NCCC307: Biochemistry and Genetics of Plant-Fungal Interactions

(Multistate Research Coordinating Committee and Information Exchange Group)

Status: Active

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SAES-422 Reports

Annual/Termination Reports:

[11/07/2023]

Date of Annual Report: 11/07/2023

Report Information

Annual Meeting Dates: 10/06/2023 - 10/06/2023
Period the Report Covers: 10/01/2022 - 10/01/2023

Participants

Vaillancourt, Lisa (vaillan@uky.edu) – University of Kentucky; Coleman, Jeff (jjcoleman@auburn.edu) – Auburn University; Belisario, Renata (renata.belisario@uky.edu) – University of Kentucky; Brown, Daren (daren.brown@ars.usda.gov) - USDA-ARS Peoria, Illinois; Caplan, Jeffrey (jcaplan@udel.edu) – University of Delaware; Cook, David (decook@k-state.edu) – Kansas State University; Drott, Milton (Milton.drott@usda.gov) – USDA-ARS, Cereal Disease Lab, St. Paul, Minnesota; Dulal, Nawaraj (ndulal2@huskers.unl.edu) – University of Nebraska-Lincoln; Farman, Mark (mark.farman@uky.edu) – University of Kentucky; Forster, Heather (Todd laboratory) – Kansas State University; Friesen, Tim (Timothy.Friesen@ars.uada.gov) - USDA-ARS Fargo, North Dakota; Goyal, Simran (simran.goyal@uky.edu) – University of Kentucky; Hamilton, Christina (christina.hamilton@wisc.edu) - University of Wisconsin-Madison; Harris, Steve (stevenh1@iastate.edu) – Iowa State University; Kariyawasam, Gayan (gayan.kariyawasam@ndsu.edu) – North Dakota State University; Konkol, Josh () – University of Florida; Kim, Saet-Byul (saetbyul.kim@unl.edu) – University of Nebraska-Lincoln; Lee, Jung-Youn (jylee@udel.edu) – University of Delaware; Lorang, Jennifer (lorangj@science.oregonstate.edu) - Oregon State University; Mathias, Caleb (mathiascaleb@uky.edu) – University of Kentucky; Nuckles, Etta (nuckles@uky.edu) – University of Kentucky; Richter, Michael (mrichter4@huskers.unl.edu) – University of Nebraska-Lincoln; Rollins, Jeff (rollinsj@ufl.edu) - University of Florida; Suelter, Tyler (Valent laboratory) – Kansas State University; Taylor, Jamari (taylorjamari6@gmail.com) – University of Kentucky; Todd, Richard (rbtodd@ksu.edu) - Kansas State University; Trail, Frances (trail@msu.edu) - Michigan State University; Valent, Barbara (bvalent@ksu.edu) - Kansas State University; Wilson, Richard (rwilson10@unl.edu) – University of Nebraska-Lincoln; Wang, Chenggang (chenggangwang@ufl.edu) – University of Florida; Wang, Zeyi (Xu laboratory) – Purdue University; Womack, Erika (edw7@msstate.edu) – Mississippi State University; Xu, Jin-Rong (jinrong@purdue.edu) - Purdue University

Brief Summary of Minutes

NCCC-307 Meeting Minutes - October 6, 2023

11:00 am – 11:30 am – Opening comments and presentation by NCCC307 Administrator Steve Harris followed by Christina Hamilton, NCRA Assistant Director and NIMSS System Administrator

11:30 am – 1:30 pm – Research presentations by graduate students and postdocs (~20 minutes each followed by 20 minutes of discussion about presented research

Michael Richter, Wilson Lab, University of Nebraska-Lincoln “Revealing the role of a Magnaporthe oryzae acyl-CoA-binding protein in thermal adaptation during rice infection.”

Zeyi Wang, Xu lab, Purdue University “RNA editing and RIP in Fusarium graminearum.”

Gayan Kariyawasam, Friesen Lab, North Dakota State University “The Parastagonospora nodorum effector SnTox5 modulates the host immune system to induce programmed cell death.”

Nawaraj Dulal, Wilson Lab, University of Nebraska-Lincoln " Translation and unconventional secretion ofMagnaporthe oryzae cytoplasmic effectors depends on tRNA modification and codon usage bias."

Renata Belisario, Vaillancourt Lab, University of Kentucky “Secretion of cell wall degrading enzymes by a signal peptidase mutant of Colletotrichum graminicola.”

