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Identification and Characterization of the Homeobox Gene Family in Fusarium pseudograminearum Reveal Their Roles in Pathogenicity

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Abstract

Homeobox transcription factors have been implicated in filamentous growth, conidia formation and virulence in fungal pathogens. However, the presence of the homeobox gene family and their potential influence on pathogenesis in Fusarium pseudograminearum have not been investigated. F. pseudograminearum is an important plant pathogen that causes wheat and barley crown rot. In this study, we performed a genome-wide survey for F. pseudograminearum homeobox genes, and 11 FpHtfs were identified and characterized. Domain analyses revealed that all of these proteins contain a complete homeobox domain that contains three helices. Expression profiles of FpHtf genes at different pathogen stages showed that six FpHtf genes were induced during infection. Further, we generated and characterized FpHtf3 deletion mutants in F. pseudograminearum, showing it was essential for virulence. These results indicated that members of the homeobox gene family are likely involved in F. pseudograminearum pathogenicity. Our work also provides a useful foundation for further studies on the complexity and function of the homeobox gene family in F. pseudograminearum.

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All data generated or analyzed during this study are included in this published article.

References

  • Akinsanmi OA, Backhouse D, Simpfendorfer S, Chakraborty S (2006) Genetic diversity of Australian Fusarium graminearum and F. pseudograminearum. Plant Pathol 55:494–504

    Article  CAS  Google Scholar 

  • Antal Z, Rascle C, Cimerman A, Viaud M, Billon-Grand G, Choquer M, Bruel C (2012) The homeobox BcHOX8 gene in Botrytis cinerea regulates vegetative growth and morphology. PLoS ONE 7:e48134

    Article  CAS  Google Scholar 

  • Cary JW, Harris-Coward P, Scharfenstein L, Mack BM, Chang PK, Wei QJ, Lebar M, Carter-Wientjes C, Majumdar R, Mitra C et al (2017) The Aspergillus flavus homeobox gene, hbx1, is required for development and aflatoxin production. Toxins 9:315

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Chen L, Ma Y, Zhao J, Geng X, Chen W, Ding S, Li H (2019) The bZIP transcription factor FpAda1 is essential for fungal growth and conidiation in Fusarium pseudograminearum. Curr Genet 66:507

    Article  CAS  Google Scholar 

  • Coppin E, Berteaux-Lecellier V, Bidard F, Brun S, Ruprich-Robert G, Espagne E, Ait-Benkhali J, Goarin A, Nesseir A, Planamente S et al (2012) Systematic deletion of homeobox genes in Podospora anserina uncovers their roles in shaping the fruiting body. PLoS ONE 7:e37488

    Article  CAS  Google Scholar 

  • Derelle R, Lopez P, Le Guyader H, Manuel M (2007) Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evol Dev 9:212–219

    Article  CAS  Google Scholar 

  • Desplan C, Theis J, O’Farrell PH (1988) The sequence specificity of homeodomain-DNA interaction. Cell 54:1081–1090

    Article  CAS  Google Scholar 

  • Deveaux Y, Toffano-Nioche C, Claisse G, Thareau V, Morin H, Laufs P, Moreau H, Kreis M, Lecharny A (2008) Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol Biol 8:1–9

    Article  Google Scholar 

  • Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A et al (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279-285

    Article  CAS  Google Scholar 

  • Garber RL, Kuroiwa A, Gehring WJ (1983) Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J 2:2027–2036

    Article  CAS  Google Scholar 

  • Gardiner DM, McDonald MC, Covarelli L, Solomon PS, Rusu AG, Marshall M, Kazan K, Chakraborty S, McDonald BA, Manners JM (2012) Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLoS Pathog 8:e1002952

    Article  CAS  Google Scholar 

  • Gardiner DM, Benfield AH, Stiller J, Stephen S, Aitken K, Liu C, Kazan K (2018) A high-resolution genetic map of the cereal crown rot pathogen Fusarium pseudograminearum provides a near-complete genome assembly. Mol Plant Pathol 19:217–226

    Article  CAS  Google Scholar 

  • Grafenhan T, Patrick SK, Roscoe M, Trelka R, Gaba D, Chan JM, McKendry T, Clear RM, Tittlemier SA (2013) Fusarium damage in cereal grains from Western Canada. 1. Phylogenetic analysis of moniliformin-producing fusarium species and their natural occurrence in mycotoxin-contaminated wheat, oats, and rye. J Agric Food Chem 61:5425–5437

    Article  CAS  Google Scholar 

  • Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244

    Article  CAS  Google Scholar 

  • Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–2629

    Article  CAS  Google Scholar 

  • Holland PW (2013) Evolution of homeobox genes. Wiley Interdiscip Rev Dev Biol 2:31–45

    Article  CAS  Google Scholar 

  • Kazan K, Gardiner DM (2018) Fusarium crown rot caused by Fusarium pseudograminearum in cereal crops: recent progress and future prospects. Mol Plant Pathol 19:1547–1562

    Article  CAS  Google Scholar 

  • Kim S, Park SY, Kim KS, Rho HS, Chi MH, Choi J, Park J, Kong S, Park J, Goh J et al (2009) Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLoS Genet 5:e1000757

