ORCID Profile
0000-0003-0514-8146
Current Organisation
Western Sydney University
Does something not look right? The information on this page has been harvested from data sources that may not be up to date. We continue to work with information providers to improve coverage and quality. To report an issue, use the Feedback Form.
In Research Link Australia (RLA), "Research Topics" refer to ANZSRC FOR and SEO codes. These topics are either sourced from ANZSRC FOR and SEO codes listed in researchers' related grants or generated by a large language model (LLM) based on their publications.
Mycology | Soil Biology | Microbiology |
Forest and Woodlands Flora, Fauna and Biodiversity | Ecosystem Assessment and Management of Forest and Woodlands Environments
Publisher: Wiley
Date: 04-06-2016
DOI: 10.1111/PCE.12757
Abstract: Breeding disease-resistant varieties is one of the most effective and economical means to combat soilborne diseases in pulse crops. Commonalities between pathogenic and mutualistic microbe colonization strategies, however, raises the concern that reduced susceptibility to pathogens may simultaneously reduce colonization by beneficial microbes. We investigate here the degree of overlap in the transcriptional response of the Phytophthora medicaginis susceptible chickpea variety 'Sonali' to the early colonization stages of either Phytophthora, rhizobial bacteria or arbuscular mycorrhizal fungi. From a total of 6476 genes differentially expressed in Sonali roots during colonization by any of the microbes tested, 10.2% were regulated in a similar manner regardless of whether it was the pathogenic oomycete or a mutualistic microbe colonizing the roots. Of these genes, 49.7% were oppositely regulated under the same conditions in the moderately Phytophthora resistant chickpea variety 'PBA HatTrick'. Chickpea varieties with improved resistance to Phytophthora also displayed lower colonization by rhizobial bacteria and mycorrhizal fungi leading to an increased reliance on N and P from soil. Together, our results suggest that marker-based breeding in crops such as chickpea should be further investigated such that plant disease resistance can be tailored to a specific pathogen without affecting mutualistic plant:microbe interactions.
Publisher: Springer Netherlands
Date: 2012
Publisher: Elsevier BV
Date: 07-2023
Publisher: Wiley
Date: 11-07-2022
Abstract: Fungivory of mycorrhizal hyphae has a significant impact on fungal fitness and, by extension, on nutrient transfer between fungi and host plants in natural ecosystems. Mycorrhizal fungi have therefore evolved an arsenal of chemical compounds that are hypothesized to protect the hyphal tissues from being eaten, such as the protease inhibitors mycocypins. The genome of the ectomycorrhizal fungus Laccaria bicolor has an unusually high number of mycocypin-encoding genes. We have characterized the evolution of this class of proteins, identified those induced by symbiosis with a host plant and characterized the biochemical properties of two upregulated L. bicolor mycocypins. More than half of L. bicolor mycocypin-encoding genes are differentially expressed during symbiosis or fruiting body formation. We show that two L. bicolor mycocypins that are strongly induced during symbiosis are cysteine protease inhibitors and exhibit similar but distinct localization in fungal tissues at different developmental stages and during interaction with a host plant. Moreover, we show that these L. bicolor mycocypins have toxic and feeding deterrent effect on nematodes and collembolans, respectively. Therefore, L. bicolor mycocypins may be part of a mechanism by which this species deters grazing by different members of the soil food web.
Publisher: Oxford University Press (OUP)
Date: 22-02-2023
Abstract: The mutualistic ectomycorrhizal (ECM) fungal genus Pisolithus comprises 19 species defined to date which colonize the roots of & hosts worldwide suggesting that substantial genomic and functional evolution occurred during speciation. To better understand this intra-genus variation, we undertook a comparative multi-omic study of nine Pisolithus species s led from North America, South America, Asia, and Australasia. We found that there was a small core set of genes common to all species (13%), and that these genes were more likely to be significantly regulated during symbiosis with a host than accessory or species-specific genes. Thus, the genetic “toolbox” foundational to the symbiotic lifestyle in this genus is small. Transposable elements were located significantly closer to gene classes including effector-like small secreted proteins (SSPs). Poorly conserved SSPs were more likely to be induced by symbiosis, suggesting that they may be a class of protein that tune host specificity. The Pisolithus gene repertoire is characterized by ergent CAZyme profiles when compared with other fungi, both symbiotic and saprotrophic. This was driven by differences in enzymes associated with symbiotic sugar processing, although metabolomic analysis suggest that neither copy number nor expression of these genes is sufficient to predict sugar capture from a host plant or its metabolism in fungal hyphae. Our results demonstrate that intra-genus genomic and functional ersity within ECM fungi is greater than previously thought, underlining the importance of continued comparative studies within the fungal tree of life to refine our focus on pathways and evolutionary processes foundational to this symbiotic lifestyle.
Publisher: Springer Science and Business Media LLC
Date: 09-03-2017
Publisher: Scientific Societies
Date: 03-2015
DOI: 10.1094/MPMI-05-14-0129-FI
Abstract: The coordinated transcriptomic responses of both mutualistic ectomycorrhizal (ECM) fungi and their hosts during the establishment of symbiosis are not well-understood. This study characterizes the transcriptomic alterations of the ECM fungus Laccaria bicolor during different colonization stages on two hosts (Populus trichocarpa and Pseudotsuga menziesii) and compares this to the transcriptomic variations of P. trichocarpa across the same timepoints. A large number of L. bicolor genes (≥8,000) were significantly regulated at the transcriptional level in at least one stage of colonization. From our data, we identify 1,249 genes that we hypothesize is the ‘core’ gene regulon necessary for the mutualistic interaction between L. bicolor and its host plants. We further identify a group of 1,210 genes that are regulated in a host-specific manner. This variable regulon encodes a number of genes coding for proteases and xenobiotic efflux transporters that we hypothesize act to counter chemical-based defenses simultaneously activated at the transcriptomic level in P. trichocarpa. The transcriptional response of the host plant P. trichocarpa consisted of differential waves of gene regulation related to signaling perception and transduction, defense response, and the induction of nutrient transfer in P. trichocarpa tissues. This study, therefore, gives fresh insight into the shifting transcriptomic landscape in both the colonizing fungus and its host and the different strategies employed by both partners in orchestrating a mutualistic interaction.
