Publications by authors named "Frances Trail"

44 Publications

Crop Management Impacts the Soybean () Microbiome.

Front Microbiol 2020 3;11:1116. Epub 2020 Jun 3.

Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, United States.

Soybean () is an important leguminous crop that is grown throughout the United States and around the world. In 2016, soybean was valued at $41 billion USD in the United States alone. Increasingly, soybean farmers are adopting alternative management strategies to improve the sustainability and profitability of their crop. Various benefits have been demonstrated for alternative management systems, but their effects on soybean-associated microbial communities are not well-understood. In order to better understand the impact of crop management systems on the soybean-associated microbiome, we employed DNA amplicon sequencing of the Internal Transcribed Spacer (ITS) region and 16S rRNA genes to analyze fungal and prokaryotic communities associated with soil, roots, stems, and leaves. Soybean plants were sampled from replicated fields under long-term conventional, no-till, and organic management systems at three time points throughout the growing season. Results indicated that sample origin was the main driver of beta diversity in soybean-associated microbial communities, but management regime and plant growth stage were also significant factors. Similarly, differences in alpha diversity are driven by compartment and sample origin. Overall, the organic management system had lower fungal and bacterial Shannon diversity. In prokaryotic communities, aboveground tissues were dominated by and while belowground samples were dominated by and Aboveground fungal communities were dominated by across all management systems, while belowground samples were dominated by and . Specific taxa including potential plant beneficials such as were indicator species of the conventional and organic management systems. No-till management increased the abundance of groups known to contain plant beneficial organisms such as and Glomeromycotina. Network analyses show different highly connected hub taxa were present in each management system. Overall, this research demonstrates how specific long-term cropping management systems alter microbial communities and how those communities change throughout the growth of soybean.
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http://dx.doi.org/10.3389/fmicb.2020.01116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7283522PMC
June 2020

Integrative Activity of Mating Loci, Environmentally Responsive Genes, and Secondary Metabolism Pathways during Sexual Development of Chaetomium globosum.

mBio 2019 12 10;10(6). Epub 2019 Dec 10.

Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut, USA

The origins and maintenance of the rich fungal diversity have been longstanding issues in evolutionary biology. To investigate how differences in expression regulation contribute to divergences in development and ecology among closely related species, transcriptomes were compared between , a homothallic pathogenic fungus thriving in highly humid ecologies, and , a heterothallic postfire saprotroph. Gene expression was quantified in perithecia at nine distinct morphological stages during nearly synchronous sexual development. Unlike , expression of all mating loci in was highly correlated. Key regulators of the initiation of sexual development in response to light stimuli-including orthologs of , -dependent gene NCU00309, and -showed regulatory dynamics matching between and Among 24 secondary metabolism gene clusters in , 11-including the cochliodones biosynthesis cluster-exhibited highly coordinated expression across perithecial development. exhibited coordinately upregulated expression of histidine kinases in hyperosmotic response pathways-consistent with gene expression responses to high humidity we identified in fellow pathogen Bayesian networks indicated that gene interactions during sexual development have diverged in concert with the capacities both to reproduce asexually and to live a self-compatible versus self-incompatible life cycle, shifting the hierarchical roles of genes associated with conidiation and heterokaryon incompatibility in and This divergence supports an evolutionary history of loss of conidiation due to unfavorable combinations of heterokaryon incompatibility in homothallic species. Fungal diversity has amazed evolutionary biologists for decades. One societally important aspect of this diversity manifests in traits that enable pathogenicity. The opportunistic pathogen is well adapted to a high-humidity environment and produces numerous secondary metabolites that defend it from predation. Many of these chemicals can threaten human health. Understanding the phases of the life cycle in which these products are made enables better control and even utilization of this fungus. Among its intriguing traits is that it both is self-fertile and lacks any means of propagule-based asexual reproduction. By profiling genome-wide gene expression across the process of sexual reproduction in and comparing it to genome-wide gene expression in the model filamentous fungus and other closely related fungi, we revealed associations among mating-type genes, sexual developmental genes, sexual incompatibility regulators, environmentally responsive genes, and secondary metabolic pathways.
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http://dx.doi.org/10.1128/mBio.02119-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6904875PMC
December 2019

Structure and Chemical Analysis of Major Specialized Metabolites Produced by the Lichen Evernia prunastri.

Chem Biodivers 2020 Jan 10;17(1):e1900465. Epub 2020 Jan 10.

Plant Biology Laboratories, Department of Plant Biology, Michigan State University, 612 Wilson Road, Room 342, East Lansing, MI 48824, USA.

We performed comparative profiling of four specialized metabolites in the lichen Evernia prunastri, collected at three different geographic locations, California and Maine, USA, and Yoshkar Ola, Mari El, Russia. Among the compounds produced at high concentrations that were identified in all three specimens, evernic acid, usnic acid, lecanoric acid and chloroatranorin, evernic acid was the most abundant. Two depsidones, salazinic acid and physodic acid, were detected in the Yoshkar-Ola collection only. The crystalline structure of evernic acid (2-hydroxy-4-[(2-hydroxy-4-methoxy-6-methylbenzoyl)oxy]-6-methylbenzoate) (hmb) revealed two crystallographically and conformationally distinct hmb anions, along with two monovalent sodium atoms. One hmb moiety contained an exotetradentate binding mode to sodium, whereas the other exhibited an exohexadentate binding mode to sodium. Embedded edge-sharing {Na O } sodium-oxygen chains connected the hmb anions into the full three-dimensional crystal structure of the title compound. The crystal used for single-crystal X-ray diffraction exhibited non-merohedral twinning. The data suggest the importance of the acetyl-polymalonyl pathway products to processes of maintaining integrity of the lichen holobiont community.
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http://dx.doi.org/10.1002/cbdv.201900465DOI Listing
January 2020

Comparative Genomics and Transcriptomics During Sexual Development Gives Insight Into the Life History of the Cosmopolitan Fungus .

