Advertisement

R-SNARE FgSec22 is essential for growth, pathogenicity and DON production of Fusarium graminearum

  • Muhammad Adnan
  • Wenqin Fang
  • Peng Sun
  • Yangling Zheng
  • Yakubu Saddeeq Abubakar
  • Jing Zhang
  • Yi Lou
  • Wenhui ZhengEmail author
  • Guo-dong LuEmail author
Original Article
  • 101 Downloads

Abstract

SNAREs (soluble N-ethylmaleimide-sensitive factor attachment protein receptors) facilitate intracellular vesicle trafficking and membrane fusion in eukaryotic cells, and play a vital role in growth, development and pathogenicity of phytopathogens. Fusarium head blight (FHB) caused by F. graminearum is one of the most devastating diseases of wheat and barley worldwide. Sec22 is a member of the SNARE family of proteins and its homologues have been shown to have diverse biological roles in different organisms. However, the functions of this protein in the development and pathogenesis of F. graminearum are currently unknown. In this study, we employed integrated biochemical, microbiological and molecular genetic approaches to investigate the roles of FgSec22 in F. graminearum. Our data reveal that this SNARE protein is localized to endoplasmic reticulum (ER) and is indispensable for normal conidiation, conidial morphology and pathogenesis of this phytopathogenic fungus. Our biochemical assay of deoxynivalenol (DON) reveals the active involvement of this protein in the production of this mycotoxin in F. graminearum. This has further been confirmed by qRT-PCR analyses of trichothecene (TRI) genes’ expression where the ΔFgsec22 deletion mutant demonstrated a significant down-regulation of these genes in comparison to the wild-type PH-1. Unlike the wild-type and the complemented strain, the mutant strain presents a remarkable defect in colony formation which reflects the critical role it plays in vegetative growth. Collectively, our data support that the SNARE protein FgSec22 is required for vegetative growth, pathogenesis and DON biosynthesis in F. graminearum.

Keywords

Vesicle trafficking Membrane fusion Fusarium head blight Phenotypic characterization Cell wall integrity 

Notes

Acknowledgements

We really appreciate Prof. Zonghua Wang (Fujian Agriculture and Forestry University), Prof. Daniel J. Ebbole (Texas A&M University), Prof. Stefan Olsson (Fujian Agriculture and Forestry University) and Dr. Justice Norvienyeku (Fujian Agriculture and Forestry University) for their valuable suggestions and fruitful discussions.

Author contributions

Conceptualization: MA, WZ, GL; data curation: MA, YZ, YS, YL, WF, JZ; formal analysis: MA, YZ, YS, JZ; funding acquisition: WZ, GL; investigation: MA, YZ, YL, WF, JZ; methodology: MA, YZ, YL, WF, JZ; supervision: WZ, GL; validation: YL, WZ, GL; visualization: MA, YZ, WZ, GL; writing—original draft: MA, YS, WZ, GL; writing—review and editing: YZ, YL, YS, WF, JZ.

Supplementary material

294_2019_1037_MOESM1_ESM.tif (837 kb)
Fig. S1. Phylogenetic analysis and domain architecture of FgSec22 and its orthologs. Phylogenetic tree of Sec22 from fungi to mammals was constructed based on the alignment of sequences of Sec22. The neighbor-joining tree was built with MEGA7 software based on the amino acid sequence of Sec22 from each species. The conserved regions or domains are represented with different colored boxes
294_2019_1037_MOESM2_ESM.jpg (506 kb)
Fig. S2 Gene knockout and southern blot analysis of ΔFgsec22 mutant in F. graminearum. A. Split marker approach was adopted to generate ΔFgsec22 gene knockout using HPH sequence instead of FgSEC22 in the wild-type PH-1 of F. graminearum. B. Southern blot analysis of FgSEC22 gene deletion. FgSEC22 deletion mutants were confirmed by southern blot analysis, DNA was digested using Xho I and Hind III restriction enzymes. FgSec22-AF (1F) and FgSec22-AR (2R) primer pair was used to amplify the upstream region of respective gene and used this fragment as a probe during hybridization
294_2019_1037_MOESM3_ESM.tif (91.4 mb)
Fig. S3. Sexual reproduction of F. graminearumA. Carrot agar plates, black perithecia were formed on carrot agar 21 dpi. B. Cirri (masses of ascospores) formed on top of perithecium of PH-1 and ΔFgsec22-Com complemented strains and perithecium of ΔFgsec22 mutant strain as well. C. Fascicles of asci observed under microscope after squeezing the perithecia. Sexual reproduction revealed that there was no obvious variation among the wild-type and mutant strains. The carrot agar plates produced abundant perithecia in all strains. Similarly, cirri were also observed in all strains. Particular rosette-like morphology of asci was observed after breaking the perithecium in all of the strains
294_2019_1037_MOESM4_ESM.docx (18 kb)
Supplementary material 4 (DOCX 17 kb)

