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FvSTR1, a striatin orthologue in Fusarium virguliforme, is required for asexual development and virulence

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Abstract

The soil-borne fungus Fusarium virguliforme causes sudden death syndrome (SDS), one of the most devastating diseases of soybean in North and South America. Despite the importance of SDS, a clear understanding of the fungal pathogenicity factors that affect the development of this disease is still lacking. We have identified FvSTR1, a F. virguliforme gene, which encodes a protein similar to a family of striatin proteins previously reported to regulate signalling pathways, cell differentiation, conidiation, sexual development, and virulence in filamentous fungi. Striatins are multi-domain proteins that serve as scaffolding units in the striatin-interacting phosphatase and kinase (STRIPAK) complex in fungi and animals. To address the function of a striatin homologue in F. virguliforme, FvSTR1 was disrupted and functionally characterized using a gene knock out strategy. The resulting Fvstr1 mutants were largely impaired in conidiation and pigmentation, and displayed defective conidia and conidiophore morphology compared to the wild-type and ectopic transformants. Greenhouse virulence assays revealed that the disruption of FvSTR1 resulted in complete loss of virulence in F. virguliforme. Microtome studies using fluorescence microscopy showed that the Fvstr1 mutants were defective in their ability to colonize the vascular system. The Fvstr1 mutants also showed a reduced transcript level of genes involved in asexual reproduction and in the production of secondary metabolites. These results suggest that FvSTR1 has a critical role in asexual development and virulence in F. virguliforme.

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References

  • Aoki T, O’Donnell K, Homma Y, Lattanzi AR (2003) Sudden-death syndrome of soybean is caused by two morphologically and phylogenetically distinct species within the Fusarium solani species complex F. virguliforme in North America and F. tucumaniae in South America. Mycologia 95:660–684

    PubMed  Google Scholar 

  • Aoki T, O’Donnell K, Scandiani MM (2005) Sudden death syndrome of soybean in South America is caused by four species of Fusarium: Fusarium brasiliense sp. nov., F. cuneirostrum sp. nov., F. tucumaniae, and F. virguliforme. Mycoscience 46:162–183. doi:10.1007/S10267-005-0235-Y

    Article  Google Scholar 

  • Aoki T, Scandiani MM, O’Donnell K (2012) Phenotypic, molecular phylogenetic, and pathogenetic characterization of Fusarium crassistipitatum sp. nov., a novel soybean sudden death syndrome pathogen from Argentina and Brazil. Mycoscience 53:167–186. doi:10.1007/s10267-011-0150-3

    Article  CAS  Google Scholar 

  • Bailly Y, Castets F (2007) Phocein: a potential actor in vesicular trafficking at Purkinje cell dendritic spines. Cerebellum 6:344–352. doi:10.1080/14734220701225912

    Article  CAS  PubMed  Google Scholar 

  • Beier A, Teichert I, Krisp C, Wolters DA, Kück U (2016) Catalytic subunit 1 of protein phosphatase 2A is a subunit of the STRIPAK complex and governs fungal sexual development. MBio 7:e00870–e00816. doi:10.1128/mBio.00870-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Benoist M, Gaillard S, Castets F (2006) The striatin family: a new signaling platform in dendritic spines. J Physiol 99:146–153. doi:10.1016/j.jphysparis.2005.12.006

    CAS  Google Scholar 

  • Benoist M, Baude A, Tasmadjian A, Dargent B, Kessler JP, Castets F (2008) Distribution of zinedin in the rat brain. J Neurochem 106:969–977. doi:10.1111/j.1471-4159.2008.05448.x

    Article  CAS  PubMed  Google Scholar 

  • Bernhards Y, Pöggeler S (2011) The phocein homologue SmMOB3 is essential for vegetative cell fusion and sexual development in the filamentous ascomycete Sordaria macrospora. Curr Genet 57:133–149. doi:10.1007/s00294-010-0333-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bölker M (1998) Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet Biol 25:143–156. doi:10.1006/fgbi.1998.1102

