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SNARE Protein DdVam7 of the Nematode-Trapping Fungus Drechslerella dactyloides Regulates Vegetative Growth, Conidiation, and the Predatory Process via Vacuole Assembly

Soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins play conserved roles in membrane fusion events in eukaryotes and have been documented to be involved in fungal growth and pathogenesis. However, little is known about the roles of SNAREs in trap morphogenesis in n...

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Autores principales: Chen, Yue, Liu, Jia, Fan, Yani, Xiang, Meichun, Kang, Seogchan, Wei, Dongsheng, Liu, Xingzhong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769606/
https://www.ncbi.nlm.nih.gov/pubmed/36287065
http://dx.doi.org/10.1128/spectrum.01872-22
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author Chen, Yue
Liu, Jia
Fan, Yani
Xiang, Meichun
Kang, Seogchan
Wei, Dongsheng
Liu, Xingzhong
author_facet Chen, Yue
Liu, Jia
Fan, Yani
Xiang, Meichun
Kang, Seogchan
Wei, Dongsheng
Liu, Xingzhong
author_sort Chen, Yue
collection PubMed
description Soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins play conserved roles in membrane fusion events in eukaryotes and have been documented to be involved in fungal growth and pathogenesis. However, little is known about the roles of SNAREs in trap morphogenesis in nematode-trapping fungi (NTF). Drechslerella dactyloides, one of the constricting ring-forming NTF, captures free-living nematodes via rapid ring cell inflation. Here, we characterized DdVam7 of D. dactyloides, a homolog of the yeast SNARE protein Vam7p. Deletion of DdVam7 significantly suppressed vegetative growth and conidiation. The mutation significantly impaired trap formation and ring cell inflation, resulting in a markedly decreased nematode-trapping ability. A large vacuole could develop in ring cells within ~2.5 s after instant inflation in D. dactyloides. In the ΔDdVam7 mutant, the vacuoles were small and fragmented in hyphae and uninflated ring cells, and the large vacuole failed to form in inflated ring cells. The localization of DdVam7 in vacuoles suggests its involvement in vacuole fusion. In summary, our results suggest that DdVam7 regulates vegetative growth, conidiation, and the predatory process by mediating vacuole assembly in D. dactyloides, and this provides a basis for studying mechanisms of SNAREs in NTF and ring cell rapid inflation. IMPORTANCE D. dactyloides is a nematode-trapping fungus that can capture nematodes through a constricting ring, the most sophisticated trapping device. It is amazing that constricting ring cells can inflate to triple their size within seconds to capture a nematode. A large centrally located vacuole is a unique signature associated with inflated ring cells. However, the mechanism underpinning trap morphogenesis, especially vacuole dynamics during ring cell inflation, remains unclear. Here, we documented the dynamics of vacuole assembly during ring cell inflation via time-lapse imaging for the first time. We characterized a SNARE protein in D. dactyloides (DdVam7) that was involved in vacuole assembly in hyphae and ring cells and played important roles in vegetative growth, conidiation, trap morphogenesis, and ring cell inflation. Overall, this study expands our understanding of biological functions of the SNARE proteins and vacuole assembly in NTF trap morphogenesis and provides a foundation for further study of ring cell rapid inflation mechanisms.
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spelling pubmed-97696062022-12-22 SNARE Protein DdVam7 of the Nematode-Trapping Fungus Drechslerella dactyloides Regulates Vegetative Growth, Conidiation, and the Predatory Process via Vacuole Assembly Chen, Yue Liu, Jia Fan, Yani Xiang, Meichun Kang, Seogchan Wei, Dongsheng Liu, Xingzhong Microbiol Spectr Research Article Soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins play conserved roles in membrane fusion events in eukaryotes and have been documented to be involved in fungal growth and pathogenesis. However, little is known about the roles of SNAREs in trap morphogenesis in nematode-trapping fungi (NTF). Drechslerella dactyloides, one of the constricting ring-forming NTF, captures free-living nematodes via rapid ring cell inflation. Here, we characterized DdVam7 of D. dactyloides, a homolog of the yeast SNARE protein Vam7p. Deletion of DdVam7 significantly suppressed vegetative growth and conidiation. The mutation significantly impaired trap formation and ring cell inflation, resulting in a markedly decreased nematode-trapping ability. A large vacuole could develop in ring cells within ~2.5 s after instant inflation in D. dactyloides. In the ΔDdVam7 mutant, the vacuoles were small and fragmented in hyphae and uninflated ring cells, and the large vacuole failed to form in inflated ring cells. The localization of DdVam7 in vacuoles suggests its involvement in vacuole fusion. In summary, our results suggest that DdVam7 regulates vegetative growth, conidiation, and the predatory process by mediating vacuole assembly in D. dactyloides, and this provides a basis for studying mechanisms of SNAREs in NTF and ring cell rapid inflation. IMPORTANCE D. dactyloides is a nematode-trapping fungus that can capture nematodes through a constricting ring, the most sophisticated trapping device. It is amazing that constricting ring cells can inflate to triple their size within seconds to capture a nematode. A large centrally located vacuole is a unique signature associated with inflated ring cells. However, the mechanism underpinning trap morphogenesis, especially vacuole dynamics during ring cell inflation, remains unclear. Here, we documented the dynamics of vacuole assembly during ring cell inflation via time-lapse imaging for the first time. We characterized a SNARE protein in D. dactyloides (DdVam7) that was involved in vacuole assembly in hyphae and ring cells and played important roles in vegetative growth, conidiation, trap morphogenesis, and ring cell inflation. Overall, this study expands our understanding of biological functions of the SNARE proteins and vacuole assembly in NTF trap morphogenesis and provides a foundation for further study of ring cell rapid inflation mechanisms. American Society for Microbiology 2022-10-26 /pmc/articles/PMC9769606/ /pubmed/36287065 http://dx.doi.org/10.1128/spectrum.01872-22 Text en Copyright © 2022 Chen et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Chen, Yue
Liu, Jia
Fan, Yani
Xiang, Meichun
Kang, Seogchan
Wei, Dongsheng
Liu, Xingzhong
SNARE Protein DdVam7 of the Nematode-Trapping Fungus Drechslerella dactyloides Regulates Vegetative Growth, Conidiation, and the Predatory Process via Vacuole Assembly
title SNARE Protein DdVam7 of the Nematode-Trapping Fungus Drechslerella dactyloides Regulates Vegetative Growth, Conidiation, and the Predatory Process via Vacuole Assembly
title_full SNARE Protein DdVam7 of the Nematode-Trapping Fungus Drechslerella dactyloides Regulates Vegetative Growth, Conidiation, and the Predatory Process via Vacuole Assembly
title_fullStr SNARE Protein DdVam7 of the Nematode-Trapping Fungus Drechslerella dactyloides Regulates Vegetative Growth, Conidiation, and the Predatory Process via Vacuole Assembly
title_full_unstemmed SNARE Protein DdVam7 of the Nematode-Trapping Fungus Drechslerella dactyloides Regulates Vegetative Growth, Conidiation, and the Predatory Process via Vacuole Assembly
title_short SNARE Protein DdVam7 of the Nematode-Trapping Fungus Drechslerella dactyloides Regulates Vegetative Growth, Conidiation, and the Predatory Process via Vacuole Assembly
title_sort snare protein ddvam7 of the nematode-trapping fungus drechslerella dactyloides regulates vegetative growth, conidiation, and the predatory process via vacuole assembly
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769606/
https://www.ncbi.nlm.nih.gov/pubmed/36287065
http://dx.doi.org/10.1128/spectrum.01872-22
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