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Systematics, Ecology and Plant Associations of Australian Species of the Genus Metarhizium

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Systematics, Ecology and Plant Associations of Australian Species of the Genus Metarhizium SYSTEMATICS, ECOLOGY AND PLANT ASSOCIATIONS OF AUSTRALIAN SPECIES OF THE GENUS METARHIZIUM Shah Mohammad Naimul Islam MS in Biotechnology Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Earth, Environmental and Biological Sciences Science and Engineering Faculty Queensland University of Technology 2018 Keywords Australia, ecology, endophyte, entomopathogen, haplotype, Metarhizium, MzIGS3, new species, plant associations, Queensland, rhizosphere, strigolactone, systematics, 5’-TEF. i Abstract Fungi of the genus Metarhizium (Family: Clavicipitaceae, Order: Hypocreales) are pleomorphic entomopathogens that are widely used as biocontrol agents. As with many Hypocrealean fungi, they are saprophytes in soil and colonisers of the rhizosphere in a mutualistic relationship with plants that can result in improved plant growth, nutrient uptake, protection from invertebrate herbivores and suppression of plant pathogens. Inoculation of the rhizosphere of crops with Hypocrealean fungi may have significant benefits to agriculture, but establishment of fungal inoculum in the rhizosphere has been inconsistent. Establishment might be improved by analysis of the biological and ecological factors in the plant/fungus relationship, and the identification of strains or species with improved rhizospheric competence in crops. This study collected and described Metarhizium isolates from agricultural fields, grasslands and forests soils in three locations in Queensland, Australia. Multi-locus analysis of concatenated sequence data sets of MzIGS3 and 5’-TEF sequences was used to determine the systematic relationships of 164 Metarhizium isolates. Five clades with strong support values were identified: three known species (M. robertsii, M. pingshaense and M. anisopliae) and two previously unidentified ‘indeterminate’ clades (provisionally annotated as M. indet. 1 and M. indet 2). Systematic and population genetic analyses indicated strongly that the two indeterminate clades represent two new Metarhizium species. Moderate genetic differences and gene flow were observed between populations from different locations and ecotypes. Factors that might affect the diversity of Metarhizium species in soils of different ecotypes, crops and locations were analysed using multivariate and univariate analyses. The distribution of Metarhizium species varied with location, ecotype and crop. The reconstructed phylogenetic relationships, population and ecological analyses of Metarhizium isolates from soil in legume and maize fields identified associations between specific clades with legume and maize crops. M. anisopliae and ii M. robertsii isolates were significantly associated with soil from legume crops and forests, and with higher nitrogen and carbon content in soil. Isolates of the M. indet. 1 clade were associated with maize and grassland soils and with low nitrogen and carbon content. The isolates of M. robertsii and M. indet. 1 were more abundant in iron rich soil. There was no relationship between phosphate and occurrence of any species. The relationship of isolates with legumes and maize plants was investigated. M. robertsii, M. anisopliae, M. pingshaense were found to be abundant in soils of legume crops, whereas the 2 new taxonomic clades M. indet. 1 and M. indet. 2 were only isolated only from soils in which maize had been recently grown. Colonisation of pea and maize roots was quantified for six fungal isolates from legume crops and six isolates from maize. Colonisation of pea roots was significantly higher than those of maize for all isolates, but isolates differed significantly in their colonisation of roots of the two plant types. The results support the proposal that the host plant influences both the Metarhizium species found in soil and colonisation of the plant roots. Finally, the effect of the plant hormone strigolactone on early stages in root colonisation by M. anisopliae was examined indirectly, through exposure to selected pea mutants with differing levels of strigolactone expression. Conidium germination in root exudates, and fungal colony forming units on the roots, were compared in wild type pea (Pisum sativum L. cv Torsdag) and two pea mutants, rms 5-3 ‘strigolactone deficient’, and rms 4-1 ‘strigolactone overproducing’ mutants. Plant varieties with known higher production of strigolactone resulted in increase in both conidium germination and root colonisation by Metarhizium. These research findings suggest that selection of Metarhizium species or strains may enhance the establishment of beneficial inocula in the rhizosphere of crops. iii Table of Contents KEYWORDS.................................................................................................................................. I ABSTRACT................................................................................................................................... II TABLE OF CONTENTS ........................................................................................................... IV LIST OF FIGURES .................................................................................................................... VI LIST OF TABLES ...................................................................................................................... IX LIST OF ABBREVIATIONS .................................................................................................... XI STATEMENT OF ORIGINAL AUTHORSHIP .................................................................. XII ACKNOWLEDGEMENTS .................................................................................................... XIII CHAPTER 1 : GENERAL INTRODUCTION ....................................................................... 1 1.1 INTRODUCTION AND BACKGROUND ............................................................................................................. 2 1.2 AIMS AND OUTLINE OF THIS THESIS ............................................................................................................. 4 CHAPTER 2 : LITERATURE REVIEW ................................................................................ 6 2.1 THE ENTOMOPATHOGENIC FUNGI OF THE GENUS METARHIZIUM. ....................................................... 7 2.2 TAXONOMY OF METARHIZIUM ....................................................................................................................... 9 2.3 METARHIZIUM ABUNDANCE ........................................................................................................................ 15 2.4 SOIL AND ENVIRONMENTAL FACTORS AFFECTING METARHIZIUM ABUNDANCE ........................... 15 2.5 METARHIZIUM, A RHIZOSPHERE ASSOCIATE ........................................................................................... 16 2.7 SIGNALLING DURING COLONISATION OF THE RHIZOSPHERE .............................................................. 19 2.8 SUMMARY ........................................................................................................................................................ 20 CHAPTER 3 : SYSTEMATICS OF AUSTRALIAN METARHIZIUM ISOLATES ...... 21 ABSTRACT ............................................................................................................................................................... 22 3.1 INTRODUCTION ............................................................................................................................................... 23 3.2 MATERIALS AND METHODS ........................................................................................................................ 27 3.2.1 Collection of soil samples .............................................................................................................. 27 3.2.2 Isolation of fungal isolates ........................................................................................................... 27 3.2.3 Genomic DNA extraction, PCR amplification, and sequencing .................................... 28 3.2.4 Phylogenetic tree construction .................................................................................................. 30 3.2.6 Haplotype distribution analysis ................................................................................................. 33 3.2.7 Statistical analysis ........................................................................................................................... 34 3.3 RESULTS ........................................................................................................................................................... 35 3.3.1 Occurrence of Metarhizium isolates ........................................................................................ 35 3.3.2 ITS phylogeny ..................................................................................................................................... 39 3.3.3 Phylogenetic analysis...................................................................................................................... 39 3.3.4 DNA divergence, genetic differentiation and gene flow ................................................. 46 3.3.5. Haplotype analysis .......................................................................................................................... 52 3.4 DISCUSSION ..................................................................................................................................................... 59 3.7 SUPPLEMENTARY DATA ..............................................................................................................................
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