The sensor histidine kinase (SLN1) and acetyl-CoA carboxylase (ACC1) coordinately regulate the response of Neurospora crassa to the springtail Sinella curviseta (Collembola: Entomobryidae) attack

ABSTRACT Eukaryotes evolved various strategies to coordinate their development and metabolism in response to harsh environments. However, it remains unknown whether fungi increase their resistance to stress from fungivorous arthropods by altering phenotype and metabolite composition. In this study, we investigated the coordinated regulation of sensor histidine kinase (SLN1) and acetyl-CoA carboxylase (ACC1) on sporulation and metabolite accumulation in Neurospora crassa, particularly upon the springtail Sinella curviseta (Collembola: Entomobryidae) attack. The mutants Δsln1, Δacc1, and double mutant Δsln1::Δacc1 exhibited reduced conidia number and defective sexual reproduction in contrast to the wild type. Intriguingly, double deletion of sln1 and acc1 results in failure of beak formation and, consequently, inhibits ascospores ejection which helps Δsln1::Δacc1 to escape the predation by S. curviseta. Furthermore, sln1 and/or acc1 play critical roles in metabolic processes in N. crassa. Compared with the control, the cultures exposed to S. curviseta produced more trehalose, carotenoids, folic acid, and fatty acids, especially in the asexual stage. The deletion of sln1 and acc1 affected the trehalose content, thereby reducing the resistance of Δsln1, Δacc1, and Δsln1::Δacc1 to S. curviseta. Null of sln1 and/or acc1 altered the lipid composition and thus carotenoids synthesis. Chemical analysis showed that N. crassa formed more fatty acids and carotenoids upon the attack of S. curviseta. Taken together, our data suggest that acc1 and sln1 work together to protect N. crassa from the stress of S. curviseta. SLN1 and ACC1 compose a regulatory system that coordinates the conidiation, perithecial formation, and metabolism, especially upon fungivores stress. IMPORTANCE Understanding the regulatory pathways by which fungi respond to environmental signals through interlinked genes provides insights into the interactions between fungi and insects. The coordinated optimization of the regulatory networks is necessary for fungi to adapt to their habitats. We demonstrated that the synergistic regulation of sensor histidine kinase (SLN1) and acetyl-CoA carboxylase (ACC1) plays a critical role in regulating the fungal response to Sinella curviseta stress. Furthermore, we found that the enhanced production of trehalose, carotenoids, and 5-MTHF plays crucial role in the resistance to the fungivore. Our results provide insights into the understanding of the adaptation of N. crassa to environmental stimuli. Understanding the regulatory pathways by which fungi respond to environmental signals through interlinked genes provides insights into the interactions between fungi and insects. The coordinated optimization of the regulatory networks is necessary for fungi to adapt to their habitats. We demonstrated that the synergistic regulation of sensor histidine kinase (SLN1) and acetyl-CoA carboxylase (ACC1) plays a critical role in regulating the fungal response to Sinella curviseta stress. Furthermore, we found that the enhanced production of trehalose, carotenoids, and 5-MTHF plays crucial role in the resistance to the fungivore. Our results provide insights into the understanding of the adaptation of N. crassa to environmental stimuli.