Front Microbiol 2019 7;10:1247. Epub 2019 Jun 7.

Department of Plant Biology, Michigan State University, East Lansing, MI, United States.

(formerly ) is a cosmopolitan fungus that has been reported from soil, herbivore dung, and as a fruit- and root-rot pathogen of numerous field crops, although it is not known to cause significant losses on any crop. Taking advantage of the fact that this species produces prolific numbers of perithecia in culture, the genome of was sequenced and transcriptomic analysis across five stages of perithecium development was performed to better understand the metabolic potential for sexual development and gain insight into its life history. Perithecium morphology together with the genome and transcriptome were compared with those of the plant pathogen , a model for studying perithecium development. Larger ascospores of and their tendency to discharge as a cluster demonstrated a duality of dispersal: the majority are passively dispersed through the formation of cirrhi, while a minority of spores are shot longer distances than those of The predicted gene number in the genome was similar to that in , but had more carbohydrate metabolism-related and transmembrane transport genes. Many transporter genes were differentially expressed during perithecium development in , which may account for its larger perithecia. Comparative analysis of the secondary metabolite gene clusters identified several polyketide synthase genes that were induced during later stages of perithecium development. Deletion of a polyketide synthase gene in resulted in a defective perithecium phenotype, suggesting an important role of the corresponding metabolite, which has yet to be identified, in perithecium development. Results of this study have provided novel insights into the genomic underpinning of development in , which may help elucidate its ability to occupy diverse ecological niches.
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http://dx.doi.org/10.3389/fmicb.2019.01247DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6568001PMC
June 2019

Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in .

mBio 2019 03 26;10(2). Epub 2019 Mar 26.

Department of Biostatistics, Yale University, New Haven, Connecticut, USA

Fungal spores germinate and undergo vegetative growth, leading to either asexual or sexual reproductive dispersal. Previous research has indicated that among developmental regulatory genes, expression is conserved across nutritional environments, whereas pathways for carbon and nitrogen metabolism appear highly responsive-perhaps to accommodate differential nutritive processing. To comprehensively investigate conidial germination and the adaptive life history decision-making underlying these two modes of reproduction, we profiled transcription of germinating on two media: synthetic Bird medium, designed to promote asexual reproduction; and a natural maple sap medium, on which both asexual reproduction and sexual reproduction manifest. A later start to germination but faster development was observed on synthetic medium. Metabolic genes exhibited altered expression in response to nutrients-at least 34% of the genes in the genome were significantly downregulated during the first two stages of conidial germination on synthetic medium. Knockouts of genes exhibiting differential expression across development altered germination and growth rates, as well as in one case causing abnormal germination. A consensus Bayesian network of these genes indicated especially tight integration of environmental sensing, asexual and sexual development, and nitrogen metabolism on a natural medium, suggesting that in natural environments, a more dynamic and tentative balance of asexual and sexual development may be typical of colonies. One of the most remarkable successes of life is its ability to flourish in response to temporally and spatially varying environments. Fungi occupy diverse ecosystems, and their sensitivity to these environmental changes often drives major fungal life history decisions, including the major switch from vegetative growth to asexual or sexual reproduction. Spore germination comprises the first and simplest stage of vegetative growth. We examined the dependence of this early life history on the nutritional environment using genome-wide transcriptomics. We demonstrated that for developmental regulatory genes, expression was generally conserved across nutritional environments, whereas metabolic gene expression was highly labile. The level of activation of developmental genes did depend on current nutrient conditions, as did the modularity of metabolic and developmental response network interactions. This knowledge is critical to the development of future technologies that could manipulate fungal growth for medical, agricultural, or industrial purposes.
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http://dx.doi.org/10.1128/mBio.00192-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6437048PMC
March 2019

The power of discussion: Support for women at the fungal Gordon Research Conference.

Fungal Genet Biol 2018 12 24;121:65-67. Epub 2018 Sep 24.

Department of Plant Biology, Michigan State University, East Lansing, MI 48824-1312, USA.

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http://dx.doi.org/10.1016/j.fgb.2018.09.007DOI Listing
December 2018

Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in Fusarium graminearum.

mBio 2018 08 14;9(4). Epub 2018 Aug 14.

Department of Plant Biology, Michigan State University, East Lansing, Michigan, USA

Long noncoding RNA (lncRNA) plays important roles in sexual development in eukaryotes. In filamentous fungi, however, little is known about the expression and roles of lncRNAs during fruiting body formation. By profiling developmental transcriptomes during the life cycle of the plant-pathogenic fungus , we identified 547 lncRNAs whose expression was highly dynamic, with about 40% peaking at the meiotic stage. Many lncRNAs were found to be antisense to mRNAs, forming 300 sense-antisense pairs. Although small RNAs were produced from these overlapping loci, antisense lncRNAs appeared not to be involved in gene silencing pathways. Genome-wide analysis of small RNA clusters identified many silenced loci at the meiotic stage. However, we found transcriptionally active small RNA clusters, many of which were associated with lncRNAs. Also, we observed that many antisense lncRNAs and their respective sense transcripts were induced in parallel as the fruiting bodies matured. The nonsense-mediated decay (NMD) pathway is known to determine the fates of lncRNAs as well as mRNAs. Thus, we analyzed mutants defective in NMD and identified a subset of lncRNAs that were induced during sexual development but suppressed by NMD during vegetative growth. These results highlight the developmental stage-specific nature and functional potential of lncRNA expression in shaping the fungal fruiting bodies and provide fundamental resources for studying sexual stage-induced lncRNAs. is the causal agent of the head blight on our major staple crops, wheat and corn. The fruiting body formation on the host plants is indispensable for the disease cycle and epidemics. Long noncoding RNA (lncRNA) molecules are emerging as key regulatory components for sexual development in animals and plants. To date, however, there is a paucity of information on the roles of lncRNAs in fungal fruiting body formation. Here we characterized hundreds of lncRNAs that exhibited developmental stage-specific expression patterns during fruiting body formation. Also, we discovered that many lncRNAs were induced in parallel with their overlapping transcripts on the opposite DNA strand during sexual development. Finally, we found a subset of lncRNAs that were regulated by an RNA surveillance system during vegetative growth. This research provides fundamental genomic resources that will spur further investigations on lncRNAs that may play important roles in shaping fungal fruiting bodies.
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http://dx.doi.org/10.1128/mBio.01292-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6094484PMC
August 2018

Light sensing by opsins and fungal ecology: NOP-1 modulates entry into sexual reproduction in response to environmental cues.

