SAES-422 Multistate Research Activity Accomplishments Report
Sections
Status: Approved
Basic Information
- Project No. and Title: NCCC_old307 : Biochemistry and Genetics of Plant-Fungal Interactions
- Period Covered: 10/01/2017 to 10/27/2018
- Date of Report: 11/27/2018
- Annual Meeting Dates: 10/25/2018 to 10/26/2018
Participants
Dr. Tim Friesen, USDA-ARS Red River Agricultural Research Center Dr. Jonathon Richards, Louisiana State University Dr. Zhaohui Liu, USDA-ARS Red River Agricultural Research Center Dr. Regina Redman, Adaptive Symbiotic Technologies Seattle, WA Dr. Rusty Rodriguez, Adaptive Symbiotic Technologies Seattle, WA Dr. Marilyn J. Roossinck, Pennsylvania State University Dr. Richard Todd, Kansas State University Dr. Nancy Keller, University of Wisconsin Dr. Frances Trail, Michigan State University Dr. Thomas Wolpert, Oregon State University Dr. Jennifer Lorang, Oregon State University Dr. Dallice Mills, Oregon State University Dr. Michael Freitag, Oregon State University Dr. Patricia Ferreira Dos Santos, University of Nevada, Reno Dr. Daren Brown, USDA-ARS Peoria, Illinois Dr. Scott Gold, USDA-ARS, University of Georgia, Athens
Summary of Minutes:
NCCC-307 Meeting Minutes – Oct. 25-27, 2017, Corvallis, OR
Oct. 25 Keynote Seminar followed by Greeting at Bombs Away Cafe
4:00 P.M. Botany and Plant Pathology Departmental Seminar, Room 4001 ALS
Dr. Rusty Rodriguez, Adaptive Symbiotic Technologies, Seattle, Washington
Ensuring Food Security in a Changing Climate by Generating Stress Tolerant, Nutritionally Independent Crops via Fungal Symbiosis
Oct. 26 Courtyard Marriot Hotel, Corvallis, OR 9:00 Set-up, Coffee mixer
9:15 Introduction, Jennifer Lorang
9:30 A.M. ZOOM meeting with NCCC-307 Administrative Advisor. Dr. Martin Draper addressed the group regarding our renewal and review.
10:00 A.M.- Speakers and open discussion
Dr. Frances Trail, Michigan State University
A search for antifungals in nature: The use of specialized metabolism in microbial communities.
Dr. Scott Gold, USDA-ARS, Athens, Georgia
Fungal lactamases in plant-fungus and microbe-fungus interactions, mostly what we don’t know…
Discussion of collaborative efforts- All
Break at 12:30
2:00 P.M.- Speakers and open discussion
Dr. Marilyn Roossinck, Plant Pathology and Environmental Microbiology, and Biology Center for Infectious Disease Dynamics, Penn State University
BEAST analysis of Pseudogymnoascus destructans partitivirus maps the spread of white nose syndrome from Kentucky to the west coast.
Dr. Jon Richards, USDA-ARS North Dakota State University
"Two for one: a single necrotrophic effector from Parastagonospora nodorum targets two non-homoeologous wheat sensitivity genes".
4:00-5 Ongoing discussion regarding collaborative efforts, with catered appetizers and beverages
Dinner 6, more informal discussion.
Oct 27 10:00 Mycology field trip to MacDonald Forest, Corvallis, OR
Meeting Abstracts
A search for antifungals in nature: The use of specialized metabolism in microbial communities.
Frances Trail, Ludmila Roze and John Linz.