1:30 pm – 3:00 pm – Break for lunch

3:00 pm – 4:10 pm – Discussion sessions (~30 minutes each)

Richard Wilson, University of Nebraska-Lincoln – Various topics on fungal; effectors, secretion, leaderless/large effectors, prediction, etc

Jennifer Lorang, Oregon State University – Teaching fungal biology; use of AI, ideas for online teaching, and collaborative teaching

4:10 pm – 4:21 pm – Discussion of next NCCC307 Meeting to be held at the 32^nd Fungal Genetics Conference, Asilomar Conference Center, Pacific Grove, CA in March 2024.

2023-2024 Elected co-chairs will be Jeffrey Coleman (Auburn University) and Jonathan Richards (Louisiana State University)

Accomplishments

NCCC307 committee members collectively increased our understanding of the biochemistry and genetics of plant-fungal interactions this past year by: 1) increasing our understanding of fungal effectors, their secretion, and modulation of the host plant immune response, 2) better understanding the function of secondary metabolites, their synthesis, and their evolutionary history, 3) understanding of the interaction and influence of bacterial and fungal populations during infection, and 4) increased understanding of plant resistance against fungal pathogens.  These efforts have produced more than 31 peer-reviewed journal publications from November 2022 through the October 2023 reporting period. Furthermore, members have engaged in teaching and outreach activities to transfer this knowledge to students, colleagues, and members of the general public.

