John M Manners

The Commonwealth Scientific and Industrial Research Organisation, Canberra, Australian Capital Territory, Australia

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Publications (204)687.14 Total impact

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    ABSTRACT: The benzoxazolinone class of phytoalexins are released by wheat, maize, rye and other agriculturally important species in the Poaceae family upon pathogen attack. Benzoxazolinones show antimicrobial effects on plant pathogens, but certain fungi have evolved mechanisms to actively detoxify these compounds which may contribute to the virulence of the pathogens. In many Fusarium spp. a cluster of genes is thought to be involved in the detoxification of benzoxazolinones. However, only one enzyme encoded in the cluster has been unequivocally assigned a role in this process. The first step in the detoxification of benzoxazolinones in Fusarium spp. involves the hydrolysis of a cyclic ester bond. This reaction is encoded by the FDB1 locus in F. verticillioides but the underlying gene is yet to be cloned. We previously proposed that FDB1 encodes a γ-lactamase, and here direct evidence for this is presented. Expression analyses in the important wheat pathogen F.pseudograminearum demonstrated that amongst the three predicted γ-lactamase genes only the one designated as FDB1, part of the proposed benzoxazolinone cluster in F.pseudograminearum, was strongly responsive to exogenous benzoxazolinone application. Analysis of independent F. pseudograminearum and F.graminearum FDB1 gene deletion mutants, as well as biochemical assays, demonstrated that the γ-lactamase enzyme, encoded by FDB1, catalyses the first step in detoxification of benzoxazolinones. Overall, our results support the notion that Fusarium pathogens that cause crown rot and head blight on wheat have adopted strategies to overcome host-derived chemical defences. Copyright © 2015. Published by Elsevier Inc.
    Fungal Genetics and Biology 08/2015; DOI:10.1016/j.fgb.2015.08.005 · 3.26 Impact Factor
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    ABSTRACT: Brachypodium distachyon has been widely adopted as a pathosystem for study of cereal pathogens. Fusarium crown rot (FCR), primarily caused by the necrotrophic fungal pathogen Fusarium pseudograminearum, constitutes a major disease risk for the Australian wheat industry. The aim of this work was to assess whether species in the genus Brachypodium will be a useful model for characterizing the molecular basis for resistance to F. pseudograminearum. Two Brachypodium species were found to be readily infected by F. pseudograminearum producing similar symptoms and disease progression to that observed in wheat and barley. A large number of Turkish natural accessions were screened for FCR susceptibility and several ecotypes were found to differ significantly in disease severity. Brachypodium hybridium accessions exhibited significantly greater quantitative resistance compared with B. distachyon accessions. RNAseq was utilized to observe the host molecular response during FCR infection in wheat and B. distachyon. Comparing induction of homologs in wheat and Brachypodium revealed a high degree of similarity in response between crop and model. However, significant differences for induction of defence related phytohormones and other defence related metabolites were observed using liquid chromatography – mass spectrometry (LC-MS). B. distachyon transformants constitutively expressing a salicylate hydroxylase (nahG) from Pseudomonas putida were developed (Bd21-3 background) to assess the importance of salicylic acid mediated defence responses in promoting resistance against necrotrophic pathogens. The potential utility and limitations for Brachypodium as a molecular model for studying cereal-pathogen interactions are discussed in light of observed similarities and differences.
    International Brachypodium Conference 2015; 06/2015
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    ABSTRACT: Plants respond to pathogens either by investing more resources into immunity which is costly to development, or by accelerating reproductive processes such as flowering time to ensure reproduction occurs before the plant succumbs to disease. In this study we explored the link between flowering time and pathogen defense using the interaction between Arabi-dopsis thaliana and the root infecting fungal pathogen Fusarium oxysporum. We report that F. oxysporum infection accelerates flowering time and regulates transcription of a number of floral integrator genes, including FLOWERING LOCUS C (FLC), FLOWERING LOCUS T (FT) and GIGANTEA (GI). Furthermore, we observed a positive correlation between late flowering and resistance to F. oxysporum in A. thaliana natural ecotypes. Late-flowering gi and autonomous pathway mutants also exhibited enhanced resistance to F. oxysporum, supporting the association between flowering time and defense. However, epistasis analysis showed that accelerating flowering time by deletion of FLC in fve-3 or fpa-7 mutants did not alter disease resistance, suggesting that the effect of autonomous pathway on disease resistance occurs independently from flowering time. Indeed, RNA-seq analyses suggest that fve-3 mediated resistance to F. oxysporum is most likely a result of altered defense-associated gene transcription. Together, our results indicate that the association between flowering time and pathogen defense is complex and can involve both pleiotropic and direct effects.