    Article  PubMed  Google Scholar 

  • Bradley CA, Allen T, Esker P (2014) Estimates of soybean yield reductions caused by diseases in the United States. Online publication. Extension and Outreach, Department of Crop Sciences, University of Illinois. http://extension.cropsciences.illinois.edu/fieldcrops/diseases/yield_reductions.php

  • Brar HK, Swaminathan S, Bhattacharyya MK (2011) The Fusarium virguliforme toxin FvTox1 causes foliar sudden death syndrome-like symptoms in soybean. Mol Plant-Microbe Interact 24:1179–1188. doi:10.1094/MPMI-12-10-0285

    Article  CAS  PubMed  Google Scholar 

  • Castets F, Rakitina T, Gaillard S, Moqrich A, Mattei MG, Monneron A (2000) Zinedin, SG2NA, and striatin are calmodulin-binding, WD repeat proteins principally expressed in the brain. J Biol Chem 275:19970–19977. doi:10.1074/jbc.M909782199

    Article  CAS  PubMed  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Catlett NL, Lee BN, Yoder OC, Turgeon BG (2003) Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet Newsl 50:9–11

    Article  Google Scholar 

  • Chang HX, Domier LL, Radwan O, Yendrek CR, Hudson ME, Hartman GL (2016) Identification of multiple phytotoxins produced by Fusarium virguliforme including a phytotoxic effector (FvNIS1) associated with sudden death syndrome foliar symptoms. Mol Plant-Microbe Interact 29:96–108. doi:10.1094/MPMI-09-15-0219-R

    Article  CAS  PubMed  Google Scholar 

  • Chen HW, Marinissen MJ, Oh S-W, Chen X, Melnick M, Perrimon N, Gutkind JS, Hou SX (2002) CKA, a novel multidomain protein, regulates the JUN N-terminal kinase signal transduction pathway in Drosophila. Mol Cell Biol 22:1792–1803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chevenet F, Brun C, Bañuls AL, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinf 7:439. doi:10.1186/1471-2105-7-439

    Article  Google Scholar 

  • Dadgostar H, Cheng G (2000) Membrane localization of TRAF 3 enables JNK activation. J Biol Chem 275:2539–2544

    Article  CAS  PubMed  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469. doi:10.1093/nar/gkn180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dettmann A, Heilig Y, Ludwig S, Schmitt K, Illgen J, Fleißner A, Valerius O, Seiler S (2013) HAM-2 and HAM-3 are central for the assembly of the Neurospora STRIPAK complex at the nuclear envelope and regulate nuclear accumulation of the MAP kinase MAK-1 in a MAK-2-dependent manner. Mol Microbiol 90:796–812. doi:10.1111/mmi.12399

    Article  CAS  PubMed  Google Scholar 

  • Di Pietro A, García-MacEira FI, Méglecz E, Roncero MI (2001) A MAP kinase of the vascular wilt fungus Fusarium oxysporum is essential for root penetration and pathogenesis. Mol Microbiol 39:1140–1152

    Article  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi:10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frey S, Reschka EJ, Pöggeler S (2015) Germinal center kinases SmKIN3 and SmKIN24 are associated with the Sordaria macrospora striatin-interacting phosphatase and kinase (STRIPAK) complex. PLoS One 10:e0139163. doi:10.1371/journal.pone.0139163

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao X, Jackson TA, Hartman GL, Niblack TL (2006) Interactions between the soybean cyst nematode and Fusarium solani f. sp. glycines based on greenhouse factorial experiments. Phytopathology 96:1409–1415. doi:10.1094/PHYTO-96-1409

