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Lincoln University Digital Thesis Copyright Statement The digital copy of this thesis is protected by the Copyright Act 1994 (New Zealand). This thesis may be consulted by you, provided you comply with the provisions of the Act and the following conditions of use: you will use the copy only for the purposes of research or private study you will recognise the author's right to be identified as the author of the thesis and due acknowledgement will be made to the author where appropriate you will obtain the author's permission before publishing any material from the thesis. A new approach for delivery of entomopathogenic fungi for plant protection against insect pests and plant diseases via maize seed coating A thesis submitted in partial fulfilment of the requirements for the Degree of Doctor of Philosophy in Plant Protection at Lincoln University by Federico Rivas Franco Lincoln University 2018 Abstract of a thesis submitted in partial fulfilment of the requirements for the Degree of Doctor of Philosophy Abstract A new approach for delivery of entomopathogenic fungi for plant protection against insect pests and plant diseases via maize seed coating by Federico Rivas Franco Entomopathogenic fungi have been recognized mainly for their ability to kill insects which has seen as an advantage for the development of these particular fungi as biocontrol agents in sustainable agriculture programmes. Recently, it was determined that some species of entomopathogenic fungi, including Metarhizium spp., also have the capability to associate with roots and aerial parts of the plant. The potential benefits from the plant-fungal association are as broad as nutrient acquisition, plant growth promotion, protection against biotic or abiotic factors and even increase of the induced defence response in the plant through modification of the phytohormone content. However, many of these the positive effects are uncertain and we are far from understanding the complex interaction between the plant, the fungus and a biotic challenger. Additionally, the establishment of the plant- fungal association relies on the specificity of the fungus and plant interaction. The complex taxon Metarhizium anisopliae had gone through an intense molecular revision, where more than 30 new species of this genus have been described. M. anisopliae, and some other members of the genus such as M. robertsii and M. brunneum, have been described as strongly associated with plants roots, and at the same time with the ability to infect insect pests. Some strains are associated with the rhizosphere and can even colonise the plant as endophytes. One of the main constrains in the use of this type of fungi for the control of soil dwelling insects or pathogens in the agriculture are the contact to the target pest, and the survival of the biocontrol agent in the environment. The soil offers an appropriate environment for fungi, where conditions of moisture and temperature are suitable. This PhD study contributes to the goal of developing improved biological control agents from selected rhizosphere competent, entomopathogenic fungi, delivered efficiently through seed coating. Using molecular approach, isolates of several genera of entomopathogenic fungi were characterised and species assigned based on phylogenetic comparisons. Among the species described, this is the first report of the presence of recently described new species of Metarhizium spp. in New Zealand, such as Metarhizium novozealandicum, M. robertsii, M. brunneum, M. guizhouense and M. frigidum. Presence of specific genes associated with plant and insect colonisation abilities were also determined, to aid ii selection of potential plant associated isolates. In addition, the selection of Metarhizium isolates with the potential to survive in the plant rhizosphere was evaluated for first time by spectrophotometric determination of fungal growth in root exudates. Conidia from the fungal isolates where then used to coat maize seed, to determine the effect of each fungal isolate –plant interaction on plant growth and resistance to insect and disease damage. In presence of the grass grub Costelytra giveni (Coleoptera: Scarabaeidae) and the maize disease fungus, Fusarium graminearum (Ascomycete), some entomopathogenic fungal treatments produced improved growth performance of the maize seedlings. It was also determined the fungal infection of the grass grubs and the decrease in the Fusarium graminearum rot root due to the seed coating with entomopathogenic fungi. Particularly, the M. anisopliae and M. robertsii isolates had significantly higher colonization of the rhizosphere than the other isolates. It was also demonstrated that colonisation of the rhizosphere by M. anisopliae produced changes in the levels of salicylic acid and jasmonic acid when compared to control plants. This is the first report where the effect of M. anisopliae on the content of the phytohormones was evaluated. The seed coating was further developed by replacing fungal conidia with resistant structures known as microsclerotia (MS). Production of these resistant structures in M. guizhouense and