Publications

Publications 2022-2023 (Names of NCCC 307 members are underlined)   <ol> <li>Aboukhadour R, Mohamed H, McDonald M, Moffat CS, Navathe S, Friesen TL, Strelkov SE, Oliver RP, Tan KC, Liu Z, Moolhuijzen PM, Phan H, See PT (2023) A revised nomenclature for ToxA haplotypes across multiple fungal species. Phytopathology 113: 1180-1184.</li> </ol>   <ol start="2"> <li>Alhashel AF, Fiedler JD, Nandety RS, Skiba RM, Bruggeman RS, Baldwin T, Friesen TL, Yang S (2023) Genetic and physical localization of a major susceptibility gene to Pyrenophora teres maculata in barley. Theoretical and Applied Genetics 136:118.</li> </ol>   <ol start="3"> <li>Belisário R, Robertson AE, Vaillancourt LJ (2022) Maize anthracnose stalk rot in the genomic era.  Plant Disease106: 2281-2298.</li> </ol>   <ol start="4"> <li>Belisário R, Torres MF, Buiate EA, Xavier KV, Nuckles EM, Vaillancourt LJ (2023) Detached maize sheaths for live-cell imaging of infection by fungal foliar maize pathogens. JoVE (Journal of Visualized Experiments), 199: e65755.</li> </ol>   <ol start="5"> <li>Brabham HJ, De La Cruz DG, Were V, Shimizu M, Saitoh M, Hernández-Pinzón I, Green P, Lorang J, Fujisaki K, Sato K, Molnar I, Simkova H, Dolezel J, Russell J, Taylor J, Smoker M, Gupta YK, Wolpert T, Talbot NJ, Terauchi R, Moscou M (2023) Barley MLA3 recognizes the host-specificity effector Pwl2 from Marnaporthe oryzae. Plant Cell</li> </ol>   <ol start="6"> <li>Brown DW, Kim HS, McGovern A, Probyn C, Proctor RH (2022) Genus-wide analysis of Fusarium polyketide synthases reveals broad chemical potential. Fungal Genetics and Biology 160: 103696.</li> </ol>   <ol start="7"> <li>Cardoza RE, McCormick SP, Izquierdo-Bueno I, Martinez-Reyes N, Lindo L, Brown DW, Collado IG, Proctor RH, Gutierrez S (2022) Identification of polyketide synthase genes required for aspinolide biosynthesis in Trichoderma arundinaceum. Applied Microbiology and Biotechnology 106: 7153-7171.</li> </ol>   <ol start="8"> <li>Del Ponte EM, Moreira GM, Ward TJ, O’Donnell K, Nicolli CP, Machado FJ, Duffeck MR, Alves KS, Tessmann DJ, Waalwijk C, van der Lee T, Zhang H, Chulze SN, Stenglein SA, Pan D, Vero S, Vaillancourt LJ, Schmale III DG, Esker PD, Moretti A, Logrieco AF, Kistler HC, Bergstrom GC, Viljoen A, Rose LJ, van Coller GJ, Lee T (2022)   Fusarium graminearum species complex: a bibliographic analysis and web-accessible database for global mapping of species and trichothecene toxin chemotypes.  Phytopathology 112: 741-751.</li> </ol>   <ol start="9"> <li>Drott MT, Park SC, Wang YW, Harrow L, Keller NP, Pringle A (2023) <a href="https://pubmed.ncbi.nlm.nih.gov/37221394/">Pangenomics of the death cap mushroom Amanita phalloides, and of Agaricales, reveals dynamic evolution of toxin genes in an invasive range. </a>ISME J 17: 1236-1246.</li> </ol>   <ol start="10"> <li>Green AJ, Mergoum M, Frohberg R, Underdahl J, Walz A, Selland T, Miranda A, Simsek S, Otteson B, Heilman-Morales AM, Murillo D, Friskop A, Rickertsen J, Ostlie M, Schatz B, Hanson B, Eriksmoen E, Martin G, Fiedler J, Rasmussen J, Zhong S, Liu Z, Friesen TL, Rouse M, Dill-Mackay R, Curland R, Gill U, Jin Y (2023) Registration of ND Frohberg Hard Red Spring Wheat. Journal of Plant Registrations 17: 385–396.</li> </ol>   <ol start="11"> <li>Kariyawasam GK, Nelson AC, Williams SJ, Solomon PS, Faris JD, Friesen TL (2023) The necrotrophic pathogen Parastagonospora nodorum is a master manipulator of wheat defense. Molecular Plant-Microbe Interactions https://doi.org/10.1094/MPMI-05-23-0067-IRW.</li> </ol>   <ol start="12"> <li>Li G, Dulal N, Gong Z, Wilson RA (2023) Unconventional secretion of Magnaporthe oryzae effectors in rice cells is regulated by tRNA modification and codon usage control. Nature Microbiology 8: 1706-1716.</li> </ol>   <ol start="13"> <li>Li G, Gong Z, Dulal N, Marroquin-Guzman M, Rocha RO, Richter M, Wilson RA (2023) A protein kinase coordinates cycles of autophagy and glutaminolysis in invasive hyphae of the fungus Magnaporthe oryzae within rice cells. Nature Communications 14: 4146.</li> </ol>   <ol start="14"> <li>Lohmar JM, Rhoades NA, Hammond TM, Brown DW (2022) Gene drive by Fusarium SKC1 is dependent on its competing allele. Fungal Genetics and Biology 163: 103749.</li> </ol>   <ol start="15"> <li>Lohmar JM, Rhoades NA, Patel TN, Proctor RH, Hammond TM, Brown DW (2022) A-to-I mRNA editing controls spore death induced by a fungal meiotic drive gene in homologous and heterologous expression systems. Genetics. 221.</li> </ol>     <ol start="16"> <li>Machado FJ, de Barros AV, McMaster N, Schmale III DG, Vaillancourt LJ, Del Ponte EM (2022) Aggressiveness and mycotoxin production by Fusarium meridionalecompared with  graminearum on maize ears and stalks in the field.  Phytopathology 112: 271-277.</li> </ol>   <ol start="17"> <li>Machado FJ, de Barros AV, McMaster N, Schmale DG, Del Ponte EM,Vaillancourt LJ (2023) A multivariate analysis of phenotypic traits of strains of Fusarium graminearum and  meridionale supports structure by species. Plant Pathology, 72: 1111–1121.</li> </ol>   <ol start="18"> <li>Mei J, Li Z, Zhou S, Chen XL, Wilson RA, Liu W (2023) Effector secretion and stability in the maize anthracnose pathogen Colletotrichum graminicola requires N-linked protein glycosylation and the ER chaperone pathway. New Phytologist 240: 1449-1466.