Brief Summary of Minutes of Annual Meeting

Minutes of the NCCC307 (North Central Coordinating Committee) “Biochemistry and Genetics of Plant-Fungal Interactions” meeting held at Asilomar Conference Center March 18, 2015 7:15 pm– 7:25 pm – Welcome and synopsis of NCCC-307 by Chair, Jeff Rollins 7:25 pm– 7:30 pm – Status and future workshop plans by Secretary, Regina Redman 2016 to be held in Florida by host Jeff Rollins 7:30pm– 7:50 pm – Cameron C. Hunter (Kansas State University) Title: “Multiple nuclear localization signals mediate nuclear localization of the GATA transcription factor AreA in Aspergillus nidulans” Cameron C. Hunter, Kendra S. Siebert, and Richard B. Todd. Department Genetics, Kansas State University Transcription factors are synthesized in the cytoplasm but act in the nucleus to regulate gene expression. The GATA transcription factor AreA from the fungus Aspergillus nidulans activates transcription of nitrogen metabolic genes. AreA accumulates in the nucleus during nitrogen starvation but not in the presence of nitrogen nutrients. We aim to understand how AreA is directed to the nucleus. Sequence analysis revealed five classical nuclear localization signals (NLSs) and one noncononical bipartite NLS. We have fused these NLSs separately and in combination to green fluorescent protein (GFP) and expressed them in A. nidulans to determine if they are sufficient for nuclear localization. The bipartite NLS strongly directed GFP to the nucleus, whereas the classical NLSs directed GFP to the nucleus via collaboration. Therefore, AreA contains multiple NLSs which work together to mediate nuclear import. 7:50pm– 8:10 pm – Jennifer Lorang (Oregon State University) Title: Plant Innate Immunity Genes that Condition Disease Susceptibility Jennifer Lorang and Tom Wolpert Dept. of Plant Pathology, Oregon State University Our primary interest is to understand genetic and molecular components of plant that allow them to be susceptible to disease. Most of this work has been done with the necrotrophic pathogen Cocliobolus victoriae. Our previous work has shown that sensitivity to the fungal toxin victorin conditions susceptibility to the pathogen in oats and the model organism Arabidopsis. We had found this response requires the Arabidopsis genes LOV and ATTRXh5. The LOV protein is an NB-LRR innate immune receptor, and together, victorin LOV and ATTRXh5 conformto the guard model of plant disease resistance, but for this necrotrophic pathogen the outcome is cell death and disease. Here we present our new findings that victorin sensitivity and thus C. victoriae susceptibility is conditioned by a plethora of NB-LRR immune receptors in diverse species, including Brachypodium, barley, rice and beans. Our data implied converged evolution for these immune receptors to guard plant thioredoxins and an addition cellular target for the toxin victorin that we hope to characterize. 8:30pm– 10:00 pm – Open panel discussions and questions and closing remarks Discussion was held concerning perception and signal transduction during plant infection. Considerable and vigorous debate concerning the molecular nature of susceptibility in the context of host and non-host interactions and necrotrophic versus biotrophic interactions was engaged by nearly all participants. Next year’s meeting was planned for Gainesville, Fl under the organizing theme of communicating and understanding the concepts of necrotrophic, hemi-biotrophic, and biotrophic host-pathogen interactions.

Members of the NCCC307 committee reported near-term accomplishments on several fronts during the past year. These include (1) Progress on understanding the regulation and requirements of primary and secondary metabolism on host-pathogen interaction, growth, development and survival. (2) Elucidation of signal transduction pathways to understand the process and regulation of infection and host colonization (3) Identification, characterization and application of biotrophic and necrotrophic effectors in understanding fungal pathogenesis and host resistance and susceptibility. (4) Crop germplasm evaluation, disease resistance mapping, and cultivar release. (5) Identification of newly emerging and endemic pathogens, characterization of pathogen population diversity, fungal community interactions, and symbiotic interactions among fungi, plants and viruses. These efforts have produced three patents and more than 105 peer-reviewed journal publications in the 2014-2015 period.