Mol Ecol 2018 01 12;27(1):216-232. Epub 2017 Dec 12.

Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA.

Understanding the genetic basis of the switch from asexual to sexual lifestyles in response to sometimes rapid environmental changes is one of the major challenges in fungal ecology. Light appears to play a critical role in the asexual-sexual switch-but fungal genomes harbour diverse light sensors. Fungal opsins are homologous to bacterial green-light-sensory rhodopsins, and their organismal functions in fungi have not been well understood. Three of these opsin-like proteins were widely distributed across fungal genomes, but homologs of the Fusarium opsin-like protein CarO were present only in plant-associated fungi. Key amino acids, including potential retinal binding sites, functionally diverged on the phylogeny of opsins. This diversification of opsin-like proteins could be correlated with life history-associated differences among fungi in their expression and function during morphological development. In Neurospora crassa and related species, knockout of the opsin NOP-1 led to a phenotype in the regulation of the asexual-sexual switch, modulating response to both light and oxygen conditions. Sexual development commenced early in ∆nop-1 strains cultured in unsealed plates under constant blue and white light. Furthermore, comparative transcriptomics showed that the expression of nop-1 is light-dependent and that the ∆nop-1 strain abundantly expresses genes involved in oxidative stress response, genes enriched in NAD/NADP binding sites, genes with functions in proton transmembrane movement and catalase activity, and genes involved in the homeostasis of protons. Based on these observations, we contend that light and oxidative stress regulate the switch via light-responsive and ROS pathways in model fungus N. crassa and other fungi.
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http://dx.doi.org/10.1111/mec.14425DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5797489PMC
January 2018

Surface interactions of Fusarium graminearum on barley.

Mol Plant Pathol 2018 06 20;19(6):1332-1342. Epub 2017 Dec 20.

Department of Plant Biology, Michigan State University, East Lansing, MI 48824, USA.

The filamentous fungus Fusarium graminearum, a devastating pathogen of barley (Hordeum vulgare L.), produces mycotoxins that pose a health hazard. To investigate the surface interactions of F. graminearum on barley, we focused on barley florets, as the most important infection site leading to grain contamination. The fungus interacted with silica-accumulating cells (trichomes and silica/cork cell pairs) on the host surface. We identified variation in trichome-type cells between two-row and six-row barley, and in the role of specific epidermal cells in the ingress of F. graminearum into barley florets. Prickle-type trichomes functioned to trap conidia and were sites of fungal penetration. Infections of more mature florets supported the spread of hyphae into the vascular bundles, whereas younger florets did not show this spread. These differences related directly to the timing and location of increases in silica content during maturation. Focal accumulation of cellulose in infected paleae of two-row and six-row barley indicated that the response is in part linked to trichome type. Overall, silica-accumulating epidermal cells had an expanded role in barley, serving to trap conidia, provide sites for fungal ingress and initiate resistance responses, suggesting a role for silica in pathogen establishment.
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http://dx.doi.org/10.1111/mpp.12616DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638126PMC
June 2018

The ancestral levels of transcription and the evolution of sexual phenotypes in filamentous fungi.

PLoS Genet 2017 Jul 13;13(7):e1006867. Epub 2017 Jul 13.

Department of Biostatistics, Yale University, New Haven, CT, United States of America.

Changes in gene expression have been hypothesized to play an important role in the evolution of divergent morphologies. To test this hypothesis in a model system, we examined differences in fruiting body morphology of five filamentous fungi in the Sordariomycetes, culturing them in a common garden environment and profiling genome-wide gene expression at five developmental stages. We reconstructed ancestral gene expression phenotypes, identifying genes with the largest evolved increases in gene expression across development. Conducting knockouts and performing phenotypic analysis in two divergent species typically demonstrated altered fruiting body development in the species that had evolved increased expression. Our evolutionary approach to finding relevant genes proved far more efficient than other gene deletion studies targeting whole genomes or gene families. Combining gene expression measurements with knockout phenotypes facilitated the refinement of Bayesian networks of the genes underlying fruiting body development, regulation of which is one of the least understood processes of multicellular development.
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http://dx.doi.org/10.1371/journal.pgen.1006867DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5509106PMC
July 2017

Compression tests of Fusarium graminearum ascocarps provide insights into the strength of the perithecial wall and the quantity of ascospores.

Fungal Genet Biol 2016 11 28;96:25-32. Epub 2016 Sep 28.

Department of Plant Pathology, Physiology, and Weed Science, 413 Latham Hall, Virginia Tech, Blacksburg, VA 24061, USA. Electronic address:

The plant pathogenic ascomycete Fusarium graminearum produces perithecia on corn and small grain residues. These perithecia forcibly discharge ascospores into the atmosphere. Little is known about the relationship among the strength of the perithecial wall, the age of the perithecium, and the quantity of ascospores produced. We used a mechanical compression testing instrument to examine the structural failure rate of perithecial walls from three different strains of F. graminearum (two wild type strains, and a mutant strain unable to produce asci). The force required to compress a perithecium by one micrometer (the mean perithecium compression constant, MPCC) was used to determine the strength of the perithecial wall. Over the course of perithecial maturation (5-12days after the initiation of perithecial development), the MPCC was compared to the number of ascospores contained inside the perithecia. The MPCC increased as perithecia matured, from 0.06Nμm at 5d to 0.12Nμm at 12d. The highest number of ascospores was found in older perithecia (12d). The results indicated that for every additional day of perithecial aging, the perithecia become more resilient to compression forces. Every additional day of perithecial aging resulted in ∼900 more ascospores. Knowledge of how perithecia respond to external forces may provide insight into the development of ascospores and the accumulation of turgor pressure. In the future, compression testing may provide a unique method of determining perithecial age in the field, which could extend to management practices that are informed by knowledge of ascospore release and dispersal.
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http://dx.doi.org/10.1016/j.fgb.2016.09.003DOI Listing
November 2016

The Fast-Evolving phy-2 Gene Modulates Sexual Development in Response to Light in the Model Fungus Neurospora crassa.

mBio 2016 Mar 8;7(2):e02148. Epub 2016 Mar 8.

Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut, USA Program in Computational Biology and Bioinformatics, Yale University, New Haven, Connecticut, USA Program in Microbiology, Yale University, New Haven, Connecticut, USA

Unlabelled: Rapid responses to changes in incident light are critical to the guidance of behavior and development in most species. Phytochrome light receptors in particular play key roles in bacterial physiology and plant development, but their functions and regulation are less well understood in fungi. Nevertheless, genome-wide expression measurements provide key information that can guide experiments that reveal how genes respond to environmental signals and clarify their role in development. We performed functional genomic and phenotypic analyses of the two phytochromes in Neurospora crassa, a fungal model adapted to a postfire environment that experiences dramatically variable light conditions. Expression of phy-1 and phy-2 was low in early sexual development and in the case of phy-2 increased in late sexual development. Under light stimulation, strains with the phytochromes deleted exhibited increased expression of sexual development-related genes. Moreover, under red light, the phy-2 knockout strain commenced sexual development early. In the evolution of phytochromes within ascomycetes, at least two duplications have occurred, and the faster-evolving phy-2 gene has frequently been lost. Additionally, the three key cysteine sites that are critical for bacterial and plant phytochrome function are not conserved within fungal phy-2 homologs. Through the action of phytochromes, transitions between asexual and sexual reproduction are modulated by light level and light quality, presumably as an adaptation for fast asexual growth and initiation of sexual reproduction of N. crassa in exposed postfire ecosystems.

Importance: Environmental signals, including light, play critical roles in regulating fungal growth and pathogenicity, and balance of asexual and sexual reproduction is critical in fungal pathogens' incidence, virulence, and distribution. Red light sensing by phytochromes is well known to play critical roles in bacterial physiology and plant development. Homologs of phytochromes were first discovered in the fungal model Neurospora crassa and then subsequently in diverse other fungi, including many plant pathogens. Our study investigated the evolution of red light sensors in ascomycetes and confirmed-using the model fungus Neurospora crassa-their roles in modulating the asexual-sexual reproduction balance in fungi. Our findings also provide a key insight into one of the most poorly understood aspects of fungal biology, suggesting that further study of the function of phytochromes in fungi is critical to reveal the genetic basis of the asexual-sexual switch responsible for fungal growth and distribution, including diverse and destructive plant pathogens.
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http://dx.doi.org/10.1128/mBio.02148-15DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4810495PMC
March 2016

Gene expression differences among three Neurospora species reveal genes required for sexual reproduction in Neurospora crassa.

PLoS One 2014 20;9(10):e110398. Epub 2014 Oct 20.

Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, United States of America; Department of Biostatistics, Yale University, New Haven, Connecticut, United States of America; Program in Computational Biology and Bioinformatics, Yale University, New Haven, Connecticut, United States of America; Program in Microbiology, Yale University, New Haven, Connecticut, United States of America.

Many fungi form complex three-dimensional fruiting bodies, within which the meiotic machinery for sexual spore production has been considered to be largely conserved over evolutionary time. Indeed, much of what we know about meiosis in plant and animal taxa has been deeply informed by studies of meiosis in Saccharomyces and Neurospora. Nevertheless, the genetic basis of fruiting body development and its regulation in relation to meiosis in fungi is barely known, even within the best studied multicellular fungal model Neurospora crassa. We characterized morphological development and genome-wide transcriptomics in the closely related species Neurospora crassa, Neurospora tetrasperma, and Neurospora discreta, across eight stages of sexual development. Despite diverse life histories within the genus, all three species produce vase-shaped perithecia. Transcriptome sequencing provided gene expression levels of orthologous genes among all three species. Expression of key meiosis genes and sporulation genes corresponded to known phenotypic and developmental differences among these Neurospora species during sexual development. We assembled a list of genes putatively relevant to the recent evolution of fruiting body development by sorting genes whose relative expression across developmental stages increased more in N. crassa relative to the other species. Then, in N. crassa, we characterized the phenotypes of fruiting bodies arising from crosses of homozygous knockout strains of the top genes. Eight N. crassa genes were found to be critical for the successful formation of perithecia. The absence of these genes in these crosses resulted in either no perithecium formation or in arrested development at an early stage. Our results provide insight into the genetic basis of Neurospora sexual reproduction, which is also of great importance with regard to other multicellular ascomycetes, including perithecium-forming pathogens, such as Claviceps purpurea, Ophiostoma ulmi, and Glomerella graminicola.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0110398PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4203796PMC
July 2015

Global gene expression and focused knockout analysis reveals genes associated with fungal fruiting body development in Neurospora crassa.

Eukaryot Cell 2014 Jan 15;13(1):154-69. Epub 2013 Nov 15.

Department of Biostatistics, Yale University, New Haven, Connecticut, USA.