Lichens are some of the longest-living organisms known, despite their slow growth and they very rarely appear to die of disease. The lichenized fungus establishes the main lichen thallus in association with an alga or cyanobacterium. This scaffold becomes a niche for a variety of other filamentous ascomycetes and basidiomycetes, yeasts, bacteria, and occasionally insects. Lichens are known to produce a plethora of unique secondary compounds. Their longevity, and robustness despite a close association with diverse microbes provides an interesting study system to view the role of secondary metabolites in managing a microbial community. We isolated extracts from 72 lichen species and tested for their effects on sporulation, hyphal growth and secondary metabolite production in fungal cultures. The structure of these compounds is under investigation, as is the identification of the microbial source. Interestingly, the most common activity by far among the lichen extracts had the effect of arresting secondary metabolite production. This finding suggests that lichens attenuate negative interactions with the incumbent fungi due to their ability to regulate secondary metabolism.
Virus as a tool to study epidemiology: How is WNS moving, and where did the Washington isolate come from?
Marilyn J. Roossinck1, Vaskar Thapa1, Gregory G. Turner2
1Department of Plant Pathology and Environmental Microbiology, Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA 16802, USA.
2Pennsylvania Game Commission, Harrisburg, PA 17110, USA
Earlier we reported the infection of a novel partitivirus, Pseudogymnoascus destructans partitivirus-pa (PdPV), in North American isolates of Pseudogymnoascus destructans (Pd). We showed that the diversity of the PdPV coat protein sequences can be explained by geographical origin. Further, we proposed that the geographical adaptation of the virus could be used as a tool to study the spread of WNS. Currently we have expanded our sampling size to over 100 isolates from diverse locations in North America and applied the most rigorous phylogeographic analysis tool, Baysian Evolutionary Analysis Sampling Trees (BEAST) to trace the spread of the disease. We found a positive temporal signature between the divergence of coat protein sequence of PdPV and the sampling dates. The relationship predicts a mean substitution rate of 2.2X10-3 substitutions per site per year with 95% credibility interval in the coat protein sequence of the virus, which is similar to many RNA virus evolutionary rate. Through BEAST, we infer that the Time to the Most Recent Common Ancestor of PdPV in Pd is somewhere in the mid 1990s. This confirms recent introduction of the virus-infected fungus in North America. The analysis further indicates that the longest spread of the fungus (almost 1300 miles) to Washington State has roots in isolates from Kentucky. The large sampling size from diverse locations in combination with the rigorous phylogeographic analysis in BEAST substantiate our early prediction that a persistence virus infection in a pathogen like Pd can be a tool to study the epidemiology of a pathogen. Many important epidemiological factors such as prediction of spread, the Most Recent Common Ancestor and the evolutionary rate associated with PdPV derived in this study validate our conclusions.
Two for one: a single necrotrophic effector from Parastagonospora nodorum targets two non-homeologous wheat sensitivity genes.
Jonathan K. Richards
JRichards@agcenter.lsu.edu
Septoria nodorum blotch, caused by the necrotrophic fungal pathogen Parastagonospora nodorum, is an economically important pathogen of cultivated wheat. Disease is typically facilitated through the production of necrotrophic effectors, which elicit program cell death through the direct or indirect interaction with host sensitivity genes. Although nine effector-host sensitivity gene interaction have been identified, only three P. nodorum necrotrophic effectors, including SnToxA, SnTox1, and SnTox3 have been cloned and characterized. This research presents the whole-genome sequencing of 198 diverse P. nodorum isolates from the United States and the implementation of a genome-wide association mapping methodology for effector identification. Using 322,613 single nucleotide polymorphism (SNP) and insertion/deletion (InDel) markers, a single locus was found to be significantly associated with virulence on BG223 (Snn2+) and ITMI37 (Snn6+). Analysis of annotated genes underlying the association revealed a single gene encoding a predicted secreted protein, candidate SnTox2/6. The development of gene disruption mutants of SnTox2/6 in isolate Sn4 abolished the interaction with Snn2 and Snn6, as evidenced by inoculation and QTL analysis of the BG and ITMI populations, respectively. Additionally, transformation of avirulent isolate Sn79 with a functional copy of SnTox2/6 resulted in virulence on lines harboring Snn2 or Snn6. Gene expression analysis was conducted via qPCR, revealing 24 hours post-inoculation as the timepoint of highest gene expression. Also, protein structural homology searches yielded chitin-binding as a potential secondary function, similar to SnTox1. Taken together, these results indicate that SnTox2/6 is a single small secreted protein that targets two non-homoeologous host sensitivity genes to induce programmed cell death.