Publisher: Proceedings of the National Academy of Sciences
Date: 20-05-2014
Abstract: Plants use the hormone jasmonic acid (JA) to modulate plant:microbe interactions. Disease-causing microbes use proteins to alter host JA signaling to aid their growth in plant tissues. Beneficial symbiotic fungi, which colonize plant tissues and provide essential ecosystem services such as carbon sequestration and plant fertilization, can also alter JA signaling in plant cells to promote colonization. Here, we demonstrate that the MiSSP7 (Mycorrhiza-induced small secreted protein-7) protein of the beneficial fungus Laccaria bicolor interacts with host plant JA signaling repressors and, in contrast to biotrophic pathogens, promotes symbiosis by blocking JA action. These results shed new light on how beneficial and pathogenic microbes have evolutionarily erged in the mechanisms by which they overcome plant defenses.
Publisher: Informa UK Limited
Date: 02-10-2022
Publisher: Oxford University Press (OUP)
Date: 31-07-2009
DOI: 10.1093/JXB/ERP228
Publisher: Wiley
Date: 09-02-2010
Publisher: Cold Spring Harbor Laboratory
Date: 09-12-2021
DOI: 10.1101/2021.12.07.471680
Abstract: Heirloom golden tomato fruit varieties are highly nutritious as they accumulate tetra- cis -lycopene, which has a higher bioavailability and recognised health benefits in treating anti-inflammatory diseases compared to all- trans -lycopene isomers found in red tomatoes. We investigated if photoisomerization of tetra- cis -lycopene occurs in roots of the golden tangerine Micro-Tom variety ( tang mic ), and how this affects root to shoot biomass, mycorrhizal colonization, abscisic acid accumulation, and responses to drought. tang mic plants grown in soil under glasshouse conditions displayed a reduction in height, number of flowers, fruit yield, and root length compared to wild type (WT). Soil inoculation with Rhizophagus irregularis revealed fewer arbuscules and other fungal structures in the endodermal cells of roots in tang mic relative to WT. The roots of tang mic hyperaccumulated acyclic cis -carotenes, while only trace levels of xanthophylls and abscisic acid were detected. In response to a water deficit, leaves from the tang mic plants displayed a rapid decline in maximum quantum yield of photosystem II compared to WT, indicating a defective root to shoot signalling response to drought. The lack of xanthophylls biosynthesis in tang mic roots reduced abscisic acid levels, thereby likely impairing endomycorrhiza colonisation and drought-induced root to shoot signalling. Photoisomerization of prolycopene to lycopene is limited in root plastids. Roots of tangerine reveal an important tissue sink to store micronutrients such as prolycopene. Roots of tangerine lack ABA and show impaired mycorrhizal colonization. The tangerine plant is drought sensitive and has a smaller biomass as well as reduced yield.
Publisher: Humana Press
Date: 2011
DOI: 10.1007/978-1-61779-040-9_19
Abstract: Given recent technological advances, we are in a golden era of cell and whole organism research. With the availability of so many sequenced genomes, and the data that has been mined there-in, it is easy to gain the impression that all our work as scientists is complete. Instead, such work and results have now provided oceans of data, but with minimal functional information. We also do not have a full grasp on the working relationships within a number of different plant developmental pathways. This is especially true in the study of the symbiotic interaction between ectomycorrhizal fungi and their plant hosts. One of the current interests in symbiotic and pathogenic interactions between plants and fungi is the role of small, secreted proteins. What makes fungal small secreted proteins so interesting is that only a few of them share sequence homology to any other known proteins, but some may act as effectors modulating plant metabolism and development. Therefore, it is difficult to make predictions as to the action of these proteins without functional analysis. For this reason, we created a pipeline to analyze the role and function of these proteins. Typically, this involves transcriptional analysis of genes followed by protein localization, identification of protein-protein interactions, and functional analysis of the protein through heterologous expression in yeast among many other different procedures. Due to the physiology of mycorrhizal root tips, there are a number of unique challenges that must be overcome to properly study a fungal effector. Here, we outline some of the methods, and hopefully helpful tips, that we are currently using to pursue the study of different effectors in the Laccaria-Populus interaction.
Publisher: Springer Science and Business Media LLC
Date: 05-2004
DOI: 10.1007/S00216-004-2583-4
Abstract: beta-1,3- D-Glucan is a biologically active component mainly from fungi that has been shown in several studies to be related to respiratory health outcomes from d building exposures. Here, we report the development and application of a method for the analysis of the glucan extracted in 0.5 N NaOH solution making use of an available preparation of Limulus amebocyte lysate (LAL). The method yields reproducible beta-1,3- D-glucan measurements from s les of outdoor air, yeast cells, fungal spore preparations and ragweed pollen, and is more sensitive than competing measurements. The LAL-based measurement compared favourably to that based on size-exclusion chromatography using UV and refractive index detection. Growth conditions of the fungi did not materially change the concentrations of glucan in spores indicating that this is a stable property. Glucan content was proportional to spore surface area however, some species contain higher relative spore glucan contents.
Publisher: Elsevier BV
Date: 03-2023
Publisher: Cold Spring Harbor Laboratory
Date: 19-01-2023
DOI: 10.1101/2023.01.16.524162
Abstract: Plant community bio ersity can be maintained, at least partially, by shifts in species interactions between facilitation and competition for resources as environmental conditions change. These interactions also drive ecosystem functioning, including productivity, and can promote over-yielding-an ecosystem service prioritized in working landscapes that occurs when there is either less competition, more facilitation, or both, between species in a community than within species. Importantly, shifts in species interactions that can result in over-yielding are unclear given rising CO 2 concentrations, especially in the context of tropical mixed-species grasslands. We examined the relative performance of two species pairs of tropical pasture grasses and legumes growing in monoculture and mixtures in a glasshouse experiment manipulating CO 2 . We investigated how over-yielding can arise from nitrogen (N) niche partitioning and biotic facilitation using stable isotopes to differentiate soil N from biological N fixation (BNF) within N acquisition into aboveground biomass for these two-species mixtures. We found that N niche partitioning in species-level use of soil N vs. BNF drove species interactions in mixtures. Importantly partitioning, though not necessarily overyielding, was generally enhanced under elevated CO 2 . However, this finding was mixture-dependent based on biomass of dominant species in mixtures and the strength of selection effects for the dominant mixture species. This study demonstrates that rising atmospheric CO 2 may alter niche partitioning between co-occurring species, with negative implications for the over-yielding benefits predicted for legume-grass mixtures in working landscapes with tropical species. Furthermore, these changes in inter-species interactions have consequences for shifts in grassland composition that are not yet considered in larger-scale projections for impacts of climate change and species distributions. Among our tropical pasture species we found that grasses (dotted lines) grown in monoculture rely fully on soil nitrogen (N), while legumes (solid lines) grown in monoculture relied approximately equally on soil N and biological nitrogen fixation (BNF) to meet N requirements. When grown with tropical grasses, however, legumes shifted to rely more strongly on BNF, indicative of niche partitioning and decreased competition for soil nutrients with grasses. This separation of niche space was strengthened under elevated CO 2 conditions, ultimately reducing legume production.
