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Pathogenic and Arbuscular Mycorrhizal Fungi in Potato Fields in Estonia

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Pathogenic and Arbuscular Mycorrhizal Fungi in Potato Fields in Estonia PATHOGENIC AND ARBUSCULAR MYCORRHIZAL FUNGI IN POTATO FIELDS IN ESTONIA PATOGEENSED JA ARBUSKULAARMÜKORIISSED SEENED EESTI KARTULIPÕLDUDEL KAIRE LOIT A Thesis for applying for the degree of Doctor of Philosophy in Agricultural Sciences Väitekiri filosoofiadoktori kraadi taotlemiseks põllumajanduse erialal Tartu 2021 Eesti Maaülikooli doktoritööd Doctoral Theses of the Estonian University of Life Sciences PATHOGENIC AND ARBUSCULAR MYCORRHIZAL FUNGI IN POTATO FIELDS IN ESTONIA PATOGEENSED JA ARBUSKULAARMÜKORIISSED SEENED EESTI KARTULIPÕLDUDEL KAIRE LOIT A Thesis for applying for the degree of Doctor of Philosophy in Agricultural Sciences Väitekiri filosoofiadoktori kraadi taotlemiseks põllumajanduse erialal Tartu 2021 Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences According to verdict No. 6-14/13-2, of May 18, 2021, the Doctoral Committee of Agricultural and Natural Sciences of the Estonian University of Life Sciences has accepted the thesis for the defense for the degree of Doctor of Philosophy in Agriculture. Opponent: Dr. Sari Timonen University of Helsinki Supervisors: Prof. Alar Astover Estonian University of Life Sciences Prof. Leho Tedersoo University of Tartu Prof. Maarja Öpik University of Tartu Reviewer: Dr. Mati Koppel Estonian University of Life Sciences Defense of Estonian University of Life Sciences, room D239, Fr. R. Kreut- the thesis: zwaldi 5, Tartu; International video conference in the BigBlue- Button web room on June 22, 2021, at 10:15. The English language was edited by Ms. Liis Tiir- mann and the Estonian by Dr. Luule Metspalu. Publication of this thesis is supported by the Esto- nian University of Life Sciences and the European Union’s European Regional Development Fund �������������� ��������� (Estonian University of Life Sciences ASTRA project ������������������ �������������� “Value-chain based bio-economy”). ���������������� © Kaire Loit, 2021 ISSN 2382-7076 ISBN 978-9949-698-88-2 (pdf) CONTENTS LIST OF ORIGINAL PUBLICATIONS ....................................... 7 ABBREVIATIONS ......................................................................... 8 1. INTRODUCTION ................................................................. 9 2. LITERATURE REVIEW ......................................................... 13 2.1. Arbuscular mycorrhizal fungi in potato production .......... 13 2.2. Phytopathogenic fungi in potato production .................... 14 2.3. Methods for rapid detection of pathogenic fungi .............. 17 3. AIMS OF THE STUDY .......................................................... 19 4. MATERIALS AND METHODS ............................................. 20 4.1. Study sites ....................................................................... 20 4.2. Sampling .......................................................................... 21 4.3. Assessment of AM fungal root colonization ...................... 22 4.4. Trap plant bioassay ........................................................... 23 4.6. Bioinformatics .................................................................. 24 4.7. Functional assignment ...................................................... 26 4.8. Statistical analyses ............................................................ 26 5. RESULTS ................................................................................. 28 5.1. Potato root AM fungal colonization ................................. 28 5.2. AM fungal inoculum potential in a potato field .............. 28 5.3. Relative abundance of AM fungi in the potato field ......... 30 5.4. Plant genotype, associated pathogens, and potato developmental phase ........................................................ 31 5.5. Pathogenic fungal richness ............................................... 35 5.6. MinION tool for ultrarapid pathogen identification ........ 36 6. DISCUSSION ......................................................................... 39 6.1. Mycorrhizal symbiosis of potato ...................................... 39 6.2. Diversity of soilborne phytopathogenic fungi ................... 40 6.3. Factors affecting the abundance of dominant fungal pathogens ............................................................. 41 6.4. Rapid molecular diagnostics of plant pathogens ............... 43 7. CONCLUSIONS .................................................................... 45 REFERENCES ............................................................................... 47 SUMMARY IN ESTONIAN .......................................................... 67 ACKNOWLEDGMENTS ............................................................. 