Dr. Scott Gold, USDA-ARS, Athens, Georgia
Fungal lactamases in plant-fungus and microbe-fungus interactions, mostly what we don’t know…
Because of the way soil fungi grow and feed they are exposed to many other organisms. Antibiosis is a common means of competition between fungi and other microbes. Successful competitors must be able to counter antibiotic effects. This is frequently achieved by enzymatic degradation of antibiotics. It has long been known that bacteria protect themselves from beta-lactam antibiotics like penicillin by the action of enzymes called beta-lactamases. Beta-lactam antibiotics interfere with bacterial cell wall production. Examination of fungal genomes shows that many contain genes that look like beta-lactamases even though they are unaffected by beta-lactam antibiotics and their cell wall is completely different from bacteria. In this paper we describe the distribution lactamases in fungi with particular focus on Fusarium verticillioides, a producer of the fumonisin type mycotoxins. Fusarium species and other fungi associated with soil environments have many more of these genes than those fungi that do not encounter the soil. Evidence in F. verticillioides suggests that many of these enzymes may degrade higher order lactam compounds, and such degradation may enhance the fitness of this fungus to compete in the environment.
Accomplishments
Accomplishments: The NCCC307 committee membership has collectively increased the knowledge of genetics and biochemistry of plant-fungal interactions during the past year. Their findings include, but are not limited to (1) Identification of newly emerging and endemic pathogens, characterization of pathogen population diversity, fungal community interactions, and symbiotic interactions among fungi, plants, bacteria and viruses. (2) Evaluation of crop and model plant germplasm for disease susceptibility/ resistance resulting in gene mapping, cloning and establishment of useful markers for breeding. (3) Identification and characterization of pathogenicity determinants from a number of phytopathogenic fungi through comparative and function genomic analyses. (4) Increased knowledge of gene cluster evolutionary dynamics and roles clusters play in fungal secondary metabolism diversity. (5) Increase knowledge of regulators of fungal development required for epidemiological and infection processes. (6) Elucidation of gene flow dynamics among fungal populations underpinning host specificity and virulence traits. The group has produced at least 83 peer-reviewed journal publications in the 2017-2018 reporting period.
Impacts
- Impact Statement: The research findings and communication of the resulting knowledge in peer-and non-peer-reviewed publications by NCCC307 members has increased understandings of plant-fungal interactions in terms of host susceptibility, pathogen virulence mechanisms and fungal-plant interactions on multiple parasitic (mutualism to pathogenic) levels. There has been a significant exchange of data among members of the group that has expedited research findings and has also resulted in new ideas for grant proposals. The knowledge gained impacts strategies used by crop breeders, farm managers and regulatory agencies for insuring the productivity and safety of plan-based agriculture products in the US.
Publications
Publications
Ali, A., and Roossinck, M. J. 2017. Analysis of quasispecies variation in single and mixed viral infection. Virus Evol. 3. https://doi.org/10.1093/ve/vex037
Ameen, G., Kariyawasam, G., Shi, G., Friesen, T. L., Faris, J. D., Ali, S., et al. 2017. Molecular manipulation of the mating-type system and development of a new approach for characterizing pathogen virulence in Pyrenophora tritici-repentis. Fungal Genetics and Biology. 109:16–25.