Publisher: Wiley
Date: 23-09-2020
DOI: 10.1111/NPH.16759
Abstract: Pathogenic microbes are known to manipulate the defences of their hosts through the production of secreted effector proteins. More recently, mutualistic mycorrhizal fungi have also been described as using these secreted effectors to promote host colonization. Here we characterize a mycorrhiza‐induced small secreted effector protein of 10 kDa produced by the ectomycorrhizal fungus Pisolithus albus , PaMiSSP10b. We demonstrate that PaMiSSP10b is secreted from fungal hyphae, enters the cells of its host, Eucalyptus grandis, and interacts with an S‐adenosyl methionine decarboxylase (AdoMetDC) in the polyamine pathway. Plant polyamines are regulatory molecules integral to the plant immune system during microbial challenge. Using biochemical and transgenic approaches we show that expression of PaMiSSP10b influences levels of polyamines in the plant roots as it enhances the enzymatic activity of AdoMetDC and increases the biosynthesis of higher polyamines. This ultimately favours the colonization success of P. albus . These results identify a new mechanism by which mutualistic microbes are able to manipulate the host´s enzymatic pathways to favour colonization.
Publisher: Elsevier BV
Date: 2009
Publisher: Scientific Societies
Date: 06-2014
DOI: 10.1094/MPMI-09-13-0286-R
Abstract: Within boreal and temperate forest ecosystems, the majority of trees and shrubs form beneficial relationships with mutualistic ectomycorrhizal (ECM) fungi that support plant health through increased access to nutrients as well as aiding in stress and pest tolerance. The intimate interaction between fungal hyphae and plant roots results in a new symbiotic “organ” called the ECM root tip. Little is understood concerning the metabolic reprogramming that favors the formation of this hybrid tissue in compatible interactions and what prevents the formation of ECM root tips in incompatible interactions. We show here that the metabolic changes during favorable colonization between the ECM fungus Laccaria bicolor and its compatible host, Populus trichocarpa, are characterized by shifts in aromatic acid, organic acid, and fatty acid metabolism. We demonstrate that this extensive metabolic reprogramming is repressed in incompatible interactions and that more defensive compounds are produced or retained. We also demonstrate that L. bicolor can metabolize a number of secreted defensive compounds and that the degradation of some of these compounds produces immune response metabolites (e.g., salicylic acid from salicin). Therefore, our results suggest that the metabolic responsiveness of plant roots to L. bicolor is a determinant factor in fungus–host interactions.
Publisher: Springer Science and Business Media LLC
Date: 28-06-2022
DOI: 10.1038/S43705-022-00139-Y
Abstract: The last few years have seen significant advances in the breadth of fungi for which we have genomic resources and our understanding of the biological mechanisms evolved to enable fungi to interact with their environment and other organisms. One field of research that has seen a paradigm shift in our understanding concerns the role of fungal small secreted proteins (SSPs) classified as effectors. Classically thought to be a class of proteins utilized by pathogenic microbes to manipulate host physiology in support of colonization, comparative genomic studies have demonstrated that mutualistic fungi and fungi not associated with a living host (i.e., saprotrophic fungi) also encode inducible effector and candidate effector gene sequences. In this review, we discuss the latest advances in understanding how fungi utilize these secreted proteins to colonize a particular niche and affect nutrition and nutrient cycles. Recent studies show that candidate effector SSPs in fungi may have just as significant a role in modulating hyphosphere microbiomes and in orchestrating fungal growth as they do in supporting colonization of a living host. We conclude with suggestions on how comparative genomics may direct future studies seeking to characterize and differentiate effector from other more generalized functions of these enigmatic secreted proteins across all fungal lifestyles.
Publisher: Frontiers Media SA
Date: 04-11-2014
Publisher: Elsevier BV
Date: 03-2012
DOI: 10.1016/J.FGB.2012.01.002
Abstract: Hydrophobins are morphogenetic, small secreted hydrophobic fungal proteins produced in response to changing development and environmental conditions. These proteins are important in the interaction between certain fungi and their hosts. In mutualistic ectomycorrhizal fungi several hydrophobins form a subclass of mycorrhizal-induced small secreted proteins that are likely to be critical in the formation of the symbiotic interface with host root cells. In this study, two genomes of the ectomycorrhizal basidiomycete Laccaria bicolor strains S238N-H82 (from North America) and 81306 (from Europe) were surveyed to construct a comprehensive genome-wide inventory of hydrophobins and to explore their characteristics and roles during host colonization. The S238N-H82 L. bicolor hydrophobin gene family is composed of 12 genes while the 81306 strain encodes nine hydrophobins, all corresponding to class I hydrophobins. The three extra hydrophobin genes encoded by the S238N-H82 genome likely arose via gene duplication and are bordered by transposon rich regions. Expression profiles of the hydrophobin genes of L. bicolor varied greatly depending on life stage (e.g. free living mycelium vs. root colonization) and on the host root environment. We conclude from this study that the complex ersity and range of expression profiles of the Laccaria hydrophobin multi-gene family have likely been a selective advantage for this mutualist in colonizing a wide range of host plants.
Publisher: Springer Science and Business Media LLC
Date: 30-05-2019
DOI: 10.1038/S41467-019-10373-Z
Abstract: Despite having key functions in terrestrial ecosystems, information on the dominant soil fungi and their ecological preferences at the global scale is lacking. To fill this knowledge gap, we surveyed 235 soils from across the globe. Our findings indicate that 83 phylotypes ( .1% of the retrieved fungi), mostly belonging to wind dispersed, generalist Ascomycota, dominate soils globally. We identify patterns and ecological drivers of dominant soil fungal taxa occurrence, and present a map of their distribution in soils worldwide. Whole-genome comparisons with less dominant, generalist fungi point at a significantly higher number of genes related to stress-tolerance and resource uptake in the dominant fungi, suggesting that they might be better in colonising a wide range of environments. Our findings constitute a major advance in our understanding of the ecology of fungi, and have implications for the development of strategies to preserve them and the ecosystem functions they provide.