    PLoS ONE 06/2015; 10(6). DOI:10.1371/journal.pone.0127699 · 3.23 Impact Factor
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    ABSTRACT: Pathogens and hosts are in an ongoing arms race and genes involved in host-pathogen interactions are likely to undergo diversifying selection. Fusarium plant pathogens have evolved diverse infection strategies, but how they interact with their hosts in the biotrophic infection stage remains puzzling. To address this, we analysed the genomes of three Fusarium plant pathogens for genes that are under diversifying selection. We found a two-speed genome structure both on the chromosome and gene group level. Diversifying selection acts strongly on the dispensable chromosomes in F. oxysporum f. sp. lycopersici and on distinct core chromosome regions in F. graminearum, all of which have associations with virulence. Members of two gene groups evolve rapidly, namely those that encode proteins with an N-terminal [SG]-P-C-[KR]-P sequence motif and proteins that are conserved predominantly in pathogens. Specifically, 29 F. graminearum genes are rapidly evolving, in planta induced and encode secreted proteins, strongly pointing towards effector function. In summary, diversifying selection in Fusarium is strongly reflected as genomic footprints and can be used to predict a small gene set likely to be involved in host-pathogen interactions for experimental verification. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Genome Biology and Evolution 05/2015; 7(6). DOI:10.1093/gbe/evv092 · 4.53 Impact Factor
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    PLoS Pathogens 05/2015; 11(5):e1004806. DOI:10.1371/journal.ppat.1004806 · 8.06 Impact Factor
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    ABSTRACT: Some of the most devastating agricultural diseases are caused by root-infecting pathogens, yet the majority of studies on these interactions to date have focused on the host responses of aerial tissues rather than those belowground. Fusarium oxysporum is a root-infecting pathogen that causes wilt disease on several plant species including Arabidopsis thaliana. To investigate and compare transcriptional changes triggered by F. oxysporum in different Arabidopsis tissues, we infected soil-grown plants with F. oxysporum and subjected root and leaf tissue harvested at early and late timepoints to RNA-seq analyses. At least half of the genes induced or repressed by F. oxysporum showed tissue-specific regulation. Regulators of auxin and ABA signalling, mannose binding lectins and peroxidases showed strong differential expression in root tissue. We demonstrate that ARF2 and PRX33, two genes regulated in the roots, promote susceptibility to F. oxysporum. In the leaves, defensins and genes associated with the response to auxin, cold and senescence were strongly regulated while jasmonate biosynthesis and signalling genes were induced throughout the plant.
    PLoS ONE 04/2015; 10(4-4):e0121902. DOI:10.1371/journal.pone.0121902 · 3.23 Impact Factor
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    ABSTRACT: Cereal diseases cause tens of billions of dollars of losses annually and have devastating humanitarian consequences in the developing world. Increased understanding of the molecular basis of cereal host-pathogen interactions should facilitate development of novel resistance strategies. However, achieving this in most cereals can be challenging due to large and complex genomes, long generation times and large plant size, as well as quarantine and intellectual property issues that may constrain the development and use of community resources. Brachypodium distachyon (brachypodium) with its small, diploid and sequenced genome, short generation time, high transformability and rapidly expanding community resources is emerging as a tractable cereal model. Recent research reviewed here has demonstrated that brachypodium is either susceptible or partially susceptible to many of the major cereal pathogens. Thus, the study of brachypodium-pathogen interactions appears to hold great potential to improve understanding of cereal disease resistance, and to guide approaches to enhance this resistance. This paper reviews brachypodium experimental pathosystems for the study of fungal, bacterial and viral cereal pathogens; the current status of the use of brachypodium for functional analysis of cereal disease resistance; and comparative genomic approaches undertaken using brachypodium to assist characterization of cereal resistance genes. Additionally, it explores future prospects for brachypodium as a model to study cereal-pathogen interactions. The study of brachypodium-pathogen interactions appears to be a productive strategy for understanding mechanisms of disease resistance in cereal species. Knowledge obtained from this model interaction has strong potential to be exploited for crop improvement. © Commonwealth Scientific and Industrial Research Organisation, 2015.