Hernández-Pinzón, I., Holden, S., Lorang, J., and Moscou, M.J. 2017. An ancient integration in a plant NLR is maintained as a trans-species polymorphism | bioRxiv. https://doi.org/10.1101/239541
Bian, Z., Ni, Y., Xu, JR. et al. Cell. Mol. Life Sci. 2018. A-to-I mRNA editing in fungi: occurrence, function, and evolution | SpringerLink. https://doi.org/10.1007/s00018-018-2936-3
Bakker, M. G., Brown, D. W., Kelly, A. C., Kim, H.-S., Kurtzman, C. P., Mccormick, S. P., et al. 2018. Fusarium mycotoxins: a trans-disciplinary overview. Canadian Journal of Plant Pathology. 40:161–171.
Blei, F., Fricke, J., Wick, J., Slot, J. C., and Hoffmeister, D. 2018. Iterative l-Tryptophan Methylation in Psilocybe Evolved by Subdomain Duplication. ChemBioChem. 19:2160–2166.
Boyce, G., Gluck-Thaler, E., Slot, J. C., Stajich, J. E., Davis, W. J., James, T. Y., et al. 2018. Discovery of psychoactive plant and mushroom alkaloids in behavior-modifying fungal cicada pathogens. bioRxiv. :375105.
Chen, D., Wu, C., Hao, C., Huang, P., Liu, H., Bian, Z., et al. 2018. Sexual specific functions of Tub1 beta-tubulins require stage-specific RNA processing and expression in Fusarium graminearum. Environmental Microbiology. 20:4009–4021.
Connell, L., Segee, B., Redman, R., Rodriguez, R. J., and Staudigel, H. 2018. Biodiversity and Abundance of Cultured Microfungi from the Permanently Ice-Covered Lake Fryxell, Antarctica. Life. 8:37.
DeIulio, G. A., Guo, L., Zhang, Y., Goldberg, J. M., Kistler, H. C., and Ma, L.-J. 2018. Kinome Expansion in the Fusarium oxysporum Species Complex Driven by Accessory Chromosomes. mSphere. 3:e00231-18.
Dickman, M., Williams, B., Li, Y., Figueiredo, P. de, and Wolpert, T. 2017. Reassessing apoptosis in plants. Nature Plants. 3:773.
Friesen, T. L., Holmes, D. J., Bowden, R. L., and Faris, J. D. 2018. ToxA Is Present in the U.S. Bipolaris sorokiniana Population and Is a Significant Virulence Factor on Wheat Harboring Tsn1. Plant Disease. :PDIS-03-18-0521-RE.
Gdanetz, K., and Trail, F. 2017. The Wheat Microbiome Under Four Management Strategies, and Potential for Endophytes in Disease Protection. Phytobiomes. 1:158–168.
Gluck-Thaler, E., and Slot, J. C. 2018. Specialized plant biochemistry drives gene clustering in fungi. The ISME Journal. 12:1694.
Gluck‐Thaler, E., Vijayakumar, V., and Slot, J. C. Fungal adaptation to plant defenses through convergent assembly of metabolic modules. Molecular Ecology. 0.
Grau, M. F., Entwistle, R., Chiang, Y.-M., Ahuja, M., Oakley, C. E., Akashi, T., et al. 2018. Hybrid Transcription Factor Engineering Activates the Silent Secondary Metabolite Gene Cluster for (+)-Asperlin in Aspergillus nidulans. ACS Chem. Biol. 13:3193–3205.
Guruceaga, X., Ezpeleta, G., Mayayo, E., Sueiro-Olivares, M., Abad-Diaz-De-Cerio, A., Urízar, J. M. A., et al. 2018a. A possible role for fumagillin in cellular damage during host infection by Aspergillus fumigatus. Virulence. 9:1548–1561.
Guruceaga, X., Ezpeleta, G., Mayayo, E., Sueiro-Olivares, M., Abad-Diaz-De-Cerio, A., Urízar, J. M. A., et al. 2018b. A possible role for fumagillin in cellular damage during host infection by Aspergillus fumigatus. Virulence. 9:1548–1561.