Publisher: Springer Berlin Heidelberg
Date: 2012
Publisher: Wiley
Date: 16-10-2017
DOI: 10.1111/NPH.14825
Publisher: Springer Science and Business Media LLC
Date: 23-03-2017
DOI: 10.1038/S41598-017-00400-8
Abstract: During symbiosis, organisms use a range of metabolic and protein-based signals to communicate. Of these protein signals, one class is defined as ‘effectors’, i.e., small secreted proteins (SSPs) that cause phenotypical and physiological changes in another organism. To date, protein-based effectors have been described in aphids, nematodes, fungi and bacteria. Using RNA sequencing of Populus trichocarpa roots in mutualistic symbiosis with the ectomycorrhizal fungus Laccaria bicolor , we sought to determine if host plants also contain genes encoding effector-like proteins. We identified 417 plant-encoded putative SSPs that were significantly regulated during this interaction, including 161 SSPs specific to P. trichocarpa and 15 SSPs exhibiting expansion in Populus and closely related lineages. We demonstrate that a subset of these SSPs can enter L. bicolor hyphae, localize to the nucleus and affect hyphal growth and morphology. We conclude that plants encode proteins that appear to function as effector proteins that may regulate symbiotic associations.
Publisher: Cold Spring Harbor Laboratory
Date: 22-12-2020
DOI: 10.1101/2020.12.21.423155
Abstract: Shifts in the timing, intensity and/or frequency of climate extremes, such as severe drought and heatwaves, can generate sustained shifts in ecosystem function with important ecological and economic impacts for rangelands and managed pastures. The Pastures and Climate Extremes experiment (PACE) in Southeast Australia was designed to investigate the impacts of a severe winter/spring drought (60% rainfall reduction) and, for a subset of species, a factorial combination of drought and elevated temperature (ambient +3 °C) on pasture productivity. The experiment included nine common pasture and Australian rangeland species from three plant functional groups (C 3 grasses, C 4 grasses and legumes) planted in monoculture. Winter/spring drought resulted in productivity declines of 45% on average and up to 74% for the most affected species ( Digitaria eriantha ) during the 6-month treatment period, with eight of the nine species exhibiting significant yield reductions. Despite considerable variation in species’ sensitivity to drought, C 4 grasses were more strongly affected by this treatment than C 3 grasses or legumes. Warming also had negative effects on cool-season productivity, associated at least partially with exceedance of optimum growth temperatures in spring and indirect effects on soil water content. The combination of winter/spring drought and year-round warming resulted in the greatest yield reductions. We identified responses that were either additive such that there was only as significant warming effect under drought ( Festuca ), or less-than-additive, where there was no drought effect under warming ( Medicago ), compared to ambient plots. Results from this study highlight the sensitivity of erse pasture species to increases in winter and spring drought severity similar to those predicted for this region, and that anticipated benefits of cool-season warming are unlikely to be realised. Overall, the substantial negative impacts on productivity suggest that future, warmer, drier climates will result in shortfalls in cool-season forage availability, with profound implications for the livestock industry and natural grazer communities.
Publisher: Wiley
Date: 03-12-2020
DOI: 10.1111/PCE.13672
Abstract: Armillaria root rot is a fungal disease that affects a wide range of trees and crops around the world. Despite being a widespread disease, little is known about the plant molecular responses towards the pathogenic fungi at the early phase of their interaction. With recent research highlighting the vital roles of metabolites in plant root-microbe interactions, we sought to explore the presymbiotic metabolite responses of Eucalyptus grandis seedlings towards Armillaria luteobuablina, a necrotrophic pathogen native to Australia. Using a metabolite profiling approach, we have identified threitol as one of the key metabolite responses in E. grandis root tips specific to A. luteobubalina that were not induced by three other species of soil-borne microbes of different lifestyle strategies (a mutualist, a commensalist, and a hemi-biotrophic pathogen). Using isotope labelling, threitol detected in the Armillaria-treated root tips was found to be largely derived from the fungal pathogen. Exogenous application of d-threitol promoted microbial colonization of E. grandis and triggered hormonal responses in root cells. Together, our results support a role of threitol as an important metabolite signal during eucalypt-Armillaria interaction prior to infection thus advancing our mechanistic understanding on the earliest stage of Armillaria disease development. Comparative metabolomics of eucalypt roots interacting with a range of fungal lifestyles identified threitol enrichment as a specific characteristic of Armillaria pathogenesis. Our findings suggest that threitol acts as one of the earliest fungal signals promoting Armillaria colonization of roots.
Publisher: Wiley
Date: 17-12-2020
DOI: 10.1111/NPH.16322
Abstract: Forest trees are able to thrive in nutrient-poor soils in part because they obtain growth-limiting nutrients, especially nitrogen (N), through mutualistic symbiosis with ectomycorrhizal (ECM) fungi. Addition of inorganic N into these soils is known to disrupt this mutualism and reduce the ersity of ECM fungi. Despite its ecological impact, the mechanisms governing the observed effects of elevated inorganic N on mycorrhizal communities remain unknown. We address this by using a compartmentalized in vitro system to independently alter nutrients to each symbiont. Using stable isotopes, we traced the nutrient flux under different nutrient regimes between Eucalyptus grandis and its ectomycorrhizal symbiont, Pisolithus albus. We demonstrate that giving E. grandis independent access to N causes a significant reduction in root colonization by P. albus. Transcriptional analysis suggests that the observed reduction in colonization may be caused, in part, by altered transcription of microbe perception genes and defence genes. We show that delivery of N to host leaves is not increased by host nutrient deficiency but by fungal nutrient availability instead. Overall, this advances our understanding of the effects of N fertilization on ECM fungi and the factors governing nutrient transfer in the E. grandis-P. microcarpus interaction.