    Annals of Botany 04/2015; 115(5):717-31. DOI:10.1093/aob/mcv010 · 3.30 Impact Factor
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    ABSTRACT: Reverse genetic techniques harnessing mutational approaches are powerful tools that can provide substantial insight into gene function in plants. However, as compared to diploid species, reverse genetic analyses in polyploid plants such as bread wheat can present substantial challenges associated with high levels of sequence and functional similarity amongst homoeologous loci. We previously developed a high-throughput method to identify deletions of genes within a physically mutagenized wheat population. Here we describe our efforts to combine multiple homoeologous deletions of three candidate disease susceptibility genes (TaWRKY11, TaPFT1 and TaPLDß1). We were able to produce lines featuring homozygous deletions at two of the three homoeoloci for all genes, but this was dependent on the individual mutants used in crossing. Intriguingly, despite extensive efforts, viable lines possessing homozygous deletions at all three homoeoloci could not be produced for any of the candidate genes. To investigate deletion size as a possible reason for this phenomenon, we developed an amplicon sequencing approach based on synteny to Brachypodium distachyon to assess the size of the deletions removing one candidate gene (TaPFT1) in our mutants. These analyses revealed that genomic deletions removing the locus are relatively large, resulting in the loss of multiple additional genes. The implications of this work for the use of heavy ion mutagenesis for reverse genetic analyses in wheat are discussed.
    PLoS ONE 02/2015; 10(2):e0117369. DOI:10.1371/journal.pone.0117369 · 3.23 Impact Factor
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    ABSTRACT: Wheat, maize, rye, and some other agriculturally important species in the Poaceae family produce the benzoxazolinone class of phytoalexins upon pest and pathogen attack. Benzoxazolinones can inhibit the growth of pathogens. However, certain fungi can actively detoxify these compounds. Despite this, a clear link between the ability to detoxify benzoxazolinones and pathogen virulence has not been shown. Here, through comparative genome analysis of several Fusarium species, we have identified a conserved genomic region around the FDB2 gene encoding a N-malonyltransferase enzyme known to be involved in benzoxazolinone degradation in the maize pathogen Fusarium verticillioides. Expression analyses demonstrated that a cluster of nine genes were responsive to exogenous benzoxazolinone in the important wheat pathogen Fusarium pseudograminearum. Analysis of independent F. pseudograminearum FDB2 knockouts and complementation of the knockout with FDB2 homologs from F. graminearum and F. verticillioides confirmed that the N-malonyltransferase enzyme encoded by this gene is central to the detoxification of benzoxazolinones, and that Fdb2 contributes quantitatively to virulence towards wheat in head blight inoculation assays. This contrasts with previous observations in F. verticillioides, where no effect of FDB2 mutations on pathogen virulence towards maize was observed. Overall, our results demonstrate detoxification of benzoxazolinones is a strategy wheat infecting F. pseudograminearum has adopted to overcome host-derived chemical defences. This article is protected by copyright. All rights reserved.
    Molecular Plant Pathology 02/2015; DOI:10.1111/mpp.12250 · 4.49 Impact Factor
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    ABSTRACT: Fusarium pathogens cause two major diseases in cereals, Fusarium crown rot (FCR) and head blight (FHB). A large-effect locus conferring resistance to FCR disease was previously located to chromosome arm 3BL (designated as Qcrs-3B) and several independent sets of near isogenic lines (NILs) have been developed for this locus. In this study, five sets of the NILs were used to examine transcriptional changes associated with the Qcrs-3B locus and to identify genes linked to the resistance locus as a step towards the isolation of the causative gene(s). Of the differentially expressed genes (DEGs) detected between the NILs, 12.7% was located on the single chromosome 3B. Of the expressed genes containing SNP (SNP-EGs) detected, 23.5% was mapped to this chromosome. Several of the DEGs and SNP-EGs are known to be involved in host-pathogen interactions, and a large number of the DEGs were among those detected for FHB in previous studies. Of the DEGs detected, 22 were mapped in the Qcrs-3B interval and they included eight which were detected in the resistant isolines only. The enrichment of DEG, and not necessarily those containing SNPs between the resistant and susceptible isolines, around the Qcrs-3B locus is suggestive of local regulation of this region by the resistance allele. Functions for 13 of these DEGs are known. Of the SNP-EGs, 28 were mapped in the Qcrs-3B interval and biological functions for 16 of them are known. These results provide insights into responses regulated by the 3BL locus and identify a tractable number of target genes for fine mapping and functional testing to identify the causative gene(s) at this QTL.