105 Publications (2014-2015) 2014 Affeldt, K.J., J. Carrig, M. Amare, and N.P. Keller. 2014. Global Survey of Canonical Aspergillus flavus G Protein-Coupled Receptors. mBio. 5:e01501–14. doi:10.1128/mBio.01501-14. Amare, M.G., and N.P. Keller. 2014. Molecular mechanisms of Aspergillus flavus secondary metabolism and development. Fungal Genetics and Biology. 66:11–18. doi:10.1016/j.fgb.2014.02.008. Bakkeren, G., and B. Valent. 2014. Do pathogen effectors play peek-a-boo? Front. Plant Sci. 5:731. doi:10.3389/fpls.2014.00731. Barcelos, Q.L., J.M.A. Pinto, L.J. Vaillancourt, and E.A. Souza. 2014. Characterization of Glomerella Strains Recovered from Anthracnose Lesions on Common Bean Plants in Brazil. PLoS ONE. 9:e90910. doi:10.1371/journal.pone.0090910. Bec, S., T.J. Ward, M. Farman, K. O’Donnell, D.E. Hershman, D.A. Van Sanford, and L. Vaillancourt. 2014. Characterization of Fusarium strains recovered from wheat with symptoms of head blight in Kentucky. Plant Disease. doi:10.1094/PDIS-06-14-0610-RE. Bok, J.W., P. Wiemann, G.S. Garvey, F.Y. Lim, B. Haas, J. Wortman, and N.P. Keller. 2014. Illumina identification of RsrA, a conserved C2H2 transcription factor coordinating the NapA mediated oxidative stress signaling pathway in Aspergillus. BMC Genomics. 15:1011. doi:10.1186/1471-2164-15-1011. Chen, D., Y. Wang, X. Zhou, Y. Wang, and J.-R. Xu. 2014a. The Sch9 Kinase Regulates Conidium Size, Stress Responses, and Pathogenesis in Fusarium graminearum. PLoS ONE. 9:e105811. doi:10.1371/journal.pone.0105811. Chen, X.-L., T. Shi, J. Yang, W. Shi, X. Gao, D. Chen, X. Xu, J.-R. Xu, N.J. Talbot, and Y.-L. Peng. 2014b. N-Glycosylation of Effector Proteins by an ?-1,3-Mannosyltransferase Is Required for the Rice Blast Fungus to Evade Host Innate Immunity. Plant Cell. tpc.114.123588. doi:10.1105/tpc.114.123588. Connell, L.B., R.R. Rodriguez, R.S. Redman, and J.J. Dalluge. 2014. Cold-Adapted Yeasts in Antarctic Deserts. In Cold-adapted Yeasts. P. Buzzini and R. Margesin, editors. Springer Berlin Heidelberg. 75–98. Crouch, J., R. O’Connell, P. Gan, E. Buiate, M.F. Torres, L. Beirn, K. Shirasu, and L. Vaillancourt. 2014. The Genomics of Colletotrichum. In Genomics of Plant-Associated Fungi: Monocot Pathogens. R.A. Dean, A. Lichens-Park, and C. Kole, editors. Springer Berlin Heidelberg. 69–102. Donofrio, N.M., J. Hu, T.K. Mitchell, and R.A. Wilson. 2014. Facilitating the Fungus: Insights from the Genome of the Rice Blast Fungus, Magnaporthe oryzae. In Genomics of Plant-Associated Fungi: Monocot Pathogens. Springer Berlin Heidelberg. 141–160. Donofrio, N.M., and R.A. Wilson. 2014. Redox and rice blast: new tools for dissecting molecular fungal–plant interactions. New Phytologist. 201:367–369. Giraldo, M.C., and B. Valent. 2013. Filamentous plant pathogen effectors in action. Nat Rev Micro. 11:800–814. doi:10.1038/nrmicro3119. Downes, D.J., M. Chonofsky, K. Tan, B.T. Pfannenstiel, S.L. Reck-Peterson, and R.B. Todd. 2014a. Characterization of the Mutagenic Spectrum of 4-Nitroquinoline 1-Oxide (4-NQO) in Aspergillus nidulans by Whole Genome Sequencing. G3. 