Publisher: Canadian Science Publishing
Date: 11-2007
DOI: 10.1139/B07-063
Abstract: We have produced the largest population of activation-tagged poplar trees to date, approximately 1800 independent lines, and report on phenotypes of interest that have been identified in tissue culture and greenhouse conditions. Activation tagging is an insertional mutagenesis technique that results in the dominant upregulation of an endogenous gene. A large-scale Agrobacterium -mediated transformation protocol was used to transform the pSKI074 activation-tagging vector into Populus tremula × Populus alba hybrid poplar. We have screened the first 1000 lines for developmental abnormalities and have a visible mutant frequency of 2.4%, with alterations in leaf and stem structure as well as overall stature. Most of the phenotypes represent new phenotypes that have not previously been identified in poplar and, in some cases, not in any other plant either. Molecular analysis of the T-DNA inserts of a subpopulation of mutant lines reveal both single and double T-DNA inserts with double inserts more common in lines with visible phenotypes. The broad range of developmental mutants identified in this pilot screen of the population reveals that it will be a valuable resource for gene discovery in poplar. The full value of this population will only be realized as we screen these lines for a wide range of phenotypes.
Publisher: Springer Science and Business Media LLC
Date: 23-11-2020
DOI: 10.1038/S41598-020-76832-6
Abstract: Despite the pivotal role of jasmonic acid in the outcome of plant-microorganism interactions, JA-signaling components in roots of perennial trees like western balsam poplar ( Populus trichocarpa ) are poorly characterized. Here we decipher the poplar-root JA-perception complex centered on PtJAZ6, a co-repressor of JA-signaling targeted by the effector protein MiSSP7 from the ectomycorrhizal basidiomycete Laccaria bicolor during symbiotic development. Through protein–protein interaction studies in yeast we determined the poplar root proteins interacting with PtJAZ6. Moreover, we assessed via yeast triple-hybrid how the mutualistic effector MiSSP7 reshapes the association between PtJAZ6 and its partner proteins. In the absence of the symbiotic effector, PtJAZ6 interacts with the transcription factors PtMYC2s and PtJAM1.1. In addition, PtJAZ6 interacts with it-self and with other Populus JAZ proteins. Finally, MiSSP7 strengthens the binding of PtJAZ6 to PtMYC2.1 and antagonizes PtJAZ6 homo-/heterodimerization. We conclude that a symbiotic effector secreted by a mutualistic fungus may promote the symbiotic interaction through altered dynamics of a JA-signaling-associated protein–protein interaction network, maintaining the repression of PtMYC2.1-regulated genes.
Publisher: Wiley
Date: 09-12-2022
DOI: 10.1111/NPH.17858
Abstract: We aimed to identify genomic traits of transitions to ectomycorrhizal ecology within the Boletales by comparing the genomes of 21 symbiotrophic species with their saprotrophic brown-rot relatives. Gene duplication rate is constant along the backbone of Boletales phylogeny with large loss events in several lineages, while gene family expansion sharply increased in the late Miocene, mostly in the Boletaceae. Ectomycorrhizal Boletales have a reduced set of plant cell-wall-degrading enzymes (PCWDEs) compared with their brown-rot relatives. However, the various lineages retain distinct sets of PCWDEs, suggesting that, over their evolutionary history, symbiotic Boletales have become functionally erse. A smaller PCWDE repertoire was found in Sclerodermatineae. The gene repertoire of several lignocellulose oxidoreductases (e.g. laccases) is similar in brown-rot and ectomycorrhizal species, suggesting that symbiotic Boletales are capable of mild lignocellulose decomposition. Transposable element (TE) proliferation contributed to the higher evolutionary rate of genes encoding effector-like small secreted proteins, proteases, and lipases. On the other hand, we showed that the loss of secreted CAZymes was not related to TE activity but to DNA decay. This study provides novel insights on our understanding of the mechanisms influencing the evolutionary ersification of symbiotic boletes.
Publisher: Wiley
Date: 18-03-2013
Publisher: Oxford University Press (OUP)
Date: 23-05-2016
Abstract: Root systems are simultaneously colonized by multiple in iduals of mycorrhizal fungi. Intraspecific competitive interactions between fungal isolates are likely to affect both fungal and plant performance and be influenced by abiotic factors. Here, we assessed the impact of intraspecific competition between three Pisolithus microcarpus isolates on the establishment of, and benefit derived from, symbioses with Eucalyptus grandis seedlings. We investigated the outcomes of competition under ambient and elevated temperature and CO2 concentration ([CO2]) in a factorial design. We observed a reduction in mycelium growth, mycorrhiza formation and seedling mass when two P. microcarpus isolates were co-inoculated on a single E. grandis seedling. Isolates invested more in mycelium than in mycorrhizas in the presence of a competitor. All isolates responded negatively to elevated [CO2] and positively to elevated temperature, which led to no changes on the outcomes of the interactions with changing conditions. However, the presence of a competitor hindered the positive response of P. microcarpus isolates to warming, which resulted in larger negative effects of competition under elevated temperature than under ambient conditions. Our study highlights the need to consider how competition affects in idual fungal responses as well as plant performance when trying to predict the impacts of climate change.
Publisher: Informa UK Limited
Date: 2012
Publisher: Springer Science and Business Media LLC
Date: 21-07-2017
Publisher: CSIRO Publishing
Date: 2019
DOI: 10.1071/FP18200
Abstract: A major goal in agricultural research is to develop ‘elite’ crops with stronger, resilient root systems. Within this context, breeding practices have focussed on developing plant varieties that are, primarily, able to withstand pathogen attack and, secondarily, able to maximise plant productivity. Although great strides towards breeding disease-tolerant or -resistant root stocks have been made, this has come at a cost. Emerging studies in certain crop species suggest that domestication of crops, together with soil management practices aimed at improving plant yield, may hinder beneficial soil microbial association or reduce microbial ersity in soil. To achieve more sustainable management of agricultural lands, we must not only shift our soil management practices but also our breeding strategy to include contributions from beneficial microbes. For this latter point, we need to advance our understanding of how plants communicate with, and are able to differentiate between, microbes of different lifestyles. Here, we present a review of the key findings on belowground plant–microbial interactions that have been made over the past decade, with a specific focus on how plants and microbes communicate. We also discuss the currently unresolved questions in this area, and propose plausible ways to use currently available research and integrate fast-emerging ‘-omics’ technologies to tackle these questions. Combining past and developing research will enable the development of new crop varieties that will have new, value-added phenotypes belowground.
