maaülikooli doktoritööd Doctoral Theses of the Estonian University of Life Sciences ASSESSMENT OF Verticillium dahliae Kleb. AND SOIL FUNGAL COMMUNITIES ASSOCIATED WITH STRAWBERRY FIELDS MAASIKA PATOGEENI Verticillium dahliae Kleb. JA MULLA SEENEKOOSLUSTE ISELOOMUSTAMINE MAASIKAPÕLDUDEL SEYED MAHYAR MIRMAJLESSI A Thesis for applying for the degree of Doctor of Philosophy in Agriculture Väitekiri filosoofiadoktori kraadi taotlemiseks põllumajanduse erialal Tartu 2017 Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences According to the verdict No 6-14/5-8, the Doctoral Committee of the Agricul- tural Sciences of the Estonian University of Life Sciences has accepted this dis- sertation for the defense of the degree of Doctor of Philosophy in Agriculture. Opponent: Professor Franco Nigro, PhD University of Bari, Department of Soil, Plant, and Food Sciences, Bari, Italy Reviewers: Professor Michael Starzycki, PhD Institute of Plant Breeding and Acclimatization-National Research, Department of Genetics and Plant Breeding, Poznan, Poland Professor Anders Kvarnheden, PhD Swedish University of Agricultural Sciences, Department of Plant Pathology, Uppsala, Sweden Supervisors: Professor Marika Mänd, PhD Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences. Department of Plant Protection, Tartu, Estonia Senior researcher Evelin Loit, PhD Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Department of Field Crops and Grass- land Husbandry, Tartu, Estonia Defense of this dissertation: Estonian University of Life Sciences, room D239, Kreutzwaldi 5, Tartu on June 20, 2017 at 10:15am. The English language in the current dissertation was edited by Dr. Ingrid H. Williams and the Estonian by Dr. Evelin Loit and Dr. Luule Metspalu. Publication of this dissertation is supported by the Estonian University of Life Sciences, Ministry of Education and Research and the Doctoral School of Earth Sciences and Ecology. © Seyed Mahyar Mirmajlessi, 2017 ISBN 978-9949-569-85-4 (trükis) ISBN 978-9949-569-86-1 (pdf) ISSN 2382-7076 Contents LIST OF ORIGINAL PUBLICATIONS ......................................... 7 ABBREVIATIONS ........................................................................... 9 1. INTRODUCTION ................................................................. 10 2. REVIEW OF THE LITERATURE .......................................... 14 2.1 Soil fungi ......................................................................... 14 2.1.1 Functional groups of soil fungi ................................ 14 2.1.2 Taxonomic groups of soil fungi ............................... 15 2.2 Soil-borne pathogens ........................................................ 15 2.2.1 Strawberry and associated important diseases .......... 16 2.2.2 Verticillium wilt caused by Verticillium dahliae ........ 17 2.2.3 Life cycle of V. dahliae ............................................. 18 2.3 Pathogen detection ........................................................... 18 2.3.1 Conventional methods ............................................ 19 2.3.2 Molecular technologies ............................................ 19 2.3.3 PCR-based techniques (I) ........................................ 20 2.3.4 Real-time PCR (II) .................................................. 20 2.4 Assessment of soil fungal diversity .................................... 21 2.5 Assessment of soil fungi by next-generation sequencing .... 22 2.6 Control of Verticillium wilt ............................................. 22 3. HYPOTHESES AND AIMS OF THE STUDY ...................... 24 4. MATERIALS AND METHODS ............................................. 26 4.1 Systematic review of PCR-based techniques (I) ................ 26 4.2 Sample collecting ............................................................. 27 4.2.1 Isolation of fungi − culture-based method ............... 29 4.2.2 Fungal cultures (III, IV) .......................................... 30 4.3 Pathogenicity test (VI) ..................................................... 30 4.4 Detection of soil fungi − PCR-based methods (III, IV) .... 30 4.4.1 DNA extraction ...................................................... 30 4.4.2 Conventional PCR ................................................. 31 4.4.3 Primer design ......................................................... 31 4.4.4 Real-time PCR ....................................................... 32 4.4.5 Standard curve ....................................................... 32 4.4.6 Spike test (IV) ......................................................... 