Two sexually compatible monokaryons from a heterokaryotic Lentinula edodes strain respond differently to heat stress
BackgroundDespite the extensive research conducted on heat responses of Lentinula edodes heterokaryotic cells, the responses of the two sexually compatible monokaryons to heat stress (HS) remain largely unknown.MethodsTo bridge this gap, we examined the nucleus-specific (SP3 and SP30) heat resistant...
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Frontiers Media S.A.
2025-02-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1522075/full |
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| author | Yuan Guo Wenyu Jiao Yajie Zhang Meiting Tan Qi Gao Yu Liu Shouxian Wang |
| author_facet | Yuan Guo Wenyu Jiao Yajie Zhang Meiting Tan Qi Gao Yu Liu Shouxian Wang |
| author_sort | Yuan Guo |
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| description | BackgroundDespite the extensive research conducted on heat responses of Lentinula edodes heterokaryotic cells, the responses of the two sexually compatible monokaryons to heat stress (HS) remain largely unknown.MethodsTo bridge this gap, we examined the nucleus-specific (SP3 and SP30) heat resistant mechanisms using an integrated physiological, metabolomic and transcriptomic approach.ResultsThe results showed that HS elicited the boost of ROS and hampered mycelium growth for both monokaryons. Metabolome and transcriptome analysis demonstrated that the two sexually compatible monokaryons responded differently to HS. For SP3, the differentially expressed genes (DEGs) were significantly enriched in Mitogen-Activated Protein Kinase (MAPK) signaling, cell cycle and sugar metabolism, whereas those DEGs for SP30 were enriched in glyoxylate and dicarboxylate metabolism, and protein processing. The differentially accumulated metabolites (DAMs) of both strains were enriched in the glycerophospholipid metabolism, alpha-linolenic acid metabolism, biosynthesis of cofactors, etc, but were regulated differently in each strain. The enriched KEGG pathways for SP3 tend to be downregulated, whereas those in SP30 exhibited a contrary trend. The genes in MAPK signaling pathway were associated with the glycerophospholipid metabolism in SP3, but not in SP30. Omics-integration analysis revealed distinguishing regulatory networks and identified completely different hub genes for the two strains.DiscussionOur findings revealed, for the first time, the different heat-resistance mechanisms of the two compatible nuclei and provided candidate metabolites, responsive genes and regulatory pathways for further experimental validation. |
| format | Article |
| id | doaj-art-5beedd576b5a421a910d62e62edaab75 |
| institution | Kabale University |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj-art-5beedd576b5a421a910d62e62edaab752025-02-12T07:26:35ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-02-011610.3389/fmicb.2025.15220751522075Two sexually compatible monokaryons from a heterokaryotic Lentinula edodes strain respond differently to heat stressYuan Guo0Wenyu Jiao1Yajie Zhang2Meiting Tan3Qi Gao4Yu Liu5Shouxian Wang6Beijing Engineering Research Center for Edible Mushroom, Institute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaCollege of Life Sciences and Technology, Mudanjiang Normal University, Mudanjiang, ChinaCollege of Plant Science and Technology, Beijing University of Agriculture, Beijing, ChinaCollege of Agriculture and Food Engineering, Baise University, Baise, ChinaBeijing Engineering Research Center for Edible Mushroom, Institute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Engineering Research Center for Edible Mushroom, Institute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Engineering Research Center for Edible Mushroom, Institute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBackgroundDespite the extensive research conducted on heat responses of Lentinula edodes heterokaryotic cells, the responses of the two sexually compatible monokaryons to heat stress (HS) remain largely unknown.MethodsTo bridge this gap, we examined the nucleus-specific (SP3 and SP30) heat resistant mechanisms using an integrated physiological, metabolomic and transcriptomic approach.ResultsThe results showed that HS elicited the boost of ROS and hampered mycelium growth for both monokaryons. Metabolome and transcriptome analysis demonstrated that the two sexually compatible monokaryons responded differently to HS. For SP3, the differentially expressed genes (DEGs) were significantly enriched in Mitogen-Activated Protein Kinase (MAPK) signaling, cell cycle and sugar metabolism, whereas those DEGs for SP30 were enriched in glyoxylate and dicarboxylate metabolism, and protein processing. The differentially accumulated metabolites (DAMs) of both strains were enriched in the glycerophospholipid metabolism, alpha-linolenic acid metabolism, biosynthesis of cofactors, etc, but were regulated differently in each strain. The enriched KEGG pathways for SP3 tend to be downregulated, whereas those in SP30 exhibited a contrary trend. The genes in MAPK signaling pathway were associated with the glycerophospholipid metabolism in SP3, but not in SP30. Omics-integration analysis revealed distinguishing regulatory networks and identified completely different hub genes for the two strains.DiscussionOur findings revealed, for the first time, the different heat-resistance mechanisms of the two compatible nuclei and provided candidate metabolites, responsive genes and regulatory pathways for further experimental validation.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1522075/fullLentinula edodesheat stress responsemetabolomicstranscriptomicsmulti-omics integration |
| spellingShingle | Yuan Guo Wenyu Jiao Yajie Zhang Meiting Tan Qi Gao Yu Liu Shouxian Wang Two sexually compatible monokaryons from a heterokaryotic Lentinula edodes strain respond differently to heat stress Frontiers in Microbiology Lentinula edodes heat stress response metabolomics transcriptomics multi-omics integration |
| title | Two sexually compatible monokaryons from a heterokaryotic Lentinula edodes strain respond differently to heat stress |
| title_full | Two sexually compatible monokaryons from a heterokaryotic Lentinula edodes strain respond differently to heat stress |
| title_fullStr | Two sexually compatible monokaryons from a heterokaryotic Lentinula edodes strain respond differently to heat stress |
| title_full_unstemmed | Two sexually compatible monokaryons from a heterokaryotic Lentinula edodes strain respond differently to heat stress |
| title_short | Two sexually compatible monokaryons from a heterokaryotic Lentinula edodes strain respond differently to heat stress |
| title_sort | two sexually compatible monokaryons from a heterokaryotic lentinula edodes strain respond differently to heat stress |
| topic | Lentinula edodes heat stress response metabolomics transcriptomics multi-omics integration |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1522075/full |
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