M. novozealandicum was evaluated for first time. Maize seeds coated with MS grew better than control plants when grown in presence of F. graminearum. The association between Metarhizium spp and maize roots, after seeds were coated with MS, was possible to determine using fluorescent and laser confocal microscopy. These observations on maize have not been previously published where soil conditions were appropriate for MS germination and hyphae developed along the maize roots which associated with the ecto- and endo-rhizosphere. These studies also confirmed the suitability of using conidia of isolates of Metarhizium transformed with the fluorescent proteins mcherry and GFP to coat maize seeds for the observation of plant colonisation. This is the first report of using a blastospore-based transformation system for M. anisopliae. Overall the results suggest that seed coating with microsclerotia of Metarhizium can be used as delivery system for the control of plant pathogens and insect pests and improve the opportunity for close association with plant roots after conidia germination and hyphal growth. Keywords: Entomopathogenic fungi, endophyte, rhizosphere-competent fungi, Zea mays, Metarhizium spp., microsclerotia, seed coating, bioprotection, plant induced response, biological control agent delivery, fungal characterization, plant root-fungal interaction, biotic stress, Fusarium graminearum, Costelytra giveni iii Acknowledgements Through this acknowledgement, I would like to express my profound appreciation to the many individuals that have supported and encouraged me during the course of my PhD program. First, I am very grateful to my supervisors, Prof. Travis Glare, Prof. John Hampton, Dr Trevor Jackson, Dr Michael Rostas and Dr Per Wessman. It has been their shared skills and vast knowledge, combined with their guidance and enthusiasm that encouraged me to pursue every challenge we came across. I am also very grateful to Dr Nora Altier and Dr Jose Terra for the encouragement to start this great challenge and support during these years. I look forward to contributing to the expertise required in the next challenges that await for us at INIA - Uruguay. I am would like also to thank INIA and ANII from Uruguay for the financial support towards the realization of this PhD. I would like to say a big thanks, to Brian Kwan, Fariba Nourozi, Leila Dadian and Norma Merrick for their enduring helpful disposition to sort out problems and obstacles, leaving all aside to look after my requirements and urgent requests. I am really thankful for your considerable help to make a difficult life science easier. I am also very grateful to Dave Saville for his expertise and support in the statistical analysis. I am also grateful to Dr Maria Moran-Diez for her assistance and guidance in the molecular aspects of this thesis, and Nic Cummings for all the assistance with the molecular identification of the fungal isolates. To my favourite consul, Maria Elena Duter, thank you for your assistance in the germination trials and for bringing me a piece of Uruguay during these long years away from home. Other big thanks to "Las Lolas Locas": Jo Narciso (Mom) and Jenny Brookes. This couple made not only my day at the lab, but they were always kind and helpful help. My special thanks, to “Mom Lab”, for her invaluable assistance in the last months that allow me to run experiments while in the hard stage of writing up the thesis. I am also grateful to Dianne Fyfe who helped with all the process, requirements and formalities for the completion of the PhD during all these years. I am very grateful to my office's mates, Jessica Dunbar and Jessica Yardley, for their cheering up and for all the happy moments we share combined with professionalism and assistance. Specials thanks to the staff and students in the Bioprotection Research Centre, to make a place to work an enjoyable home to be. Special thanks also to Sandy Wilson, for all her help but also for looking after us with treats and tricks to enrich our souls. The professional side it would not be completed if we don't have a family and friends that support us in the hard moments that everyone come through. My sincere gratitude to the "Twisted Minds", my true family everywhere on the world. Finally, I would like to say thanks to my very own family at home, that encouraged me to finish my objectives and pursue the challenges. iv List of acronyms AMF Arbuscular mycorrhizae BPM Between paper method BSM Beauveria selective medium CC Complete coating CFU Colony forming unit ConA-AF633 Concanavalin-A conjugated with Alexa Fluor 633 CS Control seeds DCM Methylene chloride DE Diatomaceous earth DPI Days post inoculation EF Entomopathogenic fungi EF1-α Elongation Factor 1 alpha ET Ethylene GAs Gibberellins GFP Green fluorescent protein IR Induced Resistance ISR Induced Systemic Resistance ITS Internal transcribed spacer JA Jasmonic acid LBA Luria-Bertani Agar LBB Luria-Bertani Broth v LSD Least significant differences MAD1 Metarhizium adhesin protein 1 MAD2 Metarhizium adhesin protein 2 MC Methyl cellulose MEB Malt extract broth MGT Metarhizium clade: M.
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