References

  1. Adnan M, Zheng W, Islam W, Arif M, Abubakar YS, Wang Z, Lu G (2018) Carbon catabolite repression in filamentous Fungi. Int J Mol Sci 19:48CrossRefGoogle Scholar
  2. Alexander NJ, McCormick SP, Hohn TM (1999) TRI12, a trichothecene efflux pump from Fusarium sporotrichioides: gene isolation and expression in yeast. Mol Gen Genet 261:977–984PubMedCrossRefPubMedCentralGoogle Scholar
  3. Alexander NJ, Proctor RH, McCormick SP (2009) Genes, gene clusters, and biosynthesis of trichothecenes and fumonisins in Fusarium. Toxin Rev. 28:198–215CrossRefGoogle Scholar
  4. Audenaert K, Vanheule A, Höfte M, Haesaert G (2013) Deoxynivalenol: a major player in the multifaceted response of Fusarium to its environment. Toxins (Basel) 6:1–19CrossRefGoogle Scholar
  5. Baker RW, Hughson FM (2016) Chaperoning SNARE assembly and disassembly. Nat Rev Mol Cell Biol 17:465PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bao J, Huang M, Petranovic D, Nielsen J (2018) Balanced trafficking between the ER and the Golgi apparatus increases protein secretion in yeast. AMB Express 8:37PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bas L, Papinski D, Licheva M, Torggler R, Rohringer S, Schuschnig M, Kraft C (2018) Reconstitution reveals Ykt6 as the autophagosomal SNARE in autophagosome-vacuole fusion. J Cell Biol 217:3656–3669PubMedPubMedCentralCrossRefGoogle Scholar
  8. Boenisch MJ, Broz KL, Purvine SO, Chrisler WB, Nicora CD, Connolly LR, Freitag M, Baker SE, Kistler HC (2017) Structural reorganization of the fungal endoplasmic reticulum upon induction of mycotoxin biosynthesis. Sci Rep 7:44296PubMedPubMedCentralCrossRefGoogle Scholar
  9. Brandizzi F, Barlowe C (2013) Organization of the ER-Golgi interface for membrane traffic control. Nat Rev Mol Cell Biol 14:382–392PubMedPubMedCentralCrossRefGoogle Scholar
  10. Catlett NL, Lee B-N, Yoder OC, Turgeon BG (2003) Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet Rep 50:9–11CrossRefGoogle Scholar
  11. Chatre L, Brandizzi F, Hocquellet A, Hawes C, Moreau P (2005) Sec22 and Memb11 are v-SNAREs of the anterograde endoplasmic reticulum-Golgi pathway in tobacco leaf epidermal cells. Plant Physiol 139:1244–1254PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chen S, Novick P, Ferro-Novick S (2013) ER structure and function. Curr Opin Cell Biol 25:428–433PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chen L, Tong Q, Zhang C, Ding K (2019) The transcription factor FgCrz1A is essential for fungal development, virulence, deoxynivalenol biosynthesis and stress responses in Fusarium graminearum. Curr Genet 65:153–166PubMedCrossRefPubMedCentralGoogle Scholar
  14. Chi MH, Park SY, Kim S, Lee YH (2009) A novel pathogenicity gene is required in the rice blast fungus to suppress the basal defenses of the host. PLoS Pathog 5:e1000401PubMedPubMedCentralCrossRefGoogle Scholar
  15. Choi Y-E, Xu J-R (2010) The cAMP signaling pathway in Fusarium verticillioides is important for conidiation, plant infection, and stress responses but not fumonisin production. Mol Plant Microbe Interact 23:522–533PubMedCrossRefPubMedCentralGoogle Scholar