Fungi can serve as highly tractable models for understanding genetic basis of sexual development in multicellular organisms. Applying a reverse-genetic approach to advance such a model, we used random and multitargeted primers to assay gene expression across perithecial development in Neurospora crassa. We found that functionally unclassified proteins accounted for most upregulated genes, whereas downregulated genes were enriched for diverse functions. Moreover, genes associated with developmental traits exhibited stage-specific peaks of expression. Expression increased significantly across sexual development for mating type gene mat a-1 and for mat A-1 specific pheromone precursor ccg-4. In addition, expression of a gene encoding a protein similar to zinc finger, stc1, was highly upregulated early in perithecial development, and a strain with a knockout of this gene exhibited arrest at the same developmental stage. A similar expression pattern was observed for genes in RNA silencing and signaling pathways, and strains with knockouts of these genes were also arrested at stages of perithecial development that paralleled their peak in expression. The observed stage specificity allowed us to correlate expression upregulation and developmental progression and to identify regulators of sexual development. Bayesian networks inferred from our expression data revealed previously known and new putative interactions between RNA silencing genes and pathways. Overall, our analysis provides a fine-scale transcriptomic landscape and novel inferences regarding the control of the multistage development process of sexual crossing and fruiting body development in N. crassa.
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http://dx.doi.org/10.1128/EC.00248-13DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3910948PMC
January 2014

Fusarium pathogenomics.

Annu Rev Microbiol 2013 ;67:399-416

Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, Massachusetts 01003; email:

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.
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http://dx.doi.org/10.1146/annurev-micro-092412-155650DOI Listing
March 2014

Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses.

Nat Genet 2012 Sep 12;44(9):1060-5. Epub 2012 Aug 12.

Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.

Colletotrichum species are fungal pathogens that devastate crop plants worldwide. Host infection involves the differentiation of specialized cell types that are associated with penetration, growth inside living host cells (biotrophy) and tissue destruction (necrotrophy). We report here genome and transcriptome analyses of Colletotrichum higginsianum infecting Arabidopsis thaliana and Colletotrichum graminicola infecting maize. Comparative genomics showed that both fungi have large sets of pathogenicity-related genes, but families of genes encoding secreted effectors, pectin-degrading enzymes, secondary metabolism enzymes, transporters and peptidases are expanded in C. higginsianum. Genome-wide expression profiling revealed that these genes are transcribed in successive waves that are linked to pathogenic transitions: effectors and secondary metabolism enzymes are induced before penetration and during biotrophy, whereas most hydrolases and transporters are upregulated later, at the switch to necrotrophy. Our findings show that preinvasion perception of plant-derived signals substantially reprograms fungal gene expression and indicate previously unknown functions for particular fungal cell types.
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http://dx.doi.org/10.1038/ng.2372DOI Listing
September 2012

Transcriptome analyses during fruiting body formation in Fusarium graminearum and Fusarium verticillioides reflect species life history and ecology.

Fungal Genet Biol 2012 Aug 15;49(8):663-73. Epub 2012 Jun 15.

Department of Plant Biology, Michigan State University, East Lansing, MI 48824, USA.

Fusarium graminearum and F. verticillioides are devastating cereal pathogens with very different life history and ecological characteristics. F. graminearum is homothallic, and sexual spores are an important component of its life cycle, responsible for disease initiation. F. verticilloides is heterothallic, and produces only modest numbers of fruiting bodies, which are not a significant source of inoculum. To identify corresponding differences in the transcriptional program underlying fruiting body development in the two species, comparative expression was performed, analyzing six developmental stages. To accompany the transcriptional analysis, detailed morphological characterization of F. verticillioides development was performed and compared to a previous morphological analysis of F. graminearum. Morphological development was similar between the two species, except for the observation of possible trichogynes in F. verticillioides ascogonia, which have not been previously reported for any Fusarium species. Expression of over 9000 orthologous genes were measured for the two species. Functional assignments of highly expressed orthologous genes at each time-point revealed the majority of highly expressed genes fell into the "unclassified proteins" category, reflecting the lack of characterization of genes for sexual development in both species. Simultaneous examination of morphological development and stage-specific gene expression suggests that degeneration of the paraphyses during sexual development is an apoptotic process. Expression of mating type genes in the two species differed, possibly reflecting the divergent roles they play in sexual development. Overall, the differences in gene expression reflect the greater role of fruiting bodies in the life cycle and ecology of F. graminearum versus F. verticillioides.
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http://dx.doi.org/10.1016/j.fgb.2012.05.009DOI Listing
August 2012

Role of Fig1, a component of the low-affinity calcium uptake system, in growth and sexual development of filamentous fungi.

Eukaryot Cell 2012 Aug 25;11(8):978-88. Epub 2012 May 25.

Genetics Graduate Program, Michigan State University, East Lansing, Michigan, USA.

The function of Fig1, a transmembrane protein of the low-affinity calcium uptake system (LACS) in fungi, was examined for its role in the growth and development of the plant pathogen Fusarium graminearum. The Δfig1 mutants failed to produce mature perithecia, and sexual development was halted prior to the formation of perithecium initials. The loss of Fig1 function also resulted in a reduced vegetative growth rate. Macroconidium production was reduced 70-fold in the Δfig1 mutants compared to the wild type. The function of the high-affinity calcium uptake system (HACS), comprised of the Ca(2+) channels Mid1 and Cch1, was previously characterized for F. graminearum. To better understand the roles of the LACS and the HACS, Δfig1 Δmid1, Δfig1 Δcch1, and Δfig1 Δmid1 Δcch1 double and triple mutants were generated, and the phenotypes of these mutants were more severe than those of the Δfig1 mutants. Pathogenicity on wheat was unaffected for the Δfig1 mutants, but the Δfig1 Δmid1, Δfig1 Δcch1, and Δfig1 Δmid1 Δcch1 mutants, lacking both LACS and HACS functions, had reduced pathogenicity. Additionally, Δfig1 mutants of Neurospora crassa were examined and did not affect filamentous growth or female fertility in a Δfig1 mating type A strain, but the Δfig1 mating type a strain failed to produce fertile fruiting bodies. These results are the first report of Fig1 function in filamentous ascomycetes and expand its role to include complex fruiting body and ascus development.
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http://dx.doi.org/10.1128/EC.00007-12DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3416067PMC
August 2012

Sexual development and ascospore discharge in Fusarium graminearum.