Jain, S., Wiemann, P., Thill, E., Williams, B., Keller, N. P., and Kabbage, M. 2018. A Bcl-2 Associated Athanogene (bagA) Modulates Sexual Development and Secondary Metabolism in the Filamentous Fungus Aspergillus nidulans. Front Microbiol. 9.
Jiang, C., Zhang, X., Liu, H., and Xu, J.-R. 2018. Mitogen-activated protein kinase signaling in plant pathogenic fungi. PLOS Pathogens. 14:e1006875.
Kershaw, M. J., Basiewicz, M., Soanes, D. M., Yan, X., Ryder, L. S., Csukai, M., et al. 2018. Conidial Morphogenesis and Septin-Mediated Plant Infection Require Smo1, a Ras GTPase-Activating Protein in Magnaporthe oryzae. Genetics. :genetics.301490.2018.
Kershaw, M. J., Basiewicz, M., Soanes, D., Yan, X., Ryder, L. S., Csukai, M., et al. 2018. Magnaporthe oryzae SMO1 encodes a Ras GTPase-activating protein required for spore morphology, appressorium function and rice blast disease. bioRxiv. :388298.
Kim, W., Miguel-Rojas, C., Wang, J., Townsend, J. P., and Trail, F. 2018a. Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in Fusarium graminearum. mBio. 9:e01292-18.
Kim, W., Miguel-Rojas, C., Wang, J., Townsend, J. P., and Trail, F. 2018b. Sexual stage-induced long noncoding RNAs in the filamentous fungus Fusarium graminearum. bioRxiv. :270298.
Kumar, D., Tannous, J., Sionov, E., Keller, N., and Prusky, D. 2018. Apple Intrinsic Factors Modulating the Global Regulator, LaeA, the Patulin Gene Cluster and Patulin Accumulation During Fruit Colonization by Penicillium expansum. Front Plant Sci. 9.
Liang, Y., Han, Y., Wang, C., Jiang, C., and Xu, J.-R. 2018. Targeted Deletion of the USTA and UvSLT2 Genes Efficiently in Ustilaginoidea virens With the CRISPR-Cas9 System. Front. Plant Sci. 9.
Lim, F. Y., Won, T. H., Raffa, N., Baccile, J. A., Wisecaver, J., Rokas, A., et al. 2018. Fungal Isocyanide Synthases and Xanthocillin Biosynthesis in Aspergillus fumigatus. mBio. 9:e00785-18.
Lin, H., Lyu, H., Zhou, S., Yu, J., P. Keller, N., Chen, L., et al. 2018. Deletion of a global regulator LaeB leads to the discovery of novel polyketides in Aspergillus nidulans. Organic & Biomolecular Chemistry. 16:4973–4976.
Lindo, L., McCormick, S. P., Cardoza, R. E., Brown, D. W., Kim, H.-S., Alexander, N. J., et al. 2018. Effect of deletion of a trichothecene toxin regulatory gene on the secondary metabolism transcriptome of the saprotrophic fungus Trichoderma arundinaceum. Fungal Genetics and Biology. 119:29–46.
Liu, R., Weisblum, B., Gellman, S., Lim, F. Y., Rank, L. A., Keller, N. P., et al. 2018. Antifungal nylon-3 polymers and combination therapy using them to treat fungal infections.
Lofgren, L. A., LeBlanc, N. R., Certano, A. K., Nachtigall, J., LaBine, K. M., Riddle, J., et al. 2018. Fusarium graminearum: pathogen or endophyte of North American grasses? New Phytologist. 217:1203–1212.
Lorang, J. M. 2018. Necrotrophic exploitation and subversion of plant defense: a lifestyle or just a phase, and implications in breeding resistance. Phytopathology.
Lorang, J. M., Hagerty, C. H., Lee, R., McClean, P. E., and Wolpert, T. J. 2018. Genetic Analysis of Victorin Sensitivity and Identification of a Causal Nucleotide-Binding Site Leucine-Rich Repeat Gene in Phaseolus vulgaris. MPMI. 31:1069–1074.