  16. Choi UB, Zhao M, White KI, Zhou Q, Pfuetzner R, Brunger AT (2018) Single SNARE complex recycling by NSF. Biophys J 114:282aCrossRefGoogle Scholar
  17. Ding S, Mehrabi R, Koten C, Kang Z, Wei Y, Seong K, Kistler HC, Xu J-R (2009) Transducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearum. Eukaryot Cell 8:867–876PubMedPubMedCentralCrossRefGoogle Scholar
  18. Dou X, Wang Q, Qi Z, Song W, Wang W, Guo M, Zhang H, Zhang Z, Wang P, Zheng X (2011) MoVam7, a conserved SNARE involved in vacuole assembly, is required for growth, endocytosis, ROS accumulation, and pathogenesis of Magnaporthe oryzae. PLoS One 6:e16439PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dräxl S, Müller J, Li WB, Michalke B, Scherb H, Hense BA, Tschiersch J, Kanter U, Schäffner AR (2013) Caesium accumulation in yeast and plants is selectively repressed by loss of the SNARE Sec22p/SEC22. Nat Commun 4:2092PubMedCrossRefPubMedCentralGoogle Scholar
  20. El-Hasan A, Schöne J, Höglinger B, Walker F, Voegele RT (2018) Assessment of the antifungal activity of selected biocontrol agents and their secondary metabolites against Fusarium graminearum. Eur J Plant Pathol 150:91–103CrossRefGoogle Scholar
  21. El-Kasmi F, Pacher T, Strompen G, Stierhof YD, Müller LM, Koncz C, Mayer U, Jürgens G (2011) Arabidopsis SNARE protein SEC22 is essential for gametophyte development and maintenance of Golgi-stack integrity. Plant J 66(2):268–279PubMedCrossRefPubMedCentralGoogle Scholar
  22. Flanagan JJ, Mukherjee I, Barlowe C (2015) Examination of Sec22 homodimer formation and role in SNARE-dependent membrane fusion. J Biol Chem 290:10657–10666PubMedPubMedCentralCrossRefGoogle Scholar
  23. Gao HM, Liu XG, Shi HB, Lu JP, Yang J, Lin FC, Liu XH (2013) MoMon1 is required for vacuolar assembly, conidiogenesis and pathogenicity in the rice blast fungus Magnaporthe oryzae. Res Microbiol 164:300–309PubMedCrossRefPubMedCentralGoogle Scholar
  24. Gardiner DM, Kazan K, Manners JM (2009) Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genet Biol 46:604–613PubMedCrossRefPubMedCentralGoogle Scholar
  25. Goswami RS, Kistler HC (2004) Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 5:515–525PubMedCrossRefPubMedCentralGoogle Scholar
  26. Guo L, Wenner N, Kuldau GA (2015) FvSO regulates vegetative hyphal fusion, asexual growth, fumonisin B1 production, and virulence in Fusarium verticillioides. Fungal Biol 119:1158–1169PubMedCrossRefPubMedCentralGoogle Scholar
  27. Han J, Pluhackova K, Böckmann RA (2017) The multifaceted role of SNARE proteins in membrane fusion. Front Physiol 8:5PubMedPubMedCentralCrossRefGoogle Scholar
  28. Hong S-YY, So J, Lee J, Min K, Son H, Park C, Yun S-HH, Lee Y-WW (2010) Functional analyses of two syntaxin-like SNARE genes, GzSYN1 and GzSYN2, in the ascomycete Gibberella zeae. Fungal Genet Biol 47:364–372PubMedCrossRefPubMedCentralGoogle Scholar
  29. Hou Z, Xue C, Peng Y, Katan T, Kistler HC, Xu J-R (2002) A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact 15:1119–1127PubMedCrossRefPubMedCentralGoogle Scholar
  30. Hu S, Zhou X, Gu X, Cao S, Wang C, Xu JR (2014) The cAMP-PKA pathway regulates growth, sexual and asexual differentiation, and pathogenesis in fusarium graminearum. Mol Plant Microbe Interact 27:557–566PubMedCrossRefPubMedCentralGoogle Scholar