    PLoS ONE 11/2014; 9(11):e113309. DOI:10.1371/journal.pone.0113309 · 3.23 Impact Factor
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    ABSTRACT: Plant pathogens cause severe losses to crop plants and threaten global food production. One striking example is the wheat stem rust fungus, Puccinia graminis f. sp. tritici, which can rapidly evolve new virulent pathotypes in response to resistant host lines. Like several other filamentous fungal and oomycete plant pathogens, its genome features expanded gene families that have been implicated in host-pathogen interactions, possibly encoding effector proteins that interact directly with target host defense proteins. Previous efforts to understand virulence largely relied on the prediction of secreted, small and cysteine-rich proteins as candidate effectors and thus delivered an overwhelming number of candidates. Here, we implement an alternative analysis strategy that uses the signal of adaptive evolution as a line of evidence for effector function, combined with comparative information and expression data. We demonstrate that in planta up-regulated genes that are rapidly evolving are found almost exclusively in pathogen-associated gene families, affirming the impact of host-pathogen co-evolution on genome structure and the adaptive diversification of specialized gene families. In particular, we predict 42 effector candidates that are conserved only across pathogens, induced during infection and rapidly evolving. One of our top candidates has recently been shown to induce genotype-specific hypersensitive cell death in wheat. This shows that comparative genomics incorporating the evolutionary signal of adaptation is powerful for predicting effector candidates for laboratory verification. Our system can be applied to a wide range of pathogens and will give insight into host-pathogen dynamics, ultimately leading to progress in strategies for disease control.
    Frontiers in Plant Science 09/2014; 5:372. DOI:10.3389/fpls.2014.00372 · 3.95 Impact Factor
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    ABSTRACT: Studies in Arabidopsis show that DELLA genes may differentially affect responses to biotrophic and necrophic pathogens. A recent report based on the study of DELLA-producing reduced height (Rht) genes in wheat and barley also hypothesized that DELLA genes likely increased susceptibility to necrotrophs but increased resistance to biotrophs. Effects of uzu, a non-GA (gibberellic acid)-responsive semi-dwarfing gene, on Fusarium crown rot (FCR) resistance in barley were investigated. Fifteen pairs of near isogenic lines for this gene were generated and assessed under two different temperature regimes. Similar to its impacts on plant height, the semi-dwarfing gene uzu also showed larger effects on FCR severity in the high temperature regime when compared with that in the low temperature regime. Results from this study add to the growing evidence showing that the effects of plant height on Fusarium resistances are unlikely related to DELLA genes but due to direct or indirect effects of height difference per se. The interaction between these two characteristics highlights the importance of understanding relationships between resistance and other traits of agronomic importance as the value of a resistance gene could be compromised if it dramatically affects plant development and morphology.
    BMC Plant Biology 01/2014; 14(1):22. DOI:10.1186/1471-2229-14-22 · 3.94 Impact Factor
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    ABSTRACT: In comparison to dicot-infecting bacteria, only limited numbers of genome sequences are available for monocot-infecting and in particular cereal-infecting bacteria. Herein we report the characterisation and genome sequence of Xanthomonas translucens isolate DAR61454 pathogenic on wheat and barley. Based on phylogenetic analysis of the ATP synthase beta subunit (atpD) gene, DAR61454 is most closely related to other X. translucens strains and the sugarcane- and banana- infecting Xanthomonas strains, but shares a type III secretion system (T3SS) with X. translucens pv. graminis and more distantly related xanthomonads. Assays with an adenylate cyclase reporter protein demonstrate that DAR61454's T3SS is functional in delivering proteins to wheat cells. X. translucens DAR61454 also encodes two type VI secretion systems with one most closely related to those found in some strains of the rice infecting strain X. oryzae pv. oryzae but not other xanthomonads. Comparative analysis of 18 different Xanthomonas isolates revealed 84 proteins unique to cereal (i.e. rice) infecting isolates and the wheat/barley infecting DAR61454. Genes encoding 60 of these proteins are found in gene clusters in the X. translucens DAR61454 genome, suggesting cereal-specific pathogenicity islands. However, none of the cereal pathogen specific proteins were homologous to known Xanthomonas spp. effectors. Comparative analysis outside of the bacterial kingdom revealed a nucleoside triphosphate pyrophosphohydrolase encoding gene in DAR61454 also present in other bacteria as well as a number of pathogenic Fusarium species, suggesting that this gene may have been transmitted horizontally from bacteria to the Fusarium lineage of pathogenic fungi. This example further highlights the importance of horizontal gene acquisition from bacteria in the evolution of fungi.