Publisher: Wiley
Date: 18-11-2021
Publisher: Springer International Publishing
Date: 2017
DOI: 10.1007/7397_2016_1
Publisher: Frontiers Media SA
Date: 02-2019
Publisher: MDPI AG
Date: 02-02-2022
DOI: 10.3390/MICROORGANISMS10020343
Abstract: Hemibiotrophic pathogens cause significant losses within agriculture, threatening the sustainability of food systems globally. These microbes colonise plant tissues in three phases: a biotrophic phase followed by a biotrophic-to-necrotrophic switch phase and ending with necrotrophy. Each of these phases is characterized by both common and discrete host transcriptional responses. Plant hormones play an important role in these phases, with foliar models showing that salicylic acid accumulates during the biotrophic phase and jasmonic acid/ethylene responses occur during the necrotrophic phase. The appropriateness of this model to plant roots has been challenged in recent years. The need to understand root responses to hemibiotrophic pathogens of agronomic importance necessitates further research. In this study, using the root hemibiotroph
Publisher: MDPI AG
Date: 07-02-2022
DOI: 10.3390/MICROORGANISMS10020383
Abstract: Austropuccinia psidii is a fungal plant pathogen that infects species within the Myrtaceae, causing the disease myrtle rust. Myrtle rust is causing declines in populations within natural and managed ecosystems and is expected to result in species extinctions. Despite this, variation in response to A. psidii exist within some species, from complete susceptibility to resistance that prevents or limits infection by the pathogen. Untargeted metabolomics using Ultra Performance Liquid Chromatography with Ion Mobility followed by analysis using MetaboAnalyst 3.0, was used to explore the chemical defence profiles of resistant, hypersensitive and susceptible phenotypes within Melaleuca quinquenervia during the early stages of A. psidii infection. We were able to identify three separate pools of secondary metabolites: (i) metabolites classified structurally as flavonoids that were naturally higher in the leaves of resistant in iduals prior to infection, (ii) organoheterocyclic and carbohydrate-related metabolites that varied with the level of host resistance post-infection, and (iii) metabolites from the terpenoid pathways that were responsive to disease progression regardless of resistance phenotype suggesting that these play a minimal role in disease resistance during the early stages of colonization of this species. Based on the classes of these secondary metabolites, our results provide an improved understanding of key pathways that could be linked more generally to rust resistance with particular application within Melaleuca.
Publisher: Springer Science and Business Media LLC
Date: 07-08-2023
Publisher: Wiley
Date: 19-06-2014
DOI: 10.1111/NPH.12891
Publisher: Wiley
Date: 02-11-2011
Publisher: Wiley
Date: 16-11-2022
DOI: 10.1111/NPH.17825
Abstract: The pathways regulated in ectomycorrhizal (EcM) plant hosts during the establishment of symbiosis are not as well understood when compared to the functional stages of this mutualistic interaction. Our study used the EcM host Eucalyptus grandis to elucidate symbiosis‐regulated pathways across the three phases of this interaction. Using a combination of RNA sequencing and metabolomics we studied both stage‐specific and core responses of E. grandis during colonization by Pisolithus microcarpus . Using exogenous manipulation of the abscisic acid (ABA), we studied the role of this pathway during symbiosis establishment. Despite the mutualistic nature of this symbiosis, a large number of disease signalling TIR‐NBS‐LRR genes were induced. The transcriptional regulation in E. grandis was found to be dynamic across colonization with a small core of genes consistently regulated at all stages. Genes associated to the carotenoid/ABA pathway were found within this core and ABA concentrations increased during fungal integration into the root. Supplementation of ABA led to improved accommodation of P. microcarpus into E. grandis roots. The carotenoid pathway is a core response of an EcM host to its symbiont and highlights the need to understand the role of the stress hormone ABA in controlling host–EcM fungal interactions.
Publisher: Wiley
Date: 15-04-2009
DOI: 10.1111/J.1399-3054.2009.01208.X
Abstract: Control of the levels of the plant hormone ethylene is crucial in the regulation of many developmental processes and stress responses. Ethylene production can be controlled by altering endogenous levels of 1-aminocyclopropane-1-carboxylic acid (ACC), the immediate precursor to ethylene or by altering its conversion to ethylene. ACC is known to be irreversibly broken down by bacterial or fungal ACC deaminases (ACDs). Sequence analysis revealed two putative ACD genes encoded for in the genome of Arabidopsis thaliana (A. thaliana) and we detected ACD activity in plant extracts. Expression of one of these A. thaliana genes (AtACD1) in bacteria indicated that it had ACD activity. Moreover, transgenic plants harboring antisense constructs of the gene decreased ACD activity to 70% of wild-type (WT) levels, displayed an increased sensitivity to ACC and produced significantly more ethylene. Taken together, these results show that AtACD1 can act as a regulator of ACC levels in A. thaliana.
Publisher: Wiley
Date: 03-01-2014
DOI: 10.1111/NPH.12655
Abstract: The plant hormones ethylene, jasmonic acid and salicylic acid have interconnecting roles during the response of plant tissues to mutualistic and pathogenic symbionts. We used morphological studies of transgenic‐ or hormone‐treated Populus roots as well as whole‐genome oligoarrays to examine how these hormones affect root colonization by the mutualistic ectomycorrhizal fungus Laccaria bicolor S238N. We found that genes regulated by ethylene, jasmonic acid and salicylic acid were regulated in the late stages of the interaction between L. bicolor and poplar. Both ethylene and jasmonic acid treatments were found to impede fungal colonization of roots, and this effect was correlated to an increase in the expression of certain transcription factors (e.g. ETHYLENE RESPONSE FACTOR1 ) and a decrease in the expression of genes associated with microbial perception and cell wall modification. Further, we found that ethylene and jasmonic acid showed extensive transcriptional cross‐talk, cross‐talk that was opposed by salicylic acid signaling. We conclude that ethylene and jasmonic acid pathways are induced late in the colonization of root tissues in order to limit fungal growth within roots. This induction is probably an adaptive response by the plant such that its growth and vigor are not compromised by the fungus.