4:2483–2492. doi:10.1534/g3.114.014712. Downes, D.J., M.A. Davis, K.H. Wong, S.D. Kreutzberger, M.J. Hynes, and R.B. Todd. 2014b. Dual DNA binding and coactivator functions of Aspergillus nidulans TamA, a Zn(II)2Cys6 transcription factor. Mol. Microbiol. 92:1198–1211. doi:10.1111/mmi.12620. Du, Z., A. Chen, W. Chen, Q. Liao, H. Zhang, Y. Bao, M.J. Roossinck, and J.P. Carr. 2014. Nuclear-cytoplasmic partitioning of cucumber mosaic virus protein 2b determines the balance between its roles as a virulence determinant and an RNA-silencing suppressor. J. Virol. 88:5228–5241. doi:10.1128/JVI.00284-14. Fernandez, J., M. Marroquin-Guzman, R. Nandakumar, S. Shijo, K.M. Cornwell, G. Li, and R.A. Wilson. 2014a. Plant defence suppression is mediated by a fungal sirtuin during rice infection by Magnaporthe oryzae. Molecular microbiology. 94:70–88. Fernandez, J., M. Marroquin-Guzman, and R.A. Wilson. 2014b. Evidence for a transketolase-mediated metabolic checkpoint governing biotrophic growth in rice cells by the blast fungus Magnaporthe oryzae. Fernandez, J., M. Marroquin-Guzman, and R.A. Wilson. 2014c. Mechanisms of Nutrient Acquisition and Utilization During Fungal Infections of Leaves. Annual review of phytopathology. Fernandez, J., and R.A. Wilson. 2014a. Cells in cells: morphogenetic and metabolic strategies conditioning rice infection by the blast fungus Magnaporthe oryzae. Protoplasma. 251:37–47. Fernandez, J., and R.A. Wilson. 2014b. Characterizing roles for the glutathione reductase, thioredoxin reductase and thioredoxin peroxidase-encoding genes of Magnaporthe oryzae during rice blast disease. PloS one. 9. Greene, G.H., K.L. McGary, A. Rokas, and J.C. Slot. 2014. Ecology drives the distribution of specialized tyrosine metabolism modules in fungi. Genome biology and evolution. 6:121–132. Hammerschmidt, R. 2014. Neutralizing nematodes. Physiological and molecular plant pathology. 86. Hunter, C.C., K.S. Siebert, D.J. Downes, K.H. Wong, S.D. Kreutzberger, J.A. Fraser, D.F. Clarke, M.J. Hynes, M.A. Davis, and R.B. Todd. 2014. Multiple nuclear localization signals mediate nuclear localization of the GATA transcription factor AreA. Eukaryotic Cell. 13:527–538. doi:10.1128/EC.00040-14. Hu, S., X. Zhou, X. Gu, S. Cao, C. Wang, and J.-R. Xu. 2014. The cAMP-PKA pathway regulates growth, sexual and asexual differentiation, and pathogenesis in Fusarium graminearum. Mol. Plant Microbe Interact. 27:557–566. doi:10.1094/MPMI-10-13-0306-R. Jonkers, W., H. Xayamongkhon, M. Haas, C. Olivain, H.C. Does, K. Broz, M. Rep, C. Alabouvette, C. Steinberg, and H.C. Kistler. 2014. EBR1 genomic expansion and its role in virulence of Fusarium species. Environmental microbiology. 16:1982–2003. Knox, B.P., Q. Deng, M. Rood, J.C. Eickhoff, N.P. Keller, and A. Huttenlocher. 2014. Distinct innate immune phagocyte responses to Aspergillus fumigatus conidia and hyphae in zebrafish larvae. Eukaryotic Cell. 13:1266–1277. doi:10.1128/EC.00080-14. LeBlanc, N., L.L. Kinkel, and H.C. Kistler. 2014. Soil fungal communities respond to grassland plant community richness and soil edaphics. Microbial ecology. 1–8. Liang, J.M., H. Xayamongkhon, K. Broz, Y. Dong, S.P. McCormick, S. Abramova, T.J. Ward, Z.H. Ma, and H.C. Kistler. 