SNARE Protein AoSec22 Orchestrates Mycelial Growth, Vacuole Assembly, Trap Formation, Stress Response, and Secondary Metabolism in <i>Arthrobotrys oligospora</i>
Soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) facilitate intracellular vesicle trafficking and membrane fusion in eukaryotes and play a vital role in fungal growth, development, and pathogenicity. However, the functions of SNAREs are still largely unknown in nematod...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-01-01
|
| Series: | Journal of Fungi |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2309-608X/9/1/75 |
| _version_ | 1797440212713865216 |
|---|---|
| author | Yingmei Zhu Duanxu Zhou Na Bai Qianqian Liu Na Zhao Jinkui Yang |
| author_facet | Yingmei Zhu Duanxu Zhou Na Bai Qianqian Liu Na Zhao Jinkui Yang |
| author_sort | Yingmei Zhu |
| collection | DOAJ |
| description | Soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) facilitate intracellular vesicle trafficking and membrane fusion in eukaryotes and play a vital role in fungal growth, development, and pathogenicity. However, the functions of SNAREs are still largely unknown in nematode-trapping fungi. <i>Arthrobotrys oligospora</i> is a representative species of nematode-trapping fungi that can produce adhesive networks (traps) for nematode predation. In this study, we characterized AoSec22 in <i>A. oligospora</i>, a homolog of the yeast SNARE protein Sec22. Deletion of <i>Aosec22</i> resulted in remarkable reductions in mycelial growth, the number of nuclei, conidia yield, and trap formation, especially for traps that failed to develop mature three-dimensional networks. Further, absence of <i>Aosec22</i> impaired fatty acid utilization, autophagy, and stress tolerance; in addition, the vacuoles became small and fragmented in the hyphal cells of the ∆<i>Aosec22</i> mutant, and large vacuoles failed to form. The reduced sporulation capacity correlated with the transcriptional repression of several sporulation-related genes, and the impaired accumulation of lipid droplets is in line with the transcriptional repression of several genes involved in fatty acid oxidation. Moreover, absence of <i>Aosec22</i> remarkably impaired secondary metabolism, resulting in 4717 and 1230 compounds upregulated and downregulated in the ∆<i>Aosec22</i> mutant, respectively. Collectively, our data highlighted that the SNARE protein AoSec22 plays a pleiotropic role in mycelial growth and development, vacuole assembly, lipid metabolism, stress response, and secondary metabolism; in particular, it is required for the proper development of traps in <i>A. oligospora</i>. |
| first_indexed | 2024-03-09T12:04:54Z |
| format | Article |
| id | doaj.art-9aa70c932b224dd2a76f579c934e9c17 |
| institution | Directory Open Access Journal |
| issn | 2309-608X |
| language | English |
| last_indexed | 2024-03-09T12:04:54Z |
| publishDate | 2023-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Journal of Fungi |
| spelling | doaj.art-9aa70c932b224dd2a76f579c934e9c172023-11-30T22:59:59ZengMDPI AGJournal of Fungi2309-608X2023-01-01917510.3390/jof9010075SNARE Protein AoSec22 Orchestrates Mycelial Growth, Vacuole Assembly, Trap Formation, Stress Response, and Secondary Metabolism in <i>Arthrobotrys oligospora</i>Yingmei Zhu0Duanxu Zhou1Na Bai2Qianqian Liu3Na Zhao4Jinkui Yang5State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, School of Life Science, Yunnan University, Kunming 650032, ChinaCollege of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, School of Life Science, Yunnan University, Kunming 650032, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, School of Life Science, Yunnan University, Kunming 650032, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, School of Life Science, Yunnan University, Kunming 650032, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, School of Life Science, Yunnan University, Kunming 650032, ChinaSoluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) facilitate intracellular vesicle trafficking and membrane fusion in eukaryotes and play a vital role in fungal growth, development, and pathogenicity. However, the functions of SNAREs are still