Publisher: Elsevier BV
Date: 11-2014
DOI: 10.1016/J.FGB.2014.08.007
Abstract: Ectomycorrhizal fungi, living in soil forests, are required microorganisms to sustain tree growth and productivity. The establishment of mutualistic interaction with roots to form ectomycorrhiza (ECM) is not well known at the molecular level. In particular, how fungal and plant cell walls are rearranged to establish a fully functional ectomycorrhiza is poorly understood. Nevertheless, it is likely that Carbohydrate Active enZymes (CAZyme) produced by the fungus participate in this process. Genome-wide transcriptome profiling during ECM development was used to examine how the CAZome of Laccaria bicolor is regulated during symbiosis establishment. CAZymes active on fungal cell wall were upregulated during ECM development in particular after 4weeks of contact when the hyphae are surrounding the root cells and start to colonize the apoplast. We demonstrated that one expansin-like protein, whose expression is specific to symbiotic tissues, localizes within fungal cell wall. Whereas L. bicolor genome contained a constricted repertoire of CAZymes active on cellulose and hemicellulose, these CAZymes were expressed during the first steps of root cells colonization. L. bicolor retained the ability to use homogalacturonan, a pectin-derived substrate, as carbon source. CAZymes likely involved in pectin hydrolysis were mainly expressed at the stage of a fully mature ECM. All together, our data suggest an active remodelling of fungal cell wall with a possible involvement of expansin during ECM development. By contrast, a soft remodelling of the plant cell wall likely occurs through the loosening of the cellulose microfibrils by AA9 or GH12 CAZymes and middle lamella smooth remodelling through pectin (homogalacturonan) hydrolysis likely by GH28, GH12 CAZymes.
Publisher: Wiley
Date: 05-11-2015
DOI: 10.1111/NPH.13103
Abstract: Using the newly available genome for Eucalyptus grandis , we sought to determine the genome‐wide traits that enable this host to form mutualistic interactions with ectomycorrhizal ( ECM ) Pisolithus sp. and to determine how future predicted concentrations of atmospheric carbon dioxide ( CO 2 ) will affect this relationship. We analyzed the physiological and transcriptomic responses of E. grandis during colonization by different Pisolithus sp. isolates under conditions of ambient (400 ppm) and elevated (650 ppm) CO 2 to tease out the gene expression profiles associated with colonization status. We demonstrate that E. grandis varies in its susceptibility to colonization by different Pisolithus isolates in a manner that is not predictable by geographic origin or the internal transcribed spacer ( ITS )‐based phylogeny of the fungal partner. Elevated concentrations of CO 2 alter the receptivity of E. grandis to Pisolithus , a change that is correlated to a dramatic shift in the transcriptomic profile of the root. These data provide a starting point for understanding how future environmental change may alter the signaling between plants and their ECM partners and is a step towards determining the mechanism behind previously observed shifts in Eucalypt‐ associated fungal communities exposed to elevated concentrations of atmospheric CO 2 .
Publisher: Wiley
Date: 18-01-2018
DOI: 10.1111/TPJ.13802
Abstract: Microorganisms, or 'microbes', have formed intimate associations with plants throughout the length of their evolutionary history. In extant plant systems microbes still remain an integral part of the ecological landscape, impacting plant health, productivity and long-term fitness. Therefore, to properly understand the genetic wiring of plants, we must first determine what perception systems plants have evolved to parse beneficial from commensal from pathogenic microbes. In this review, we consider some of the most recent advances in how plants respond at the molecular level to different microbial lifestyles. Further, we cover some of the means by which microbes are able to manipulate plant signaling pathways through altered destructiveness and nutrient sinks, as well as the use of effector proteins and micro-RNAs (miRNAs). We conclude by highlighting some of the major questions still to be answered in the field of plant-microbe research, and suggest some of the key areas that are in greatest need of further research investment. The results of these proposed studies will have impacts in a wide range of plant research disciplines and will, ultimately, translate into stronger agronomic crops and forestry stock, with immune perception and response systems bred to foster beneficial microbial symbioses while repudiating pathogenic symbioses.
Publisher: Oxford University Press (OUP)
Date: 31-03-2023
Abstract: Ectomycorrhizal (ECM) fungi are key players in forest carbon (C) sequestration, receiving a substantial proportion of photosynthetic C from their forest tree hosts in exchange for plant growth-limiting soil nutrients. However, it remains unknown whether the fungus or plant controls the quantum of C in this exchange, nor what mechanisms are involved. Here, we aimed to identify physiological and genetic properties of both partners that influence ECM C transfer. Using a microcosm system, stable isotope tracing, and transcriptomics, we quantified plant-to-fungus C transfer between the host plant Eucalyptus grandis and nine isolates of the ECM fungus Pisolithus microcarpus that range in their mycorrhization potential and investigated fungal growth characteristics and plant and fungal genes that correlated with C acquisition. We found that C acquisition by P. microcarpus correlated positively with both fungal biomass production and the expression of a subset of fungal C metabolism genes. In the plant, C transfer was not positively correlated to the number of colonized root tips, but rather to the expression of defence- and stress-related genes. These findings suggest that C acquisition by ECM fungi involves in idual fungal demand for C and defence responses of the host against C drain.
Publisher: Proceedings of the National Academy of Sciences
Date: 10-01-2022
Abstract: Plant genomes encode hundreds of genes controlling the detection, signaling pathways, and immune responses necessary to defend against pathogens. Pathogens, in turn, continually evolve to evade these defenses. Small RNAs, such as microRNAs (miRNAs), are one mechanism used by pathogens to overcome plant defenses and facilitate plant colonization. Mounting evidence would suggest that beneficial microbes, likewise, use miRNAs to facilitate symbiosis. Here, we demonstrate that the beneficial fungus Pisolithus microcarpus encodes a miRNA that enters plant cells and stabilizes the symbiotic interaction. These results demonstrate that beneficial fungi may regulate host gene expression through the use of miRNAs and sheds light on how beneficial microbes have evolved mechanisms to colonize plant tissues.
Publisher: Frontiers Media SA
Date: 29-03-2019
Publisher: Wiley
Date: 2022
Abstract: Forest trees rely on ectomycorrhizal (ECM) fungi to obtain growth‐limiting nutrients. While addition of nitrogen (N) has the potential to disrupt these critical relationships, there is conflicting evidence as to the mechanism by which ECM:host mutualism may be affected. We evaluated how N fertilization altered host interactions and gene transcription between Eucalyptus grandis and Pisolithus microcarpus or Pisolithus albus , two closely related ECM species that typically co‐occur within the same ecosystem. Our investigation demonstrated species‐specific responses to elevated N: P. microcarpus maintained its ability to transport microbially sourced N to its host but had a reduced ability to penetrate into root tissues, while P. albus maintained its colonization ability but reduced delivery of N to its host. Transcriptomic analysis suggests that regulation of different suites of N‐transporters may be responsible for these species‐specific differences. In addition to N‐dependent responses, we were also able to define a conserved ‘core’ transcriptomic response of Eucalyptus grandis to mycorrhization that was independent of abiotic conditions. Our results demonstrate that even between closely related ECM species, responses to N fertilization can vary considerably, suggesting that a better understanding of the breadth and mechanisms of their responses is needed to support forest ecosystems into the future.