    PLoS ONE 01/2014; 9(1):e84995. DOI:10.1371/journal.pone.0084995 · 3.23 Impact Factor
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    ABSTRACT: Fungal pathogens cause devastating losses in economically important cereal crops by utilising pathogen proteins to infect host plants. Secreted pathogen proteins are referred to as effectors and have thus far been identified by selecting small, cysteine-rich peptides from the secretome despite increasing evidence that not all effectors share these attributes. We take advantage of the availability of sequenced fungal genomes and present an unbiased method for finding putative pathogen proteins and secreted effectors in a query genome via comparative hidden Markov Model analyses followed by unsupervised protein clustering. Our method returns experimentally validated fungal effectors in Stagonospora nodorum and Fusarium oxysporum as well as the N-terminal Y/F/WxC-motif from the barley powdery mildew pathogen. Application to the cereal pathogen Fusarium graminearum reveals a secreted phosphorylcholine phosphatase that is characteristic of hemibiotrophic and necrotrophic cereal pathogens and shares an ancient selection process with bacterial plant pathogens. Three F. graminearum protein clusters are found with an enriched secretion signal. One of these putative effector clusters contains proteins that share a [SG]-P-C-[KR]-P sequence motif in the N-terminal and show features not commonly associated with fungal effectors. This motif is conserved in secreted pathogenic Fusarium proteins and a prime candidate for functional testing. Our pipeline has successfully uncovered conservation patterns, putative effectors and motifs of fungal pathogens that would have been overlooked by existing approaches that identify effectors as small, secreted, cysteine-rich peptides. It can be applied to any pathogenic proteome data, such as microbial pathogen data of plants and other organisms.
    BMC Genomics 11/2013; 14(1):807. DOI:10.1186/1471-2164-14-807 · 4.04 Impact Factor
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    ABSTRACT: Fusarium is a genus of filamentous fungi that contains many agronomically important plant pathogens, mycotoxin producers, and opportunistic human pathogens. Comparative analyses have revealed that the Fusarium genome is compartmentalized into regions responsible for primary metabolism and reproduction (core genome), and pathogen virulence, host specialization, and possibly other functions (adaptive genome). Genes involved in virulence and host specialization are located on pathogenicity chromosomes within strains pathogenic to tomato (Fusarium oxysporum f. sp. lycopersici) and pea (Fusarium 'solani' f. sp. pisi). The experimental transfer of pathogenicity chromosomes from F. oxysporum f. sp. lycopersici into a nonpathogen transformed the latter into a tomato pathogen. Thus, horizontal transfer may explain the polyphyletic origins of host specificity within the genus. Additional genome-scale comparative and functional studies are needed to elucidate the evolution and diversity of pathogenicity mechanisms, which may help inform novel disease management strategies against fusarial pathogens.
    Annual review of microbiology 09/2013; 67(1):399-416. DOI:10.1146/annurev-micro-092412-155650 · 13.02 Impact Factor
  • Donald M Gardiner · Kemal Kazan · John M Manners
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    ABSTRACT: The constant interaction between plants and their pathogens has resulted in the evolution of a diverse array of microbial infection strategies. It is increasingly evident that horizontal acquisition of new virulence functions in fungi is one of the evolutionary processes that maintain pathogens' competitive edge over host plants. Genome analyses of fungi are pointing towards this phenomenon being particularly prevalent in the subphylum Pezizomycota. While the extent of cross-kingdom gene transfer can be determined with existing genomic tools and databases, so far very few horizontally transmitted genes have been functionally characterised, and an understanding of their physiological roles in virulence has been determined for even fewer genes. Understanding the evolutionary selection pressures that drive the retention of acquired genes in particular fungal lineages is important, as it will undoubtedly reveal new insights into both fungal virulence mechanisms and corresponding plant defence processes in the future.