J Vis Exp 2012 Mar 29(61). Epub 2012 Mar 29.

Genetics Program, Michigan State University, USA.

Fusarium graminearum has become a model system for studies in development and pathogenicity of filamentous fungi. F. graminearum most easily produces fruiting bodies, called perithecia, on carrot agar. Perithecia contain numerous tissue types, produced at specific stages of perithecium development. These include (in order of appearance) formation of the perithecium initials (which give rise to the ascogenous hyphae), the outer wall, paraphyses (sterile mycelia which occupy the center of the perithecium until the asci develop), the asci, and the ascospores within the asci. The development of each of these tissues is separated by approximately 24 hours and has been the basis of transcriptomic studies during sexual development. Refer to Hallen et al. (2007) for a more thorough description of development, including photographs of each stage. Here, we present the methods for generating and harvesting synchronously developing lawns of perithecia for temporal studies of gene regulation, development, and physiological processes. Although these methods are written specifically to be used with F. graminearum, the techniques can be used for a variety of other fungi, provided that fruiting can be induced in culture and there is some synchrony to development. We have recently adapted this protocol to study the sexual development of F. verticillioides. Although individual perithecia must be hand picked in this species, because a lawn of developing perithecia could not be induced, the process worked well for studying development (Sikhakolli and Trail, unpublished). The most important function of fungal fruiting bodies is the dispersal of spores. In many of the species of Ascomycota (ascus producing fungi), spores are shot from the ascus, due to the generation of turgor pressure within the ascus, driving ejection of spores (and epiplasmic fluid) through the pore in the ascus tip. Our studies of forcible ascospore discharge have resulted in development of a "spore discharge assay", which we use to screen for mutations in the process. Here we present the details of this assay. F. graminearum is homothallic, and thus can form fruiting bodies in the absence of a compatible partner. The advantage of homothallism is that crossing is not necessary to generate offspring homozygous for a particular trait, a facet that has facilitated the study of sexual development in this species. However, heterothallic strains have been generated that can be used for crossing. It is also possible to cross homothallic strains to obtain mutants for several genes in one strain. This is done by coinoculating one Petri dish with 2 strains. Along the meeting point, the majority of perithecia will be recombinant (provided a mutation in one of the parent strains does not inhibit outcrossing). As perithecia age, they exude ascospores en masse instead of forcibly discharging them. The resulting spore exudate (called a cirrhus) sits at the tip of the perithecium and can easily be removed for recovery of individual spores. Here we present a protocol to facilitate the identification of recombinant perithecia and the recovery of recombinant progeny.
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http://dx.doi.org/10.3791/3895DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3460587PMC
March 2012

Differential impact of nutrition on developmental and metabolic gene expression during fruiting body development in Neurospora crassa.

Fungal Genet Biol 2012 May 26;49(5):405-13. Epub 2012 Mar 26.

Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520, USA.

Fungal fruiting body size and form are influenced by the ecology of the species, including diverse environmental stimuli. Accordingly, nutritional resources available to the fungus during development can be vital to successful production of fruiting bodies. To investigate the effect of nutrition, perithecial development of Neurospora crassa was induced on two different media, a chemically sparsely nutritive Synthetic Crossing Medium (SCM) and a natural Carrot Agar (CA). Protoperithecia were collected before crossing, and perithecia were collected at 2, 24, 48, 72, 96, 120, and at full maturity 144 h after crossing. No differences in fruiting body morphology were observed between the two media at any time point. A circuit of microarray hybridizations comparing cDNA from all neighboring stages was performed. For a majority of differentially expressed genes, expression was higher in SCM than in CA, and expression of core metabolic genes was particularly affected. Effects of nutrition were highest in magnitude before crossing, lowering in magnitude during early perithecial development. Interestingly, metabolic effects of the media were also large in magnitude during late perithecial development, at which stage the lower expression in CA presumably reflected the continued intake of diverse complex initial compounds, diminishing the need for expression of anabolic pathways. However, for genes with key regulatory roles in sexual development, including pheromone precursor ccg-4 and poi2, expression patterns were similar between treatments. When possible, a common nutritional environment is ideal for comparing transcriptional profiles between different fungi. Nevertheless, the observed consistency of the developmental program across media, despite considerable metabolic differentiation is reassuring. This result facilitates comparative studies that will require different nutritional resources for sexual development in different fungi.
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http://dx.doi.org/10.1016/j.fgb.2012.03.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3397380PMC
May 2012

Fusarium graminearum from expression analysis to functional assays.

Methods Mol Biol 2011 ;722:79-101

Department of Plant Biology, Michigan State University, East Lansing, MI, USA.

Fusarium graminearum, the causal agent of head blight of wheat, was the third filamentous fungus to have a completed genome sequence. Since the release of the genome sequence in 2003, F. graminearum has become a model for studies of genomics and transcriptomics, mycotoxins, fungal population genetics, gene function, and sexual development. Herein we present the techniques we have used in our laboratory to perform expression analyses on life cycle stages of F. graminearum and techniques to functionally characterize those genes identified as potentially interesting.
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http://dx.doi.org/10.1007/978-1-61779-040-9_6DOI Listing
September 2011

Deoxynivalenol biosynthesis-related gene expression during wheat kernel colonization by Fusarium graminearum.

Phytopathology 2011 Sep;101(9):1091-6

Department of Plant Biology, Michigam State University, East Lansing, MI, USA.