  31. Irieda H, Maeda H, Akiyama K, Hagiwara A, Saitoh H, Uemura A, Terauchi R, Takano Y (2014) Colletotrichum orbiculare secretes virulence effectors to a biotrophic interface at the primary hyphal neck via exocytosis coupled with SEC22-mediated traffic. Plant Cell 26:2265–2281PubMedPubMedCentralCrossRefGoogle Scholar
  32. Jenczmionka NJ, Schäfer W (2005) The Gpmk1 MAP kinase of Fusarium graminearum regulates the induction of specific secreted enzymes. Curr Genet 47:29–36PubMedCrossRefPubMedCentralGoogle Scholar
  33. Jiang C, Zhang C, Wu C, Sun P, Hou R, Liu H, Wang C, Xu J (2016) TRI6 and TRI10 play different roles in the regulation of deoxynivalenol (DON) production by cAMP signalling in Fusarium graminearum. Environ Microbiol 18:3689–3701PubMedCrossRefPubMedCentralGoogle Scholar
  34. Jonkers W, Dong Y, Broz K, Kistler HC (2012) The Wor1-like protein Fgp1 regulates pathogenicity, toxin synthesis and reproduction in the phytopathogenic fungus Fusarium graminearum. PLoS Pathog 8:e1002724PubMedPubMedCentralCrossRefGoogle Scholar
  35. Kang’ethe EK, Sirma AJ, Murithi G, Mburugu-Mosoti CK, Ouko EO, Korhonen HJ, Nduhiu GJ, Mungatu JK, Joutsjoki V, Lindfors E (2017) Occurrence of mycotoxins in food, feed, and milk in two counties from different agro-ecological zones and with historical outbreak of aflatoxins and fumonisins poisonings in Kenya. Food Qual Saf 1:161–170CrossRefGoogle Scholar
  36. Karnahl M, Park M, Krause C, Hiller U, Mayer U, Stierhof Y-D, Jürgens G (2018) Functional diversification of Arabidopsis SEC1-related SM proteins in cytokinetic and secretory membrane fusion. Proc Natl Acad Sci 115:6309–6314PubMedCrossRefGoogle Scholar
  37. Kazan K, Gardiner DM, Manners JM (2012) On the trail of a cereal killer: recent advances in Fusarium graminearum pathogenomics and host resistance. Mol Plant Pathol 13:399–413PubMedCrossRefGoogle Scholar
  38. Kulik T, Buśko M, Pszczółkowska A, Perkowski J, Okorski A (2014) Plant lignans inhibit growth and trichothecene biosynthesis in fusarium graminearum. Lett Appl Microbiol 59:99–107PubMedCrossRefGoogle Scholar
  39. Kurokawa K, Okamoto M, Nakano A (2014) Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER. Nat Commun 5:3653PubMedPubMedCentralCrossRefGoogle Scholar
  40. Lee H, Noh H, Mun J, Gu C, Sever S, Park S (2016) Anks1a regulates COPII-mediated anterograde transport of receptor tyrosine kinases critical for tumorigenesis. Nat Commun 7:12799PubMedPubMedCentralCrossRefGoogle Scholar
  41. Lerich A, Hillmer S, Langhans M, Scheuring D, van Bentum P, Robinson DG (2012) ER import sites and their relationship to ER exit sites: a new model for bidirectional ER-Golgi transport in higher plants. Front Plant Sci 3:143PubMedPubMedCentralCrossRefGoogle Scholar
  42. Li X, Wu Y, Shen C, Belenkaya TY, Ray L, Lin X (2015) Drosophila p24 and Sec22 regulate Wingless trafficking in the early secretory pathway. Biochem Biophys Res Commun 463:483–489PubMedPubMedCentralCrossRefGoogle Scholar