    Plant Science 09/2013; 210C:151-158. DOI:10.1016/j.plantsci.2013.06.002 · 4.11 Impact Factor
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    ABSTRACT: Fusarium pathogens represent a major constraint to wheat and barley production worldwide. To facilitate future comparative studies of Fusarium species that are pathogenic to wheat, the genome sequences of four Fusarium pseudograminearum isolates, a single Fusarium acuminatum isolate, and an organism from the Fusarium incarnatum-F. equiseti species complex are reported.
    Genome Announcements 08/2013; 1(5). DOI:10.1128/genomeA.00670-13
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    ABSTRACT: FgABC1 (FGSG_04580) is predicted to encode a pleiotropic drug resistance-class ABC transporter in Fusarium graminearum, a globally important pathogen of wheat. Deletion mutants of FgABC1 showed reduced virulence towards wheat in crown and root infection assays but were unaltered in infectivity on barley. Expression of FgABC1 during head blight and crown rot disease increases during the necrotrophic phases of infection suggestive of a role for FgABC1 in late infection stages in different tissue types. Deletion of FgABC1 also led to increased sensitivity of the fungus to the antifungal compound benalaxyl in culture but the response to known cereal defence compounds, gramine, 2-benzoxazalinone and tryptamine, was un-altered. FgABC1 appears to have a role in protecting the fungus from antifungal compounds and is likely to help combat as yet unidentified wheat defence compounds during disease development. This article is protected by copyright. All rights reserved.
    FEMS Microbiology Letters 08/2013; 348(1). DOI:10.1111/1574-6968.12240 · 2.72 Impact Factor
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    ABSTRACT: Reactive oxygen species (ROS) are produced in plant cells in response to diverse biotic and abiotic stresses as well as during normal growth and development. Although a large number of transcription factor (TF) genes are up- or down-regulated by ROS, currently very little is known about the functions of these TFs during oxidative stress. In this work, we examined the role of ERF6 (ETHYLENE RESPONSE FACTOR6), an AP2/ERF domain-containing TF, during oxidative stress responses in Arabidopsis. Mutant analyses showed that NADPH oxidase (RbohD) and calcium signaling are required for ROS-responsive expression of ERF6. erf6 insertion mutant plants showed reduced growth and increased H2O2 and anthocyanin levels. Expression analyses of selected ROS-responsive genes during oxidative stress identified several differentially expressed genes in the erf6 mutant. In particular, a number of ROS responsive genes, such as ZAT12, HSFs, WRKYs, MAPKs, RBOHs, DHAR1, APX4, and CAT1 were more strongly induced by H2O2 in erf6 plants than in wild-type. In contrast, MDAR3, CAT3, VTC2 and EX1 showed reduced expression levels in the erf6 mutant. Taken together, our results indicate that ERF6 plays an important role as a positive antioxidant regulator during plant growth and in response to biotic and abiotic stresses.
    PLoS ONE 08/2013; 8(8):e70289. DOI:10.1371/journal.pone.0070289 · 3.23 Impact Factor
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    ABSTRACT: Compared to those of dicot-infecting bacteria, the available genome sequences of bacteria that infect wheat and barley are limited. Herein, we report the draft genome sequences of four pseudomonads originally isolated from these cereals. These genome sequences provide a useful resource for comparative analyses within the genus and for cross-kingdom analyses of plant pathogenesis.
    Genome Announcements 05/2013; 1(3). DOI:10.1128/genomeA.00209-13

Publication Stats

8k Citations
687.14 Total Impact Points

Institutions

  • 1988–2014
    • The Commonwealth Scientific and Industrial Research Organisation
      • Division of Plant Industry
      Canberra, Australian Capital Territory, Australia
  • 2012
    • The University of Warwick
      • School of Life Sciences
      Coventry, ENG, United Kingdom
  • 1983–2011
    • University of Queensland
      • School of Agriculture and Food Sciences
      Brisbane, Queensland, Australia
  • 1977–2008
    • Imperial College London
      Londinium, England, United Kingdom