    Article  CAS  PubMed  Google Scholar 

  • Goudreault M, D’Ambrosio LM, Kean MJ, Mullin MJ, Larsen BG, Sanchez A, Chaudhry S, Chen GI, Sicheri F, Nesvizhskii AI, Aebersold R, Raught B, Gingras AC (2009) A PP2A phosphatase high density interaction network identifies a novel striatin-interacting phosphatase and kinase complex linked to the cerebral cavernous malformation 3 (CCM3) protein. Mol Cell Proteomics 8:157–171. doi:10.1074/mcp.M800266-MCP200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  • Hashmi RY, Bond JP, Schmidt ME, Klein JH (2005) A temperature-controlled water bath method for evaluating soybean reaction to sudden death syndrome (SDS). Plant Health Prog Online. doi:10.1094/PHP-2005-0906-01-RS

  • Hughes TJ, O’Donnell K, Sink S, Rooney AP, Scandiani MM, Luque A, Bhattacharyya MK, Huang X (2014) Genetic architecture and evolution of the mating type locus in fusaria that cause soybean sudden death syndrome and bean root rot. Mycologia 106:686–697. doi:10.3852/13-318

    Article  CAS  PubMed  Google Scholar 

  • Jenczmionka NJ, Maier FJ, Lösch AP, Schäfer W (2003) Mating, conidiation and pathogenicity of Fusarium graminearum, the main causal agent of the head-blight disease of wheat, are regulated by the MAP kinase gpmk1. Curr Genet 43:87–95. doi:10.1007/s00294-003-0379-2

    CAS  PubMed  Google Scholar 

  • Jiang J, Liu X, Yin Y, Ma Z (2011) Involvement of a velvet protein FgVeA in the regulation of asexual development, lipid and secondary metabolisms and virulence in Fusarium graminearum. PLoS One 6:e28291. doi:10.1371/journal.pone.0028291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin H, Hartman GL, Nickell CD, Widholm JM (1996) Characterization and purification of a phytotoxin produced by Fusarium solani, the causal agent of soybean sudden death syndrome. Phytopathology 86:277–282

    Article  CAS  Google Scholar 

  • Kandel YR, Haudenshield JS, Srour AY, Islam KT, Fakhoury AM, Santos P, Wang J, Chilvers MI, Hartman GL, Malvick DK, Floyd CM, Mueller DS, Leandro LFS (2015) Multilaboratory comparison of quantitative PCR assays for detection and quantification of Fusarium virguliforme from soybean roots and soil. Phytopathology 105:1601–1611. doi:10.1094/PHYTO-04-15-0096-R

    Article  CAS  PubMed  Google Scholar 

  • Kandel YR, Wise KA, Bradley CA, Chilvers MI, Tenuta AU, Mueller DS (2016) Fungicide and cultivar effects on sudden death syndrome and yield of soybean. Plant Dis 100:1339–1350. doi:10.1094/PDIS-11-15-1263-RE

    Article  Google Scholar 

  • Koenning SR, Carolina N, Box PO, Wrather JA (2010) Suppression of soybean yield potential in the continental United States by plant diseases from 2006 to 2009. Plant Health Prog. doi:10.1094/PHP-2010-1122-01-RS

  • Kück U, Beier AM, Teichert I (2016) The composition and function of the striatin-interacting phosphatases and kinases (STRIPAK) complex in fungi. Fungal Genet Biol 90:31–38. doi:10.1016/j.fgb.2015.10.001

    Article  PubMed  Google Scholar 

  • Lengeler KB, Davidson RC, D’souza C, Harashima T, Shen WC, Wang P, Pan X, Waugh M, Heitman J (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64:746–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma HL, Peng YL, Gong L, Liu WB, Sun S, Liu J, Zheng CB, Fu H, Yuan D, Zhao J, Chen PC, Xie S, Zeng XM, Xiao Y-M, Liu Y, Li DWC (2009) The goldfish SG2NA gene encodes two alpha-type regulatory subunits for PP-2A and displays distinct developmental expression pattern. Gene Regul Syst Bio 3:115–129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma LJ, Geiser DM, Proctor RH, Rooney AP, O’Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K (2013) Fusarium pathogenomics. Annu Rev Microbiol 67:399–416. doi:10.1146/annurev-micro-092412-155650