  43. Lv W, Wu J, Xu Z, Dai H, Ma Z, Wang Z (2019) The putative histone-like transcription factor FgHltf1 is required for vegetative growth, sexual reproduction, and virulence in Fusarium graminearum. Curr Genet 65:981–994PubMedCrossRefPubMedCentralGoogle Scholar
  44. Maeda K, Nakajima Y, Motoyama T, Kitou Y, Kosaki T, Saito T, Nishiuchi T, Kanamaru K, Osada H, Kobayashi T (2014) Effects of acivicin on growth, mycotoxin production and virulence of phytopathogenic fungi. Lett Appl Microbiol 59:377–383PubMedCrossRefPubMedCentralGoogle Scholar
  45. Maeda K, Nakajima Y, Tanahashi Y, Kitou Y, Miwa A, Kanamaru K, Kobayashi T, Nishiuchi T, Kimura M (2017) l-Threonine and its analogue added to autoclaved solid medium suppress trichothecene production by Fusarium graminearum. Arch Microbiol 199:945–952PubMedCrossRefPubMedCentralGoogle Scholar
  46. Magan N, Medina A (2016) Integrating gene expression, ecology and mycotoxin production by Fusarium and Aspergillus species in relation to interacting environmental factors. World Mycotoxin J 9:673–684CrossRefGoogle Scholar
  47. McCormick SP, Harris LJ, Alexander NJ, Ouellet T, Saparno A, Allard S, Desjardins AE (2004) Tri1 in Fusarium graminearum encodes a P450 oxygenase. Appl Environ Microbiol 70:2044–2051PubMedPubMedCentralCrossRefGoogle Scholar
  48. Menke J, Dong Y, Kistler HC (2012) Fusarium graminearum Tri12p influences virulence to wheat and trichothecene accumulation. Mol Plant Microbe Interact 25:1408–1418PubMedCrossRefPubMedCentralGoogle Scholar
  49. Nair U, Klionsky DJ (2011) Autophagosome biogenesis requires SNAREs. Autophagy 7(12):1570–1572PubMedPubMedCentralCrossRefGoogle Scholar
  50. Pani G, Scherm B, Azara E, Balmas V, Jahanshiri Z, Carta P, Fabbri D, Dettori MA, Fadda A, Dessì A (2014) Natural and natural-like phenolic inhibitors of type B trichothecene in vitro production by the wheat (Triticum sp.) pathogen Fusarium culmorum. J Agric Food Chem 62:4969–4978PubMedCrossRefPubMedCentralGoogle Scholar
  51. Paul PA, Lipps PE, Hershman DE, McMullen MP, Draper MA, Madden LV (2008) Efficacy of triazole-based fungicides for Fusarium head blight and deoxynivalenol control in wheat: a multivariate meta-analysis. Phytopathology 98:999–1011PubMedCrossRefPubMedCentralGoogle Scholar
  52. Qin J, Wang G, Jiang C, Xu JR, Wang C (2015) Fgk3 glycogen synthase kinase is important for development, pathogenesis, and stress responses in Fusarium graminearum. Sci Rep 5:8504PubMedPubMedCentralCrossRefGoogle Scholar
  53. Sharma KK, Pothana A, Prasad K, Shah D, Kaur J, Bhatnagar D, Chen ZY, Raruang Y, Cary JW, Rajasekaran K et al (2018) Peanuts that keep aflatoxin at bay: a threshold that matters. Plant Biotechnol J 16:1024–1033PubMedCrossRefPubMedCentralGoogle Scholar
  54. Shen L, Yang S, Yang T, Liang J, Cheng W, Wen J, Liu Y, Li J, Shi L, Tang Q et al (2016) CaCDPK15 positively regulates pepper responses to Ralstonia solanacearum inoculation and forms a positive-feedback loop with CaWRKY40 to amplify defense signaling. Sci Rep 6:22439PubMedPubMedCentralCrossRefGoogle Scholar
  55. Sobrova P, Adam V, Vasatkova A, Beklova M, Zeman L, Kizek R (2010) Deoxynivalenol and its toxicity. Interdiscip Toxicol 3:94–99PubMedPubMedCentralCrossRefGoogle Scholar