</li> </ol>   <ol start="19"> <li>Nelson AC, Kariyawasam G, Wyatt NA, Li J, Haueisen J, Stukenbrock EH, Borowicz P, Liu Z, Friesen TL (2023) Unleashing the secrets of plant-fungal interactions using a transformation-free confocal staining technique that supports AI-assisted quantitative analysis. BioRxiv doi: https://doi.org/10.1101/2023.10.04.560942</li> </ol>   <ol start="20"> <li>Nickles GR, Oestereicher B, Keller NP, Drott MT (2023) <a href="https://pubmed.ncbi.nlm.nih.gov/37427794/">Mining for a new class of fungal natural products: the evolution, diversity, and distribution of isocyanide synthase biosynthetic gene clusters. </a>Nucleic Acids Research 51: 7220-7235.</li> </ol>   <ol start="21"> <li>Pereira D, Potgieter L, Bolton MD, Friesen TL, Stephan W, Dutheil JY Stukenbrock EH Large-scale analyses reveal the contribution of adaptive evolution in pathogenic and non-pathogenic fungal species. BioRxiv doi: https://doi.org/10.1101/2023.08.28.555124</li> </ol>   <ol start="22"> <li>Peters-Haugrud A, Shi G, Seneviratne S, Running KLD, Zhang Z, Singh G, Szabo-Hever A, Acharya K, Friesen TL, Liu Z, Faris JD (2023) Genome-wide association mapping of resistance to the foliar diseases septoria nodorum blotch and tan spot in a global winter wheat collection. Molecular Breeding 43:54.</li> </ol>   <ol start="23"> <li>Poddar S, Tanaka J, Running KLD, Kariyawasam GK, Faris JD, Friesen TL, Cho M-J, Cate JHD, Staskawicz B (2023) Optimization of highly efficient exogenous-DNA-free Cas9-ribonucleoprotein mediated gene editing in disease susceptibility loci in wheat (Triticum aestivum ). Frontiers in Plant Science 13:1084700.</li> </ol>   <ol start="24"> <li>Pokhrel A, Coleman JJ (2023) Inventory of the secondary metabolite biosynthetic potential of members within the terminal clade of the Fusarium solani species complex.  Journal of Fungi 9: 799.</li> </ol>   <ol start="25"> <li>Szabo-Hever A, Singh G, Peters-Haugrud AR, Running KLD, Seneviratne S, Zhang Z, Shi G, Bassi FM, Maccaferri M, Cattivelli L, Tuberosa R, Friesen TL, Liu Z, Xu SS, Faris JD (2023) Association mapping of resistance to tan spot in the Global Durum Panel. Phytopathology Online ahead of print doi: 10.1094/PHYTO-02-23-0043-R</li> </ol>   <ol start="26"> <li>Taliadoros D, Feurtey A, Wyatt N, Gladieux P, Friesen T, Stukenbrock E. (2023) Emergence and spread of the barley net blotch pathogen coincided with crop domestication and cultivation history. bioRxiv 2023.07.28.550921; doi: https://doi.org/10.1101/2023.07.28.550921</li> </ol>   <ol start="27"> <li>Tannous J, Cosetta CM, Drott MT, Rush TA, Abraham PE, Giannone RJ, Keller NP, Wolfe BE. (2023) <a href="https://pubmed.ncbi.nlm.nih.gov/37162223/">LaeA-regulated fungal traits mediate bacterial community assembly. </a>mBio 14: e0076923.</li> </ol>   <ol start="28"> <li>Wang Q, Song R, Fan S, Coleman JJ, Xu X, Hu X (2023) Diversity of Fusarium community assembly shapes mycotoxin accumulation of diseased wheat heads.  Molecular Ecology 32: 2504-2518.</li> </ol>   <ol start="29"> <li>Wang Q, Qin M, Coleman JJ, Shang W, Hu X (2023) Rapid and sensitive detection of Verticillium dahliae from complex samples using CRISPR/Cas12a technology combined with RPA.  Plant Disease 107: 1664-1669.</li> </ol>   <ol start="30"> <li>White NH,Neves DL, Nuckles EM, Vaillancourt LJ, Zhang J, Zhang G, Bradley CA (2023)   Identification of quinone outside inhibitor fungicide-resistant isolates of Parastagonospora nodorum from Illinois and Kentucky.  Plant Disease 107: 38-45.</li> </ol>   <ol start="31"> <li>Yuzon JD, Wyatt NA, Vasighzadeh A, Clare S, Navratil E, Friesen TL, Stukenbrock EH (2023) Hybrid inferiority and genetic incompatibilities drive divergence of fungal pathogens infecting the same host. Genetics 224: iyad037</li> </ol>

Impact Statements

The publications by NCCC307 members describing their research findings have increased understanding of how plant-fungi interactions impact economically important diseases of crops and food production and threats to humans and animals through the consumption of mycotoxin contaminated foods. The exchange of ideas and of biochemical and genetic data among members has contributed to these publications and fostered new ideas and research directions. About a quarter of the publications (8/31) have resulted from collaborations among members of the NCCC307 group (see below). Additionally, there are several ongoing collaborations (Trail and Vaillancourt; Friesen, Liu, Richards, and Gill; Keller and Drott). During the 2023 annual meeting ideas for new collaborations were developed among attendees, including arrangements to share materials and expertise, and a plan to write a joint review article that will compile our current knowledge about characterized fungal effectors for submission to an appropriate journal. The research generated from members of this NCCC307 multistate project will be of use to plant pathologists, plant breeders, and other scientists involved in the development of control strategies aimed at reducing crop diseases and mycotoxin contamination problems caused by fungi. The research will also benefit academic, government, and private-sector organizations that assess the risks that fungi pose to human and animal health.