2014. Temporal dynamics and population genetic structure of Fusarium graminearum in the upper Midwestern United States. Fungal Genetics and Biology. 73:83–92. Lim, F.Y., B. Ames, C.T. Walsh, and N.P. Keller. 2014. Co-ordination between BrlA regulation and secretion of the oxidoreductase FmqD directs selective accumulation of fumiquinazoline C to conidial tissues in Aspergillus fumigatus. Cell. Microbiol. 16:1267–1283. doi:10.1111/cmi.12284. Lim, F.Y., and N.P. Keller. 2014. Spatial and temporal control of fungal natural product synthesis. Nat Prod Rep. 31:1277–1286. doi:10.1039/c4np00083h. Luo, Y., H. Zhang, L. Qi, S. Zhang, X. Zhou, Y. Zhang, and J.-R. Xu. 2014. FgKin1 kinase localizes to the septal pore and plays a role in hyphal growth, ascospore germination, pathogenesis, and localization of Tub1 beta-tubulins in Fusarium graminearum. New Phytol. 204:943–954. doi:10.1111/nph.12953. Lu, S., J.D. Faris, R. Sherwood, T.L. Friesen, and M.C. Edwards. 2014. A dimeric PR-1-type pathogenesis-related protein interacts with ToxA and potentially mediates ToxA-induced necrosis in sensitive wheat. Molecular plant pathology. 15:650–663. Lysøe, E., L.J. Harris, S. Walkowiak, R. Subramaniam, H.H. Divon, E.S. Riiser, C. Llorens, T. Gabaldón, H.C. Kistler, W. Jonkers, and others. 2014. The Genome of the Generalist Plant Pathogen Fusarium avenaceum Is Enriched with Genes Involved in Redox, Signaling and Secondary Metabolism. Ma, L.-J., T. Shea, S. Young, Q. Zeng, and H.C. Kistler. 2014. Genome sequence of Fusarium oxysporum f. sp. melonis strain NRRL 26406, a fungus causing wilt disease on melon. Genome announcements. 2:e00730–14. Mattupalli, C., J.E. Spraker, E. Berthier, N.P. Keller, A.O. Charkowski, and R.W. Shepherd. 2014. A Microfluidic Assay for Identifying Differential Responses of Plant and Human Fungal Pathogens to Tobacco Phylloplanins. Plant Health Progress. doi:10.1094/PHP-RS-14-0009. Mergoum, M., S. Simsek, S. Zhong, M. Acevedo, T.L. Friesen, P.K. Singh, T.B. Adhikari, M.S. Alamri, and R.C. Frohberg. 2014. “Velva”Spring Wheat: An Adapted Cultivar to North-Central Plains of the United States with High Agronomic and Quality Performance. Journal of Plant Registrations. 8:32–37. Miyamoto, K., T. Murakami, P. Kakumyan, N.P. Keller, and K. Matsui. 2014. Formation of 1-octen-3-ol from Aspergillus flavus conidia is accelerated after disruption of cells independently of Ppo oxygenases, and is not a main cause of inhibition of germination. PeerJ. 2:e395. doi:10.7717/peerj.395. Niu, Z., D.L. Klindworth, G. Yu, T.L. Friesen, S. Chao, Y. Jin, X. Cai, J.-B. Ohm, J.B. Rasmussen, and S.S. Xu. 2014. Development and characterization of wheat lines carrying stem rust resistance gene Sr43 derived from Thinopyrum ponticum. Theoretical and applied genetics. 127:969–980. Oliver, R., J. Lichtenzveig, K.-C. Tan, O. Waters, K. Rybak, J. Lawrence, T. Friesen, and P. Burgess. 2014. Absence of detectable yield penalty associated with insensitivity to Pleosporales necrotrophic effectors in wheat grown in the West Australian wheat belt. Plant Pathology. 63:1027–1032. Ostrander, J.C., R.B. Todd, and M.M. Kennelly. 2014. Resistance of Kansas Sclerotinia homoeocarpa Isolates to Thiophanate-Methyl and Determination of Associated ?