  56. Song W, Dou X, Qi Z, Wang Q, Zhang X, Zhang H, Guo M, Dong S, Zhang Z, Wang P (2010) R-SNARE homolog MoSec22 is required for conidiogenesis, cell wall integrity, and pathogenesis of Magnaporthe oryzae. PLoS One 5:e13193PubMedPubMedCentralCrossRefGoogle Scholar
  57. Spang A (2013) Retrograde traffic from the Golgi to the endoplasmic reticulum. Cold Spring Harb Perspect Biol 5:a013391PubMedPubMedCentralCrossRefGoogle Scholar
  58. Tang W, Ru Y, Hong L, Zhu Q, Zuo R, Guo X, Wang J, Zhang H, Zheng X, Wang P et al (2015) System-wide characterization of bZIP transcription factor proteins involved in infection-related morphogenesis of Magnaporthe oryzae. Environ Microbiol 17:1377–1396PubMedCrossRefPubMedCentralGoogle Scholar
  59. Tokai T, Koshino H, Takahashi-Ando N, Sato M, Fujimura M, Kimura M (2007) Fusarium Tri4 encodes a key multifunctional cytochrome P450 monooxygenase for four consecutive oxygenation steps in trichothecene biosynthesis. Biochem Biophys Res Commun 353:412–417PubMedCrossRefPubMedCentralGoogle Scholar
  60. Traeger S, Nowrousian M (2015) Functional analysis of developmentally Regulated genes chs7 and sec22 in the Ascomycete Sordaria macrospora. G3 (Bethesda) 5:1233–1245CrossRefGoogle Scholar
  61. Tralamazza SM, Bemvenuti RH, Zorzete P, de Souza Garcia F, Corrêa B (2016) Fungal diversity and natural occurrence of deoxynivalenol and zearalenone in freshly harvested wheat grains from Brazil. Food Chem 196:445–450PubMedCrossRefPubMedCentralGoogle Scholar
  62. Varga J, Tóth B, Mesterházy Á, Téren J, Fazekas B (2004) Mycotoxigenic fungi and mycotoxins in foods and feeds in Hungary. In: Logrieco A, Visconti A (eds) An overview on toxigenic fungi and mycotoxins in Europe. Kluwer Academic Publishers, The Netherlands, pp 123–139CrossRefGoogle Scholar
  63. Wang J, Tian L, Zhang D-D, Short DPG, Zhou L, Song S-S, Liu Y, Wang D, Kong Z-Q, Cui W-Y (2018) SNARE-encoding genes VdSec22 and VdSso1 mediate protein secretion required for full virulence in Verticillium dahliae. Mol Plant Microbe Interact 31:651–664PubMedCrossRefPubMedCentralGoogle Scholar
  64. Wedlich-Soldner R (2002) A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J 19:1974–1986CrossRefGoogle Scholar
  65. Xie Q, Chen A, Zhang Y, Zhang C, Hu Y, Luo Z, Wang B, Yun Y, Zhou J, Li G et al (2019) ESCRT-III accessory proteins regulate fungal development and plant infection in Fusarium graminearum. Curr Genet 65:1041–1055PubMedCrossRefPubMedCentralGoogle Scholar
  66. Xu L, Wang M, Tang G, Ma Z, Shao W (2019) The endocytic cargo adaptor complex is required for cell-wall integrity via interacting with the sensor FgWsc2B in Fusarium graminearum. Curr Genet 65:1071–1080PubMedCrossRefPubMedCentralGoogle Scholar
  67. Yang W, Cao X, Li X (2017) Enhanced simultaneous overlap extension-PCR by gold nanoparticles. Nanomedicine 13:2263–2266PubMedCrossRefPubMedCentralGoogle Scholar
  68. Yang P, Chen Y, Wu H, Fang W, Liang Q, Zheng Y, Olsson S, Zhang D, Zhou J, Wang Z et al (2018) The 5-oxoprolinase is required for conidiation, sexual reproduction, virulence and deoxynivalenol production of Fusarium graminearum. Curr Genet 64:285–301PubMedCrossRefPubMedCentralGoogle Scholar