Marroquin-Guzman, M., Krotz, J., Appeah, H., and Wilson, R. A. 2018. Metabolic constraints on Magnaporthe biotrophy: loss of de novo asparagine biosynthesis aborts invasive hyphal growth in the first infected rice cell. Microbiology.
Mettenleiter, T. C., Kielian, M., and Roossinck, M. J. 2018. Preface to Volume 100: History and Looking Forward. In Advances in Virus Research, eds. Margaret Kielian, Thomas C. Mettenleiter, and Marilyn J. Roossinck. Academic Press, p. xv–xxiv.
Mochizuki, T., Ohara, R., and Roossinck, M. J. 2018. Large-Scale Synonymous Substitutions in Cucumber Mosaic Virus RNA 3 Facilitate Amino Acid Mutations in the Coat Protein. Journal of Virology. 92:e01007-18.
Molnár, Á. P., Németh, Z., Fekete, E., Flipphi, M., Keller, N. P., and Karaffa, L. 2018. Analysis of the Relationship between Alternative Respiration and Sterigmatocystin Formation in Aspergillus nidulans. Toxins. 10:168.
Moolhuijzen, P., See, P. T., Hane, J. K., Shi, G., Liu, Z., Oliver, R. P., et al. 2018. Comparative genomics of the wheat fungal pathogen Pyrenophora tritici-repentis reveals chromosomal variations and genome plasticity. BMC Genomics. 19:279.
Multi-environment assessment of fungicide performance for managing wheat head blast (WHB) in Brazil and Bolivia | SpringerLink.
Peng, Z., Oliveira-Garcia, E., Lin, G., Hu, Y., Dalby, M., Migeon, P., et al. 2018. Effector Gene Reshuffling Involves Dispensable Mini-chromosomes in the Wheat Blast Fungus. bioRxiv. :359455.
Peyambari, M., and Roossinck, M. J. 2018. Characterizing Mycoviruses. In Plant Pathogenic Fungi and Oomycetes: Methods and Protocols, Methods in Molecular Biology, eds. Wenbo Ma and Thomas Wolpert. New York, NY: Springer New York, p. 13–24.
Peyambari, M., Warner, S., Stoler, N., Rainer, D., and Roossinck, M. J. 2018. A 1000 year-old RNA virus. Journal of Virology. :JVI.01188-18.
Phosphorylation by Prp4 kinase releases the self-inhibition of FgPrp31 in Fusarium graminearum | SpringerLink.
Proctor, R. H., McCormick, S. P., Kim, H.-S., Cardoza, R. E., Stanley, A. M., Lindo, L., et al. 2018. Evolution of structural diversity of trichothecenes, a family of toxins produced by plant pathogenic and entomopathogenic fungi. PLOS Pathogens. 14:e1006946.
Prusky, D. B., and Wilson, R. A. 2018. Does increased nutritional carbon availability in fruit and foliar hosts contribute to modulation of pathogen colonization? Postharvest Biology and Technology. 145:27–32.
Rank, L. A., Walsh, N. M., Lim, F. Y., Gellman, S. H., Keller, N. P., and Hull, C. M. 2018. Peptide-Like Nylon-3 Polymers with Activity against Phylogenetically Diverse, Intrinsically Drug-Resistant Pathogenic Fungi. mSphere. 3:e00223-18.
Redman, R. S., and Rodriguez, R. J. 2017. The Symbiogenic Tango: Achieving Climate-Resilient Crops Via Mutualistic Plant-Fungal Relationships. In Functional Importance of the Plant Microbiome: Implications for Agriculture, Forestry and Bioenergy, ed. Sharon Lafferty Doty. Cham: Springer International Publishing, p. 71–87.
Reynolds, H. T., Slot, J. C., Divon, H. H., Lysøe, E., Proctor, R. H., and Brown, D. W. 2017. Differential Retention of Gene Functions in a Secondary Metabolite Cluster. Mol Biol Evol. 34:2002–2015.