largely unknown in nematode-trapping fungi. <i>Arthrobotrys oligospora</i> is a representative species of nematode-trapping fungi that can produce adhesive networks (traps) for nematode predation. In this study, we characterized AoSec22 in <i>A. oligospora</i>, a homolog of the yeast SNARE protein Sec22. Deletion of <i>Aosec22</i> resulted in remarkable reductions in mycelial growth, the number of nuclei, conidia yield, and trap formation, especially for traps that failed to develop mature three-dimensional networks. Further, absence of <i>Aosec22</i> impaired fatty acid utilization, autophagy, and stress tolerance; in addition, the vacuoles became small and fragmented in the hyphal cells of the ∆<i>Aosec22</i> mutant, and large vacuoles failed to form. The reduced sporulation capacity correlated with the transcriptional repression of several sporulation-related genes, and the impaired accumulation of lipid droplets is in line with the transcriptional repression of several genes involved in fatty acid oxidation. Moreover, absence of <i>Aosec22</i> remarkably impaired secondary metabolism, resulting in 4717 and 1230 compounds upregulated and downregulated in the ∆<i>Aosec22</i> mutant, respectively. Collectively, our data highlighted that the SNARE protein AoSec22 plays a pleiotropic role in mycelial growth and development, vacuole assembly, lipid metabolism, stress response, and secondary metabolism; in particular, it is required for the proper development of traps in <i>A. oligospora</i>.https://www.mdpi.com/2309-608X/9/1/75<i>Arthrobotrys oligospora</i>SNARE proteinconidiationvacuole assemblytrap formationsecondary metabolism |
| spellingShingle | Yingmei Zhu Duanxu Zhou Na Bai Qianqian Liu Na Zhao Jinkui Yang SNARE Protein AoSec22 Orchestrates Mycelial Growth, Vacuole Assembly, Trap Formation, Stress Response, and Secondary Metabolism in <i>Arthrobotrys oligospora</i> Journal of Fungi <i>Arthrobotrys oligospora</i> SNARE protein conidiation vacuole assembly trap formation secondary metabolism |
| title | SNARE Protein AoSec22 Orchestrates Mycelial Growth, Vacuole Assembly, Trap Formation, Stress Response, and Secondary Metabolism in <i>Arthrobotrys oligospora</i> |
| title_full | SNARE Protein AoSec22 Orchestrates Mycelial Growth, Vacuole Assembly, Trap Formation, Stress Response, and Secondary Metabolism in <i>Arthrobotrys oligospora</i> |
| title_fullStr | SNARE Protein AoSec22 Orchestrates Mycelial Growth, Vacuole Assembly, Trap Formation, Stress Response, and Secondary Metabolism in <i>Arthrobotrys oligospora</i> |
| title_full_unstemmed | SNARE Protein AoSec22 Orchestrates Mycelial Growth, Vacuole Assembly, Trap Formation, Stress Response, and Secondary Metabolism in <i>Arthrobotrys oligospora</i> |
| title_short | SNARE Protein AoSec22 Orchestrates Mycelial Growth, Vacuole Assembly, Trap Formation, Stress Response, and Secondary Metabolism in <i>Arthrobotrys oligospora</i> |
| title_sort | snare protein aosec22 orchestrates mycelial growth vacuole assembly trap formation stress response and secondary metabolism in i arthrobotrys oligospora i |
| topic | <i>Arthrobotrys oligospora</i> SNARE protein conidiation vacuole assembly trap formation secondary metabolism |
| url | https://www.mdpi.com/2309-608X/9/1/75 |
| work_keys_str_mv | AT yingmeizhu snareproteinaosec22orchestratesmycelialgrowthvacuoleassemblytrapformationstressresponseandsecondarymetabolisminiarthrobotrysoligosporai AT duanxuzhou snareproteinaosec22orchestratesmycelialgrowthvacuoleassemblytrapformationstressresponseandsecondarymetabolisminiarthrobotrysoligosporai AT nabai snareproteinaosec22orchestratesmycelialgrowthvacuoleassemblytrapformationstressresponseandsecondarymetabolisminiarthrobotrysoligosporai AT qianqianliu snareproteinaosec22orchestratesmycelialgrowthvacuoleassemblytrapformationstressresponseandsecondarymetabolisminiarthrobotrysoligosporai AT nazhao snareproteinaosec22orchestratesmycelialgrowthvacuoleassemblytrapformationstressresponseandsecondarymetabolisminiarthrobotrysoligosporai AT jinkuiyang snareproteinaosec22orchestratesmycelialgrowthvacuoleassemblytrapformationstressresponseandsecondarymetabolisminiarthrobotrysoligosporai |