  69. Yin T, Zhang Q, Wang J, Liu H, Wang C, Xu JR, Jiang C (2018) The cyclase-associated protein FgCap1 has both protein kinase A-dependent and-independent functions during deoxynivalenol production and plant infection in Fusarium graminearum. Mol Plant Pathol 19:552–563PubMedCrossRefPubMedCentralGoogle Scholar
  70. Yu J-HH, Hamari Z, Han K-HH, Seo J-AA, Reyes-Domínguez Y, Scazzocchio C (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41:973–981PubMedCrossRefPubMedCentralGoogle Scholar
  71. Yuen GY, Schoneweis SD (2007) Strategies for managing Fusarium head blight and deoxynivalenol accumulation in wheat. Int J Food Microbiol 119:126–130PubMedCrossRefPubMedCentralGoogle Scholar
  72. Zhang H, Li B, Fang Q, Li Y, Zheng X, Zhang Z (2016) SNARE protein FgVam7 controls growth, asexual and sexual development, and plant infection in Fusarium graminearum. Mol Plant Pathol 17:108–119PubMedCrossRefPubMedCentralGoogle Scholar
  73. Zhang L, Liu C, Wang L, Sun S, Liu A, Liang Y, Yu J, Dong H (2019a) FgPEX1 and FgPEX10 are required for the maintenance of Woronin bodies and full virulence of Fusarium graminearum. Curr Genet 65:1383–1396CrossRefGoogle Scholar
  74. Zhang L, Wang L, Liang Y, Yu J (2019b) FgPEX4 is involved in development, pathogenicity, and cell wall integrity in Fusarium graminearum. Curr Genet 65:747–758PubMedCrossRefPubMedCentralGoogle Scholar
  75. Zhao X, Yang H, Liu W, Duan X, Shang W, Xia D, Tong C (2015) Sec22 regulates endoplasmic reticulum morphology but not autophagy and is required for eye development in Drosophila. J Biol Chem 290:7943–7951PubMedPubMedCentralCrossRefGoogle Scholar
  76. Zhao Y, Holmgren BT, Hinas A (2017) The conserved SNARE SEC-22 localizes to late endosomes and negatively regulates RNA interference in Caenorhabditis elegans. RNA 23:297–307PubMedPubMedCentralCrossRefGoogle Scholar
  77. Zheng D, Zhang S, Zhou X, Wang C, Xiang P, Zheng Q, Xu J-R (2012) The FgHOG1 pathway regulates hyphal growth, stress responses, and plant infection in Fusarium graminearum. PLoS One 7:e49495PubMedPubMedCentralCrossRefGoogle Scholar
  78. Zheng H, Miao P, Lin X, Li L, Wu C, Chen X, Abubakar YS, Norvienyeku J, Li G, Zhou J (2018) Small GTPase Rab7-mediated FgAtg9 trafficking is essential for autophagy-dependent development and pathogenicity in Fusarium graminearum. PLoS Genet 14:e1007546PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Muhammad Adnan
    • 1
    • 2
  • Wenqin Fang
    • 1
    • 2
  • Peng Sun
    • 1
    • 2
  • Yangling Zheng
    • 1
    • 2
  • Yakubu Saddeeq Abubakar
    • 4
  • Jing Zhang
    • 1
    • 2
  • Yi Lou
    • 1
    • 2
  • Wenhui Zheng
    • 1
    • 2
    • 3
    Email author
  • Guo-dong Lu
    • 1
    • 2
    Email author
  1. 1.State Key Laboratory of Ecological Pest Control for Fujian and Taiwan CropsFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.Key Laboratory of Biopesticides and Chemical Biology of Education MinistryFujian Agriculture and Forestry UniversityFuzhouChina
  3. 3.Temasek Life Sciences LaboratoryNational University of SingaporeSingaporeSingapore
  4. 4.Department of Biochemistry, Faculty of Life SciencesAhmadu Bello UniversityZariaNigeria

Personalised recommendations