Reynolds, H. T., Vijayakumar, V., Gluck‐Thaler, E., Korotkin, H. B., Matheny, P. B., and Slot, J. C. 2018. Horizontal gene cluster transfer increased hallucinogenic mushroom diversity. Evolution Letters. 2:88–101.
Rhoades, N. A., Harvey, A. M., Samarajeewa, D. A., Svedberg, J., Yusifov, A., Abusharekh, A., et al. 2018. Identification of a genetic element required for spore killing in Neurospora. bioRxiv. :404004.
Richards, J., Ameen, G., Brueggeman, R., Ameen, G., and Brueggeman, R. 2017. Inverse gene-for-gene: Necrotrophic specialist’s modus operandi in barley and wheat. Management of Wheat and Barley Diseases.
Richards, J. K., Wyatt, N. A., Liu, Z., Faris, J. D., and Friesen, T. L. 2018. Reference Quality Genome Assemblies of Three Parastagonospora nodorum Isolates Differing in Virulence on Wheat. G3: Genes, Genomes, Genetics. 8:393–399.
Robey, M. T., Ye, R., Bok, J. W., Clevenger, K. D., Islam, M. N., Chen, C., et al. 2018. Identification of the First Diketomorpholine Biosynthetic Pathway Using FAC-MS Technology. ACS Chem. Biol. 13:1142–1147.
Rocha, R. O., and Wilson, R. A. 2018. Essential, deadly, enigmatic: Polyamine metabolism and roles in fungal cells. Fungal Biology Reviews.
Rodriguez, R. J., and Redman, R. S. 2018. Compositions and methods related to isolated endophytes.
Roossinck, M. J. Evolutionary and ecological links between plant and fungal viruses. New Phytologist. 0.
Rosowski, E. E., Raffa, N., Knox, B. P., Golenberg, N., Keller, N. P., and Huttenlocher, A. 2018. Macrophages inhibit Aspergillus fumigatus germination and neutrophil-mediated fungal killing. PLOS Pathogens. 14:e1007229.
Safari, M., and Roossinck, M. J. 2018. Coevolution of a Persistent Plant Virus and Its Pepper Hosts. MPMI. 31:766–776.
Sakulkoo, W., Osés-Ruiz, M., Garcia, E. O., Soanes, D. M., Littlejohn, G. R., Hacker, C., et al. 2018. A single fungal MAP kinase controls plant cell-to-cell invasion by the rice blast fungus. Science. 359:1399–1403.
Sapkota, S., Zhang, Q., Chittem, K., Mergoum, M., Xu, S. S., and Liu, Z. 2018. Evaluation of triticale accessions for resistance to wheat bacterial leaf streak caused by Xanthomonas translucens pv. undulosa. Plant Pathology. 67:595–602.
Simmonds, P., Adams, M. J., Benkő, M., Breitbart, M., Brister, J. R., Carstens, E. B., et al. 2017. Consensus statement: Virus taxonomy in the age of metagenomics. Nature Reviews Microbiology. 15:161–168.
Sipos, G., Prasanna, A. N., Walter, M. C., O’Connor, E., Bálint, B., Krizsán, K., et al. 2017. Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria. Nature Ecology & Evolution. 1:1931.
Slot, J. C. 2018. Fungal Ecology. In eLS, American Cancer Society, p. 1–10.
Spraker, J. E., Wiemann, P., Baccile, J. A., Venkatesh, N., Schumacher, J., Schroeder, F. C., et al. 2018. Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi. mBio. 9:e00820-18.
Sun, M., Zhang, Y., Wang, Q., Wu, C., Jiang, C., and Xu, J.-R. 2018. The tri-snRNP specific protein FgSnu66 is functionally related to FgPrp4 kinase in Fusarium graminearum. Molecular Microbiology. 109:494–508.