32 4.5 Characterization of soil fungal communities – Illumina sequencing (V) ................................................................ 33 5 4.6 Biocontrol of Verticillium wilt (VI) .................................. 33 4.6.1 Antagonistic ability of T. harzianum on V. dahliae – in vitro .......................................................... 33 4.6.2 Antagonistic ability of T. harzianum on V. dahliae – in vivo .......................................................... 34 4.6.3 Antagonistic ability of G. catenulatum on V. dahliae – in vitro .......................................................... 34 4.7 Bioinformatics and statistical analyses .............................. 34 5. RESULTS ................................................................................. 35 5.1 Soil fungi ......................................................................... 35 5.1.1 Isolation of pathogens and antagonist ..................... 35 5.1.2 Detection and quantification of V. dahliae in field soils (III, IV) .................................................................... 35 5.1.3 Validation of detection protocol by spike assay (IV) 36 5.1.4 Characterization of fungal communities in soil − Illumina sequencing (V) ................................................... 36 5.2 Biological control of Verticillium wilt (VI) ....................... 37 5.2.1 Pathogenicity test (VI) ............................................ 37 5.2.2 Antagonistic ability of T. harzianum on V. dahliae – in vitro .......................................................... 37 5.2.3 Antagonistic ability of T. harzianum on V. dahliae – in vivo .......................................................... 37 5.2.4 Antagonistic ability of G. catenulatum on V. dahliae – in vitro .......................................................... 38 6. DISCUSSION ......................................................................... 39 6.1 Detection and quantification of V. dahliae in strawberry plants and field soils (III, IV) .......................................... 39 6.2 Characterization of fungal communities in soil (V) .......... 40 6.3 Biological control of Verticillium wilt (VI) ....................... 42 7. CONCLUSIONS .................................................................... 45 REFERENCES ............................................................................... 48 SUMMARY IN ESTONIAN .......................................................... 63 ACKNOWLEDGEMENTS ........................................................... 68 ORIGINAL PUBLICATIONS ....................................................... 71 CURRICULUM VITAE ............................................................... 145 ELULOOKIRJELDUS ................................................................. 148 LIST OF PUBLICATIONS .......................................................... 151 6 LIST OF ORIGINAL PUBLICATIONS This dissertation is based on the following papers; the references to the papers are given in Roman numerals in the text. The papers are repro- duced by kind permission of the journals. I Mirmajlessi SM, Destefanis M, Gottsberger RA, Mänd M, Loit E, 2015. PCR-based specific techniques used for detecting the most important pathogens on strawberry: a systematic review. Systematic Reviews 4, 9. II Mirmajlessi SM, Loit E, Mänd M, Mansouripour SM, 2015. Real- time PCR applied to study on plant pathogens: potential applica- tions in diagnosis. Plant Protection Science 51(4), 177–190. III Mirmajlessi SM, Larena I, Mänd M, Loit E, 2016. First report on the detection and quantification of Verticillium dahliae from Esto- nian strawberry fields using quantitative real-time PCR. Zemdir byste- Agriculture 103(1), 115–118. IV Mirmajlessi SM, Larena I, Mänd M, Loit E, 2016. A rapid diag- nostic assay for detection and quantification of the causal agent of strawberry wilt from field samples. Acta Agriculturae Scandinavica, Section B — Soil & Plant Science 66(7), 619–629. V Mirmajlessi SM, Bahram M, Mänd M, Mansouripour SM, Loit E, 2017. Survey of soil fungal communities in strawberry fields by Illumina amplicon sequencing. European Journal of Plant Pathology, Under Review. VI Mirmajlessi SM, Mänd M, Najdabbasi N, Larena I, Loit E, 2016. Screening of native Trichoderma harzianum isolates for their ability to control Verticillium wilt of strawberry. Zemdirbyste-Agriculture 103(4), 397–404. 7 The contributions from the authors to the papers are as follows: Idea and Sampling
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