Abstract
Ste12 transcription factors, downstream of mitogen-activated protein kinase (MAPK) signalling pathways, are exclusively found in the fungal kingdom and regulate fungal mating, development, and pathogenicity. The nematode-trapping fungus Drechslerella dactyloides can capture free-living nematodes using constricting rings by cell inflation within 1 s when stimulated by nematodes entering the rings. The MAPK signalling pathways are involved in the trap formation of nematode-trapping fungi, but their downstream regulation is not clearly understood. In this study, disruption of the DdaSTE12 gene in D. dactyloides disabled cell inflation of constricting rings and led to an inability to capture nematodes. The number of septa of constricting rings and the ring cell vacuoles were changed in ΔDdaSTE12. Compared with the wild type, ΔDdaSTE12 reduced trap formation, conidiation, and vegetative growth by 79.3%, 80.3%, and 21.5%, respectively. The transcriptomes of ΔDdaSTE12-3, compared with those of the wild type, indicated that the expression of genes participating in trap formation processes, including signal transduction (Gpa2 and a 7-transmembrane receptor), vesicular transport and cell fusion (MARVEL domain-containing proteins), and nematode infection (PEX11 and CFEM domain-containing proteins), is regulated by DdaSTE12. The results suggest that DdaSTE12 is involved in trap formation and ring cell inflation, as well as conidiation and vegetative growth, by regulating a wide range of downstream functions. Our findings expanded the roles of Ste12 homologous transcription factors in the development of constricting rings and provided new insights into the downstream regulation of the MAPK signalling pathway involved in nematode predation.
Key points
• DdaSTE12 was the first gene disrupted in D. dactyloides.
• DdaSTE12 is related to ring cell inflation, vegetative growth, and conidiation.
• DdaSTE12 deletion resulted in defects in trap formation and ring development.
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Data availability
Strains and plasmids are available upon request. The whole genome shotgun project of D. dactyloides strain 29 (BioSample: SAMN18837316) is available at GenBank under the accession number JAGTWJ000000000 and can be freely accessed under the BioProject number PRJNA723920 (http://www.ncbi.nlm.nih.gov/bioproject/723920). Transcriptome raw data (.fastq) are available at the SRA under the BioProject number PRJNA723922 (http://www.ncbi.nlm.nih.gov/bioproject/723922). Supporting figures and data have been included in supplementary files, including ESM_1 (Fig. S1 to S4; Supplementary Tables S1 to S11) and ESM_2 (Supplementary Tables S12 to S14).
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Acknowledgements
We thank Prof. Zhiqiang An at the University of Texas Health Science Center at Houston (USA) for his kind help with the pAg1-H3 vector. We are very grateful to Prof. Weidong Chen of USDA-ARS for his valuable comments and kind help in polishing the manuscript.
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The research described here is jointly supported by the National Natural Science Foundation of China (No. 31770065) and the National Key Research and Development Program (2018YFD0201202).
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XZ Liu, MC Xiang, and YN Fan designed the study; YN Fan and Y Chen performed the research; YN Fan and WW Zhang analyzed the data; YN Fan and WW Zhang wrote the manuscript; and XZ Liu and MC Xiang revised the manuscript. All the authors reviewed and approved the manuscript.
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Fan, Y., Zhang, W., Chen, Y. et al. DdaSTE12 is involved in trap formation, ring inflation, conidiation, and vegetative growth in the nematode-trapping fungus Drechslerella dactyloides. Appl Microbiol Biotechnol 105, 7379–7393 (2021). https://doi.org/10.1007/s00253-021-11455-z
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DOI: https://doi.org/10.1007/s00253-021-11455-z