    Article  CAS  PubMed  Google Scholar 

  • Mansouri S, van Wijk R, Rep M, Fakhoury AM (2009) Transformation of Fusarium virguliforme, the causal agent of sudden death syndrome of soybean. J Phytopathol 157:319–321. doi:10.1111/j.1439-0434.2008.01485.x

    Article  CAS  Google Scholar 

  • Moreno CS, Park S, Nelson K, Ashby D, Hubalek F, Lane WS, Pallas DC (2000) WD40 repeat proteins striatin and S/G(2) nuclear autoantigen are members of a novel family of calmodulin-binding proteins that associate with protein phosphatase 2A. J Biol Chem 275:5257–5263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navi SS, Yang XB, Pathology P (2008) Foliar symptom expression in association with early infection and xylem colonization by Fusarium virguliforme ( formerly F . solani f . sp . glycines), the causal agent of soybean sudden death syndrome. Plant Health Progress. doi:10.1094/PHP-2008-0222-01-RS

  • Nordzieke S, Zobel T, Fränzel B, Wolters DA, Kück U, Teichert I (2015) A fungal sarcolemmal membrane-associated protein (SLMAP) homolog plays a fundamental role in development and localizes to the nuclear envelope, endoplasmic reticulum, and mitochondria. Eukaryot Cell 14:345–358. doi:10.1128/EC.00241-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Donnell K, Sink S, Scandiani MM, Luque A, Colletto A, Biasoli M, Lenzi L, Salas G, González V, Ploper LD, Formento N, Pioli RN, Aoki T, Yang XB, Sarver BAJ (2010) Soybean sudden death syndrome species diversity within North and South America revealed by multilocus genotyping. Phytopathology 100:58–71. doi:10.1094/PHYTO-100-1-0058

    Article  PubMed  Google Scholar 

  • Pöggeler S, Kück U (2004) A WD40 repeat protein regulates fungal cell differentiation and can be replaced functionally by the mammalian homologue striatin. Eukaryot Cell 3:232–240

    Article  PubMed  PubMed Central  Google Scholar 

  • Pracheil T, Liu Z (2013) Tiered assembly of the yeast Far3-7-8-9-10-11 complex at the endoplasmic reticulum. J Biol Chem 288:16986–16997. doi:10.1074/jbc.M113.451674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy KW (1997) Fusarium solani on soybean roots: nomenclature of the causal agent of sudden death syndrome and identity and relevance of F. solani form B. Plant Dis 81:259–266. doi:10.1094/PDIS.1997.81.3.259

    Article  Google Scholar 

  • Roy KW, Lawrence GW, Hodges HH, Mclean KS, Killebrew JF (1989) Sudden death syndrome of soybean: Fusarium solani as incitant and relation of Heterodera glycines to disease severity. Phytopathology 79:191–197

    Article  Google Scholar 

  • Roy KW, Rupe JC, Hershman DE, Abney TS (1997) Sudden death syndrome of soybean. Plant Dis 81:1100–1111. doi:10.1094/PDIS.1997.81.10.1100

    Article  Google Scholar 

  • Rupe JC, Correll JC, Guerber JC, Becton CM, Gbur EE Jr, Cummings MS, Yount P (2001) Differentiation of the sudden death syndrome pathogen of soybean, Fusarium solani f.sp. glycines, from other isolates of F. solani based on cultural morphology, pathogenicity, and mitochondrial DNA restriction fragment length polymorp. Can J Bot 79:829–835. doi:10.1139/cjb-79-7-829