Deoxynivalenol (DON) is a potent mycotoxin and virulence factor produced by Fusarium graminearum. We examined the expression of the core DON biosynthetic gene Tri5 during wheat head infection of susceptible and resistant cultivars and susceptible cultivars treated with strobilurin fungicides (e.g., azoxystrobin). DON was quantified to correlate expression with toxin accumulation. The highest Tri5 expression relative to housekeeping genes occurred at the infection front. As infection progressed, earliest-infected kernels showed diminished relative Tri5 expression but Tri5 expression never ceased during the 21 days observed. Azoxystrobin treatment showed no significant effect on either relative Tri5 expression or DON quantity. The resistant cultivar 'Alsen' showed minimal spread of the fungus, with no fungus detected by day 21. DON was not detected in significant quantities in Alsen in the later stages sampled. In Wheaten, DON levels were negligible at 8 days postinoculation (dpi), with detectable DON at later-sampled time points. Tri5 was detected even in fully senesced kernels 21 dpi. Our data demonstrate the presence of Tri5 transcripts in a susceptible cultivar over a much longer time period than has been previously documented. This suggests the ability of the fungus to rapidly resume toxin biosynthesis in dried infected grain should conducive environmental conditions be present, and provides a possible mechanism for high DON levels in asymptomatic grain.
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http://dx.doi.org/10.1094/PHYTO-01-11-0023DOI Listing
September 2011

Mid1, a mechanosensitive calcium ion channel, affects growth, development, and ascospore discharge in the filamentous fungus Gibberella zeae.

Eukaryot Cell 2011 Jun 25;10(6):832-41. Epub 2011 Feb 25.

Department of Plant Biology, Michigan State University, 342 Plant Biology Laboratory, East Landing, MI 48824-1312, USA.

The role of Mid1, a stretch-activated ion channel capable of being permeated by calcium, in ascospore development and forcible discharge from asci was examined in the pathogenic fungus Gibberella zeae (anamorph Fusarium graminearum). The Δmid1 mutants exhibited a >12-fold reduction in ascospore discharge activity and produced predominately abnormal two-celled ascospores with constricted and fragile septae. The vegetative growth rate of the mutants was ∼50% of the wild-type rate, and production of macroconidia was >10-fold lower than in the wild type. To better understand the role of calcium flux, Δmid1 Δcch1 double mutants were also examined, as Cch1, an L-type calcium ion channel, is associated with Mid1 in Saccharomyces cerevisiae. The phenotype of the Δmid1 Δcch1 double mutants was similar to but more severe than the phenotype of the Δmid1 mutants for all categories. Potential and current-voltage measurements were taken in the vegetative hyphae of the Δmid1 and Δcch1 mutants and the wild type, and the measurements for all three strains were remarkably similar, indicating that neither protein contributes significantly to the overall electrical properties of the plasma membrane. Pathogenicity of the Δmid1 and Δmid1Δcch1 mutants on the host (wheat) was not affected by the mutations. Exogenous calcium supplementation partially restored the ascospore discharge and vegetative growth defects for all mutants, but abnormal ascospores were still produced. These results extend the known roles of Mid1 to ascospore development and forcible discharge. However, Neurospora crassa Δmid1 mutants were also examined and did not exhibit defects in ascospore development or in ascospore discharge. In comparison to ion channels in other ascomycetes, Mid1 shows remarkable adaptability of roles, particularly with regard to niche-specific adaptation.
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http://dx.doi.org/10.1128/EC.00235-10DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3127676PMC
June 2011

A novel gene, ROA, is required for normal morphogenesis and discharge of ascospores in Gibberella zeae.

Eukaryot Cell 2010 Oct 27;9(10):1495-503. Epub 2010 Aug 27.

Department of Agricultural Biotechnology, Center for Fungal Pathogenesis, Seoul National University, Republic of Korea.

Head blight, caused by Gibberella zeae, is a significant disease among cereal crops, including wheat, barley, and rice, due to contamination of grain with mycotoxins. G. zeae is spread by ascospores forcibly discharged from sexual fruiting bodies forming on crop residues. In this study, we characterized a novel gene, ROA, which is required for normal sexual development. Deletion of ROA (Δroa) resulted in an abnormal size and shape of asci and ascospores but did not affect vegetative growth. The Δroa mutation triggered round ascospores and insufficient cell division after spore delimitation. The asci of the Δroa strain discharged fewer ascospores from the perithecia but achieved a greater dispersal distance than those of the wild-type strain. Turgor pressure within the asci was calculated through the analysis of osmolytes in the epiplasmic fluid. Deletion of the ROA gene appeared to increase turgor pressure in the mutant asci. The higher turgor pressure of the Δroa mutant asci and the mutant spore shape contributed to the longer distance dispersal. When the Δroa mutant was outcrossed with a Δmat1-2 mutant, a strain that contains a green fluorescence protein (GFP) marker in place of the MAT1-2 gene, unusual phenotypic segregation occurred. The ratio of GFP to non-GFP segregation was 1:1; however, all eight spores had the same shape. Taken together, the results of this study suggest that ROA plays multiple roles in maintaining the proper morphology and discharge of ascospores in G. zeae.
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http://dx.doi.org/10.1128/EC.00083-10DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2950417PMC
October 2010

A partial chromosomal deletion caused by random plasmid integration resulted in a reduced virulence phenotype in Fusarium graminearum.

Mol Plant Microbe Interact 2010 Aug;23(8):1083-96

Department of Plant Pathology and Microbiology, Rothamsted Research, Harpenden, Herts, UK.

Fusarium graminearum (teleomorph: Gibberella zeae) is an Ascomycete fungal plant pathogen which infects a range of agriculturally important crops, including wheat, barley, and maize. A random plasmid insertion mutagenesis approach was used to analyze the pathogenicity of the PH-1 strain, for which full genomic information is available. Fungal transformants were initially screened for their ability to infect wheat ears. From a total of 1,170 transformants screened, eight were confirmed to be highly reduced in pathogenicity toward wheat ears and roots. These were designated disease-attenuated F. graminearum (daf) mutants. The in vitro growth rate and appearance of each daf mutant was equivalent to the parental strain. Deoxynivalenol (DON) was not detected in threshed grain recovered from ears inoculated with the daf10 mutant. Plasmid rescue and sequencing of the mutant daf10 revealed a deletion of approximately 350 kb from one end of chromosome 1. This chromosome segment is predicted to contain 146 genes. Microarray analysis of daf10 gene expression during growth in DON-inducing conditions confirmed the large deletion. The identities of the genes deleted and their potential role in DON production, pathogenesis, and other life processes are discussed.
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http://dx.doi.org/10.1094/MPMI-23-8-1083DOI Listing
August 2010

Atrazine binds to the growth hormone-releasing hormone receptor and affects growth hormone gene expression.