Syme, R. A., Martin, A., Wyatt, N. A., Lawrence, J. A., Muria-Gonzalez, M. J., Friesen, T. L., et al. 2018. Transposable Element Genomic Fissuring in Pyrenophora teres Is Associated With Genome Expansion and Dynamics of Host–Pathogen Genetic Interactions. Front. Genet. 9.
Syme, R. A., Tan, K.-C., Rybak, K., Friesen, T. L., McDonald, B. A., Oliver, R. P., et al. 2018. Pan-Parastagonospora Comparative Genome Analysis—Effector Prediction and Genome Evolution. Genome Biol Evol. 10:2443–2457.
Tang, G., Chen, Y., Xu, J.-R., Kistler, H. C., and Ma, Z. 2018. The fungal myosin I is essential for Fusarium toxisome formation. PLOS Pathogens. 14:e1006827.
Tannous, J., Kumar, D., Sela, N., Sionov, E., Prusky, D., and Keller, N. P. 2018. Fungal attack and host defence pathways unveiled in near-avirulent interactions of Penicillium expansum creA mutants on apples. Molecular Plant Pathology. 19:2635–2650.
Trail, F., and Jones, A. D. 2018. Compounds for inhibition of fungal toxin production.
Vainio, E. J., Chiba, S., Ghabrial, S. A., Maiss, E., Roossinck, M., Sabanadzovic, S., et al. 2018. ICTV Virus Taxonomy Profile: Partitiviridae. Journal of General Virology. 99:17–18.
de Vries, R. P., Riley, R., Wiebenga, A., Aguilar-Osorio, G., Amillis, S., Uchima, C. A., et al. 2017. Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus. Genome Biology. 18:28.
Wang, G., Sun, P., Gong, Z., Gu, L., Lou, Y., Fang, W., et al. 2018. Srk1 kinase, a SR protein-specific kinase, is important for sexual reproduction, plant infection and pre-mRNA processing in Fusarium graminearum. Environmental Microbiology. 20:3261–3277.
Wang, Q., Chen, D., Wu, M., Zhu, J., Jiang, C., Xu, J.-R., et al. 2018. MFS Transporters and GABA Metabolism Are Involved in the Self-Defense Against DON in Fusarium graminearum. Front Plant Sci. 9.
Wang, Q., Liu, H., Xu, H., Hei, R., Zhang, S., Jiang, C., et al. Independent losses and duplications of autophagy-related genes in fungal tree of life. Environmental Microbiology. 0.
Wang, Z., Gudibanda, A., Ugwuowo, U., Trail, F., and Townsend, J. P. 2018. Using evolutionary genomics, transcriptomics, and systems biology to reveal gene networks underlying fungal development. Fungal Biology Reviews. 32:249–264.
Wen, A., Jayawardana, M., Fiedler, J., Sapkota, S., Shi, G., Peng, Z., et al. 2018. Genetic mapping of a major gene in triticale conferring resistance to bacterial leaf streak. Theor Appl Genet. 131:649–658.
Wyatt, N. A., Richards, J. K., Brueggeman, R. S., and Friesen, T. L. 2018. Reference Assembly and Annotation of the Pyrenophora teres f. teres Isolate 0-1. G3: Genes, Genomes, Genetics. 8:1–8.
Xavier, K. V., Mizubuti, E. S. G., Queiroz, M. V., Chopra, S., and Vaillancourt, L. 2018. Genotypic and Pathogenic Diversity of Colletotrichum sublineola Isolates from Sorghum (Sorghum bicolor) and Johnsongrass (S. halepense) in the Southeastern United States. Plant Disease. 102:2341–2351.
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Yasuhara-Bell, J., Pedley, K. F., Farman, M., Valent, B., and Stack, J. P. 2018. Specific Detection of the Wheat Blast Pathogen (Magnaporthe oryzae Triticum) by Loop-Mediated Isothermal Amplification. Plant Disease. 102:2550–2559.
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