Publisher: Scientific Societies
Date: 06-2013
DOI: 10.1094/MPMI-02-13-0051-IA
Abstract: A wide ersity of pathogens and mutualists of plant and animal hosts, including oomycetes and fungi, produce effector proteins that enter the cytoplasm of host cells. A major question has been whether or not entry by these effectors can occur independently of the microbe or requires machinery provided by the microbe. Numerous publications have documented that oomycete RxLR effectors and fungal RxLR-like effectors can enter plant and animal cells independent of the microbe. A recent reexamination of whether the RxLR domain of oomycete RxLR effectors is sufficient for microbe-independent entry into host cells concluded that the RxLR domains of Phytophthora infestans Avr3a and of P. sojae Avr1b alone are NOT sufficient to enable microbe-independent entry of proteins into host and nonhost plant and animal cells. Here, we present new, more detailed data that unambiguously demonstrate that the RxLR domain of Avr1b does show efficient and specific entry into soybean root cells and also into wheat leaf cells, at levels well above background nonspecific entry. We also summarize host cell entry experiments with a wide ersity of oomycete and fungal effectors with RxLR or RxLR-like motifs that have been independently carried out by the seven different labs that coauthored this letter. Finally we discuss possible technical reasons why specific cell entry may have been not detected by Wawra et al. (2013).
Publisher: Wiley
Date: 28-10-2016
Publisher: Elsevier BV
Date: 2021
Publisher: Elsevier BV
Date: 2011
DOI: 10.1016/J.TIG.2010.10.005
Abstract: Soils contain a multitude of fungi with vastly ergent lifestyles ranging from saprotrophic to mutualistic and pathogenic. The recent release of many fungal genomes has led to comparative studies that consider the extent to which these lifestyles are encoded in the genome. The genomes of the symbiotic fungi Laccaria bicolor and Tuber melanosporum are proving especially useful in characterizing the genetic foundation of mutualistic symbiosis. New insights gleaned from these genomes, as compared to their saprotrophic and pathogenic cousins, have helped to redefine and shape our understanding of the nature of the symbiotic lifestyle. Here we detail the current state of research into this complex relationship and discuss avenues for future exploration.
Publisher: Elsevier BV
Date: 07-2011
DOI: 10.1016/J.CUB.2011.05.033
Abstract: Soil-borne mutualistic fungi, such as the ectomycorrhizal fungi, have helped shape forest communities worldwide over the last 180 million years through a mutualistic relationship with tree roots in which the fungal partner provides a large array of nutrients to the plant host in return for photosynthetically derived sugars. This exchange is essential for continued growth and productivity of forest trees, especially in nutrient-poor soils. To date, the signals from the two partners that mediate this symbiosis have remained uncharacterized. Here we demonstrate that MYCORRHIZAL iNDUCED SMALL SECRETED PROTEIN 7 (MiSSP7), the most highly symbiosis-upregulated gene from the ectomycorrhizal fungus Laccaria bicolor, encodes an effector protein indispensible for the establishment of mutualism. MiSSP7 is secreted by the fungus upon receipt of diffusible signals from plant roots, imported into the plant cell via phosphatidylinositol 3-phosphate-mediated endocytosis, and targeted to the plant nucleus where it alters the transcriptome of the plant cell. L. bicolor transformants with reduced expression of MiSSP7 do not enter into symbiosis with poplar roots. MiSSP7 resembles effectors of pathogenic fungi, nematodes, and bacteria that are similarly targeted to the plant nucleus to promote colonization of the plant tissues and thus can be considered a mutualism effector.
Publisher: Springer Science and Business Media LLC
Date: 23-02-2015
DOI: 10.1038/NG.3223
Abstract: To elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell wall-degrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess erse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7-38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a 'symbiosis toolkit', with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.
Publisher: Wiley
Date: 03-01-2012
Publisher: Elsevier BV
Date: 08-2015
DOI: 10.1016/J.PBI.2015.06.001
Abstract: Mutualistic mycorrhizal plant-fungal interactions have shaped the evolution of plant life on land. In these intimate associations, fungal hyphae grow invasively within plant tissues. Despite this invasion, these mycorrhizal fungi are not repulsed leading to a great deal of research focused on the signals exchanged between mutualistic fungi and their host plants in an effort to understand how these relationships are established. In this review, we focus on one type of signal used by mutualistic fungi during symbiosis: effector proteins. These small secreted proteins have recently been found to be used by a range of beneficial fungi to alter the physiological status of the plant host such that symbiosis is favoured. We discuss how the role of these novel proteins has altered our vision of how the 'mutualistic' lifestyle evolved in fungi: rather than being perceived as beneficial by their plant hosts, these microbes currently viewed as 'beneficial' may actually be overcoming the defences of their plant hosts in a mechanism originally thought to be unique to pathogenic microbes.
Publisher: Elsevier BV
Date: 08-2021
Start Date: 2017
End Date: 2020
Funder: Meat and Livestock Australia
View Funded ActivityStart Date: 2019
End Date: 2022
Funder: Australian Research Council
View Funded ActivityStart Date: 2018
End Date: 2021
Funder: NSW Department of Primary Industries
View Funded ActivityStart Date: 2020
End Date: 2023
Funder: Marsden Fund
View Funded ActivityStart Date: 05-2019
End Date: 05-2022
Amount: $431,000.00
Funder: Australian Research Council
View Funded ActivityStart Date: 01-2015
End Date: 01-2018
Amount: $393,416.00
Funder: Australian Research Council
View Funded ActivityStart Date: 06-2016
End Date: 05-2019
Amount: $371,100.00
Funder: Australian Research Council
View Funded ActivityStart Date: 2022
End Date: 10-2025
Amount: $440,072.00
Funder: Australian Research Council
View Funded Activity