72 ORIGINAL PUBLICATIONS ..................................................... 73 CURRICULUM VITAE .............................................................. 127 ELULOOKIRJELDUS ................................................................. 130 LIST OF PUBLICATIONS .......................................................... 132 6 LIST OF ORIGINAL PUBLICATIONS The thesis is based on the following studies, presented in papers which are referred to in the text by their Roman numerals: I Loit, K., Soonvald, L., Kukk, M., Astover, A., Runno-Paurson, E., Kaart, T., Öpik, M. (2018). The indigenous arbuscular mycorrhizal fungal colonisation potential in potato roots is affected by agricul- tural treatments. Agronomy Research, 16 (2). DOI: 10.15159/ar. 18.063. II Loit, K., Soonvald, L., Astover, A., Runno-Paurson, E., Öpik, M., Tedersoo, L. (2020). Temporal and Cultivar-Specific Effects on Potato Root and Soil Fungal Diversity. Agronomy, 10 (10), ARTN 1535. DOI: 10.3390/agronomy10101535. III Loit, K., Adamson, K., Bahram, M., Puusepp, R., Anslan, S., Kii- ker, R., Drenkhan, R., Tedersoo, L. (2019). Relative Performance of MinION (Oxford Nanopore Technologies) versus Sequel (Pacific Biosciences) Third-Generation Sequencing Instruments in Identi- fication of Agricultural and Forest Fungal Pathogens. Applied and Environmental Microbiology, 85 (21), ARTN e01368-19. DOI: 10.1128/AEM.01368-19. The contribution of Kaire Loit to the papers was the following: Paper Idea and study Experiments Data analysis Manuscript writing design I ERP, MÖ ERP, MK, MÖ KL, LS, TK AA, ERP, KL, LS, MÖ, TK II ERP, KL, LS, ERP, KL, LS AA, ERP, KL, AA, ERP, KL, LS, LT, MÖ LS, LT, MÖ LT, MÖ III 1 KA, KL, LT, KA, KL, LT, KA, KL, LT, KA, KL, LT, MB, MB, RP MB, RP MB, RP RD, RK, RP, SA AA – Alar Astover; ERP – Eve Runno-Paurson; KA – Kalev Adamson; KL – Kaire Loit; LS – Liina Soonvald; LT – Leho Tedersoo; MB – Mohammad Bahram; MK – Martin Kukk; MÖ – Maarja Öpik; RD – Rein Drenkhan; RK – Rasmus Puusepp; RP – Rasmus Puusepp; SA – Sten Anslan; TK – Tanel Kaart. 1 Only the MinION-based identification of agricultural pathogens is handled within this thesis. 7 ABBREVIATIONS AM fungi . Arbuscular mycorrhizal fungi BBCH-scale . Decimal scale of plant growth stages BEM . Before emergence CC . Cover crop cDNA . Complementary DNA CFS . Conventional farming system Corg . Organic carbon DNA . Deoxyribonucleic acid FL . Flowering GLM . Generalized linear model HCL . Hydrochloric acid HTS . High-throughput sequencing IP . Inoculum potential IPM . Integrated pest management KOH . Potassium hydroxide LAMP . Loop-mediated isothermal amplification M . Manure N . Nitrogen NS . Not significant OFS . Organic farming system OTU . Operational taxonomic unit P . Phosphorus PCR . Polymerase chain reaction qPCR . Quantitative polymerase chain reaction RNA . Ribonucleic acid SSC . Senescence 8 1. INTRODUCTION Soil fungi have fundamental ecological roles as decomposers, mutualists, or pathogens of plants. Roots of agricultural crops are hosts of different microorganisms. These include many harmful, often soilborne, patho- gens, as well as beneficial organisms, such as plant growth and health-pro- moting arbuscular mycorrhizal (AM) fungi (Smith and Read 2008). In agroecosystems, fungal plant diseases can be a major limitation determin- ing agricultural productivity (Raaijmakers et al. 2009). Diseases caused by soilborne plant pathogens tend to produce only one infection cycle per host cycle, the infection starts when the roots of the newly planted crop encounter the propagules of the pathogen embedded in the soil. Therefore, soilborne fungal pathogens are challenging to manage, as they can remain in the soil for years (Bebber et al. 204). The most important group of beneficial soil fungi in agricultural soils are AM fungi that play vital roles in improving plant performance (Frac et al. 208; Smith and Read 2008) and protecting plants against soilborne pathogens (Pozo et al. 205; Thirkell et al. 207; Whipps 2004). In agricultural fields, benefi- cial and detrimental microbial communities are affected by several abi- otic factors like soil type (Berg and Smalla 2009; Tkacz et al. 2020), pH (Soonvald et al. 2020; Tedersoo et al. 204; Tedersoo et al. 2020 a), and biotic factors such as plant developmental stage (Hannula et al. 202; Jia et al. 2020), plant health (Ginnan et al. 2020), as well as anthropogenic factors like crop rotation (Detheridge et al. 206), agricultural practices (Benitez et al. 206; Sharma-Poudyal et al. 207), fertilization (Geisseler and Scow 204), and pesticide application (Kalia and Gosal 20), but crop selection of its fungal community in agroecosystems remains poorly understood. Potato (Solanum tuberosum L.) ranks first as a non-cereal food crop for human consumption worldwide (FAO 2009). According to FAO (2009), the average global potato consumption per capita per year reached
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