    Article  Google Scholar 

  • Li HL, Yuan HX, Fu B, Xing XP, Sun BJ, Tang WH (2012) First report of Fusarium pseudograminearum causing crown rot of wheat in Henan, China. Plant Dis 96:1065–1065

    Article  CAS  Google Scholar 

  • Liu Z, Friesen TL (2012) Polyethylene glycol (PEG)-mediated transformation in filamentous fungal pathogens. Methods Mol Biol 835:365–375

    Article  CAS  Google Scholar 

  • Liu WD, Xie SY, Zhao XH, Chen X, Zheng WH, Lu GD, Xu JR, Wang ZH (2010) A homeobox gene is essential for conidiogenesis of the rice blast fungus Magnaporthe oryzae. Mol Plant Microbe Interact 23:366–375

    Article  CAS  Google Scholar 

  • Mishra PK, Tewari JP, Clear RM, Turkington TK (2006) Genetic diversity and recombination within populations of Fusarium pseudograminearum from western Canada. Int Microbiol 9:65–68

    CAS  PubMed  Google Scholar 

  • Mukherjee K, Brocchieri L, Burglin TR (2009) A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol 26:2775–2794

    Article  CAS  Google Scholar 

  • Murthi P (2014) Review: placental homeobox genes and their role in regulating human fetal growth. Placenta 35(Suppl):S46-50

    Article  CAS  Google Scholar 

  • Nunes FD, de Almeida FC, Tucci R, de Sousa SC (2003) Homeobox genes: a molecular link between development and cancer. Pesquisa Odontologica Brasileira = Braz Oral Res 17:94–98

    Article  Google Scholar 

  • Obanor F, Chakraborty S (2014) Aetiology and toxigenicity of Fusarium graminearum and F. pseudograminearum causing crown rot and head blight in Australia under natural and artificial infection. Plant Pathol 63:1218–1229

    Article  CAS  Google Scholar 

  • Obanor F, Neate S, Simpfendorfer S, Sabburg R, Wilson P, Chakraborty S (2013) Fusarium graminearum and Fusarium pseudograminearum caused the 2010 head blight epidemics in Australia. Plant Pathol 62:79–91

    Article  CAS  Google Scholar 

  • Que F, Wang GL, Li T, Wang YH, Xu ZS, Xiong AS (2018) Genome-wide identification, expansion, and evolution analysis of homeobox genes and their expression profiles during root development in carrot. Funct Integr Genomics 18:685

    Article  CAS  Google Scholar 

  • Sabburg R, Obanor F, Aitken E, Chakraborty S (2015) Changing fitness of a necrotrophic plant pathogen under increasing temperature. Glob Change Biol 21:3126–3137

    Article  Google Scholar 

  • Siebers T, Catarino B, Agusti J (2017) Identification and expression analyses of new potential regulators of xylem development and cambium activity in cassava (Manihot esculenta). Planta 245:539–548

    Article  CAS  Google Scholar 

  • Son H, Seo YS, Min K, Park AR, Lee J, Jin JM, Lin Y, Cao P, Hong SY, Kim EK et al (2011) A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog 7:e1002310

    Article  CAS  Google Scholar 

  • Zheng WH, Zhao X, Xie QR, Huang QP, Zhang CK, Zhai HC, Xu LP, Lu GD, Shim WB, Wang ZH (2012) A conserved homeobox transcription factor Htf1 is required for Phialide development and conidiogenesis in Fusarium species. PLoS ONE 7:e45432

    Article  CAS  Google Scholar 

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Funding

This project is supported by Grants from the National Natural Science Foundation of China (U2004140 and 31961143018) and the Spcial Research and Development and Promotion Project of Henan Province (202102110226).

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Authors and Affiliations

  1. College of Plant Protection, Henan Agricultural University, Zhengzhou, 450000, Henan, China

    Yuming Ma, Jingya Zhao, Wenbo Chen, Xuejing Geng, Tianli He, Shengli Ding, Bingjian Sun, Honglian Li & Linlin Chen

  2. National Key Laboratory of Wheat and Maize Crop Science, Zhengzhou, 450000, Henan, China

    Shengli Ding, Honglian Li & Linlin Chen

Authors
  1. Yuming Ma
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  2. Jingya Zhao
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  3. Wenbo Chen
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  4. Xuejing Geng
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  5. Tianli He
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  6. Shengli Ding
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  7. Bingjian Sun
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  8. Honglian Li
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  9. Linlin Chen
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Contributions

LLC conceived and designed the research. LLC, MYM, WBC, JYZ, XJG and TLH performed the experiments and analyzed the data. SLD provided assistance for fungal infection. BJS contributed constructions. LLC wrote the paper. HLL revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Linlin Chen.

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Ma, Y., Zhao, J., Chen, W. et al. Identification and Characterization of the Homeobox Gene Family in Fusarium pseudograminearum Reveal Their Roles in Pathogenicity. Biochem Genet 60, 1601–1614 (2022). https://doi.org/10.1007/s10528-021-10150-y

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  • DOI: https://doi.org/10.1007/s10528-021-10150-y

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