    CAS  Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA sepacer-length polymorphism in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci 81:8014–8019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Scandiani MM, Aoki T, Luque AG, Carmona MA, O’Donnell K (2010) First report of sexual reproduction by the soybean sudden death syndrome pathogen Fusarium tucumaniae in nature. Plant Dis 94:1411–1416. doi:10.1094/PDIS-06-10-0403

    Article  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. doi:10.1038/nmeth.2089

    Article  CAS  PubMed  Google Scholar 

  • Shim WB, Sagaram US, Choi Y-E, So J, Wilkinson HH, Lee YW (2006) FSR1 is essential for virulence and female fertility in Fusarium verticillioides and F. graminearum. Mol Plant-Microbe Interact 19:725–733. doi:10.1094/MPMI-19-0725

    Article  CAS  PubMed  Google Scholar 

  • Simonin AR, Rasmussen CG, Yang M, Glass NL (2010) Genes encoding a striatin-like protein (ham-3) and a forkhead associated protein (ham-4) are required for hyphal fusion in Neurospora crassa. Fungal Genet Biol 47:855–868. doi:10.1016/j.fgb.2010.06.010

    Article  CAS  PubMed  Google Scholar 

  • Singh NS, Shao N, McLean JR, Sevugan M, Ren L, Chew TG, Bimbo A, Sharma R, Tang X, Gould KL, Balasubramanian MK (2011) SIN-inhibitory phosphatase complex promotes Cdc11p dephosphorylation and propagates SIN asymmetry in fission yeast. Curr Biol 21(23):1968–1978. doi:10.1016/j.cub.2011.10.051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang CL (2011) Assessing the roles of striatin orthologs in fungal morphogenesis, sexual development and pathogenicity. Dissertation, University of Tesax A&M. http://oaktrust.library.tamu.edu/bitstream/handle/1969.1/ETD-TAMU-2011-08-9935

  • Wang CL, Shim WB, Shaw BD (2010) Aspergillus nidulans striatin (StrA) mediates sexual development and localizes to the endoplasmic reticulum. Fungal Genet Biol 47:789–799. doi:10.1016/j.fgb.2010.06.007

    Article  CAS  PubMed  Google Scholar 

  • Wang CL, Shim WB, Shaw BD (2016) The Colletotrichum graminicola striatin orthologue Str1 is necessary for anastomosis and is a virulence factor. Mol Plant Pathol 7:931–942. doi:10.1111/mpp.12339

    Article  Google Scholar 

  • Westphal A, Abney TS, Xing LJ, Shaner GE (2008) Sudden death syndrome of soybean. Plant Health Instr. doi:10.1094/PHI-I-2008-0102-01

  • Yamamura Y, Shim WB (2008) The coiled-coil protein-binding motif in Fusarium verticillioides Fsr1 is essential for maize stalk rot virulence. Microbiology 154:1637–1645. doi:10.1099/mic.0.2008/016782-0

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Xue C, Kim Y, Xu J (2004) A ligation-PCR approach for generating gene replacement constructs in Magnaporthe grisea. Fungal Genet Newsl 51:17–18

  • Zhao X, Kim Y, Park G, Xu JR (2005) A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell 17:1317–1329. doi:10.1105/tpc.104.029116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Fusarium virguliforme genome sequence data generated from the support of the Soybean Research and Development Council and the Iowa Soybean Association and available through http://fvgbrowse.agron.iastate.edu/ were used in this study. We thank Dr. Joe Cheatwood (SIU School of Medicine) for his generous help with the microtome study and fluorescent microscopy and Dr. Karen Renzaglia (former director of SIU IMAGE facility) for her kind help in electron microscopy.

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Correspondence to Ahmad M. Fakhoury.

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This research was funded by the United Soybean Board.

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Islam, K.T., Bond, J.P. & Fakhoury, A.M. FvSTR1, a striatin orthologue in Fusarium virguliforme, is required for asexual development and virulence. Appl Microbiol Biotechnol 101, 6431–6445 (2017). https://doi.org/10.1007/s00253-017-8387-1

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