Environ Health Perspect 2010 Oct 8;118(10):1400-5. Epub 2010 Jun 8.

Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824, USA.

Background: Atrazine (ATR), a commonly used herbicide in the United States, is widely distributed in water and soil because of its mobility through ecosystems and its persistence in the environment. ATR has been associated with defects in sexual development in animals, but studies on mammalian systems have failed to clearly identify a cellular target.

Objectives: Our goal in this study was to identify a ligand-binding receptor for ATR in pituitary cells that may explain the mechanism of action at the gene expression level.

Methods: We used pituitary cells from postnatal day 7 male rats and pituitary cell lines to study the effect of ATR on gene expression of growth hormone (GH), luteinizing hormone (LH), and prolactin (PRL) at RNA and protein levels. 14C-ATR was used to determine its specific binding to the growth hormone-releasing hormone receptor (GHRHR). The effect of ATR on structural proteins was visualized using immunofluorescent in situ staining.

Results: The treatment of rat pituitary cells with ATR, at environmentally relevant concentrations (1 ppb and 1 ppm), resulted in a reduction of GH expression. This effect appeared to result from the inhibition of GH gene transcription due to ATR binding to the GHRHR of the pituitary cells.

Conclusions: Identification of GHRHR as the target of ATR is consistent with the myriad effects previously reported for ATR in mammalian systems. These findings may lead to a better understanding of the hazards of environmental ATR contamination and inform efforts to develop guidelines for establishing safe levels in water systems.
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http://dx.doi.org/10.1289/ehp.0900738DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2957919PMC
October 2010

Triacylglyceride metabolism by Fusarium graminearum during colonization and sexual development on wheat.

Mol Plant Microbe Interact 2009 Dec;22(12):1492-503

Department of Plant Biology, Michigan State University, East Lansing, MI 48824, USA.

Fusarium graminearum, a devastating pathogen of small grains, overwinters on crop residues and produces ephemeral perithecia. Accumulation of lipids in overwintering hyphae would provide reserves for overwinter survival and perithecium development. Fatty acid composition of cultures during perithecium development indicated a drop in neutral lipid levels during development but little change in fatty acid composition across stages. Microscopic examination of cultures early in sexual development revealed hyphal cells engorged with lipid bodies. In comparison, vegetative hyphae contained few lipid bodies. Microarray analysis was performed on wheat stems at stages of colonization through perithecium development. Gene expression analysis during stages of perithecium development both in planta and in vitro (previously published) supports the view that lipid biosynthesis occurs during early stages of wheat colonization leading to sexual development and that lipid oxidation occurs as perithecia are developing. Analysis of gene expression during the stages of wheat stem colonization also revealed sets of genes unique to these stages. These results support the view that lipids accumulate in hyphae colonizing wheat stalks and are subsequently used in perithecium formation on stalk tissue. These results indicate that extensive colonization of plant tissue prior to harvest is essential for subsequent sporulation on crop residues and, thus, has important implications for inoculum reduction.
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http://dx.doi.org/10.1094/MPMI-22-12-1492DOI Listing
December 2009

For blighted waves of grain: Fusarium graminearum in the postgenomics era.

Authors:
Frances Trail

Plant Physiol 2009 Jan;149(1):103-10

Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824-1312, USA.

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http://dx.doi.org/10.1104/pp.108.129684DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2613717PMC
January 2009

The L-type calcium ion channel cch1 affects ascospore discharge and mycelial growth in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum).

Eukaryot Cell 2008 Feb 14;7(2):415-24. Epub 2007 Dec 14.

Department of Plant Biology, Michigan State University, East Lansing, MI 48824-1312, USA.

Cch1, a putative voltage-gated calcium ion channel, was investigated for its role in ascus development in Gibberella zeae. Gene replacement mutants of CCH1 were generated and found to have asci which did not forcibly discharge spores, although morphologically ascus and ascospore development in the majority of asci appeared normal. Additionally, mycelial growth was significantly slower, and sexual development was slightly delayed in the mutant; mutant mycelia showed a distinctive fluffy morphology, and no cirrhi were produced. Wheat infected with Deltacch1 mutants developed symptoms comparable to wheat infected with the wild type; however, the mutants showed a reduced ability to protect the infected stalk from colonization by saprobic fungi. Transcriptional analysis of gene expression in mutants using the Affymetrix Fusarium microarray showed 2,449 genes with significant, twofold or greater, changes in transcript abundance across a developmental series. This work extends the role of CCH1 to forcible spore discharge in G. zeae and suggests that this channel has subtle effects on growth and development.
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http://dx.doi.org/10.1128/EC.00248-07DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2238158PMC
February 2008

The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization.

Science 2007 Sep;317(5843):1400-2

Broad Institute of the Massachusetts Institute of Technology and Harvard, Cambridge, MA 02142, USA.

We sequenced and annotated the genome of the filamentous fungus Fusarium graminearum, a major pathogen of cultivated cereals. Very few repetitive sequences were detected, and the process of repeat-induced point mutation, in which duplicated sequences are subject to extensive mutation, may partially account for the reduced repeat content and apparent low number of paralogous (ancestrally duplicated) genes. A second strain of F. graminearum contained more than 10,000 single-nucleotide polymorphisms, which were frequently located near telomeres and within other discrete chromosomal segments. Many highly polymorphic regions contained sets of genes implicated in plant-fungus interactions and were unusually divergent, with higher rates of recombination. These regions of genome innovation may result from selection due to interactions of F. graminearum with its plant hosts.
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http://dx.doi.org/10.1126/science.1143708DOI Listing
September 2007