-Tubulin Mutation. Plant Health Progress. doi:10.1094/PHP-RS-13-0120. Peyambari, M., M.K. Habibi, K.-B. Fotouhifar, A. Dizadji, and and M.J. Roossinck. 2014. 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Predicting genome-scale Arabidopsis-Pseudomonas syringae interactome using domain and interolog-based approaches. BMC bioinformatics. 15:S13. Shjerve, R.A., J.D. Faris, R.S. Brueggeman, C. Yan, Y. Zhu, V. Koladia, and T.L. Friesen. 2014. Evaluation of a Pyrenophora teres f. teres mapping population reveals multiple independent interactions with a region of barley chromosome 6H. Fungal Genetics and Biology. 70:104–112. Sikora, E.J., T.W. Allen, K.A. Wise, G. Bergstrom, C.A. Bradley, J. Bond, D. Brown-Rytlewski, M. Chilvers, J. Damicone, E. DeWolf, A. Dorrance, N. Dufault, P. Esker, T.R. Faske, L. Giesler, N. Goldberg, J. Golod, I.R.G. Gómez, C. Grau, A. Grybauskas, G. Franc, R. Hammerschmidt, G.L. Hartman, R.A. Henn, D. Hershman, C. Hollier, T. Isakeit, S. Isard, B. Jacobsen, D. Jardine, R. Kemerait, S. Koenning, M. Langham, D. Malvick, S. Markell, J.J. Marois, S. Monfort, D. Mueller, J. Mueller, R. Mulrooney, M. Newman, L. Osborne, G.B. Padgett, B.E. Ruden, J. Rupe, R. Schneider, H. Schwartz, G. Shaner, S. Singh, E. Stromberg, L. Sweets, A. Tenuta, S. Vaiciunas, X.B. Yang, H. Young-Kelly, and J. Zidek. 2014. A Coordinated Effort to Manage Soybean Rust in North America: A Success Story in Soybean Disease Monitoring. Plant Disease. 98:864–875. doi:10.1094/PDIS-02-14-0121-FE. Spraker, J.E., K. Jewell, L.V. Roze, J. Scherf, D. Ndagano, R. Beaudry, J.E. Linz, C. Allen, and N.P. Keller. 2014. A volatile relationship: profiling an inter-kingdom dialogue between two plant pathogens, Ralstonia Solanacearum and Aspergillus Flavus. J. Chem. Ecol. 40:502–513. doi:10.1007/s10886-014-0432-2. Stack, J.P., R.M. Bostock, R. Hammerschmidt, J.B. Jones, and E. Luke. 2014. The National Plant Diagnostic Network: Partnering to Protect Plant Systems. Plant Disease. 98:708–715. doi:10.1094/PDIS-08-13-0876-FE. Stobbe, A.H., and M.J. Roossinck. 2014. Plant virus metagenomics: what we know and why we need to know more. Front Plant Sci. 5. doi:10.3389/fpls.2014.00150. Todd, R.B., M. 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Spatial Regulation of a Common Precursor from Two Distinct Genes Generates Metabolite Diversity. Chem. Sci. doi:10.1039/C5SC01058F. Guo, L., A. Breakspear, G. Zhao, L. Gao, H.C. Kistler, J.-R. Xu, and L.-J. Ma. 2015b. Conservation and divergence of the cyclic adenosine monophosphate-protein kinase A (cAMP-PKA) pathway in two plant-pathogenic fungi: Fusarium graminearum and F.?verticillioides. Mol. Plant Pathol. doi:10.1111/mpp.12272. Hammerschmidt, R. 2015. Plants inducing plants. Physiological and Molecular Plant Pathology. 90:iii. Hou, R., C. Jiang, Q. Zheng, C. Wang, and J.-R. Xu. 2015. The AreA transcription factor mediates the regulation of deoxynivalenol (DON) synthesis by ammonium and cyclic adenosine monophosphate (cAMP) signalling in Fusarium graminearum. Mol. Plant Pathol. doi:10.1111/mpp.12254. Jiang, C., S. Zhang, Q. Zhang, Y. Tao, C. Wang, and J.-R. Xu. 2015. 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