New insights into temperature-impacted mycovirus-fungus interactions regulated by a microRNA in Lentinula edodes

Summary

When shiitake mushrooms are infected with a virus and exposed to heat stress, the virus replicates more aggressively, which makes the mushrooms more susceptible to heat damage and competitive fungi. Researchers discovered that a small regulatory RNA molecule called led-milR-21 plays a key role in this process by suppressing the mushroom’s heat defense mechanisms when the virus is present. This discovery is important because it shows how viruses can exploit heat stress to overcome fungal defenses, with implications for mushroom cultivation in a warming climate.

Background

Mycoviruses typically persist asymptomatically in fungi, but environmental factors like temperature can influence infection outcomes. Heat stress (HS) is known to impair fungal growth and thermotolerance, yet the interaction between temperature, mycoviruses, and mushroom hosts remains poorly understood, particularly in commercially important species like Lentinula edodes.

Objective

This study investigates how heat stress influences the interaction between Lentinula edodes mycovirus HKB (LeV) and its mushroom host, and to elucidate the molecular mechanisms regulating this temperature-dependent viral-host interaction, particularly through microRNA-mediated pathways.

Results

Heat stress increased LeV replication and compromised host thermotolerance in infected mycelia. The host microRNA led-milR-21 was induced by both LeV infection and heat stress, negatively regulating growth rate, thermotolerance, and resistance to Trichoderma atroviride. Led-milR-21 targeted the thermotolerance-related transcription factor LE01Gene01783, and multiple metabolic pathways including tryptophan metabolism were affected.

Conclusion

This is the first report of a fungal microRNA induced by a mycovirus. Heat stress disrupts the LeV-L. edodes equilibrium by promoting viral replication and led-milR-21 expression, which suppresses host thermotolerance through targeting LE01Gene01783. These findings enhance understanding of how fruiting body-forming fungi respond to viral infection and abiotic stress in scenarios of global warming.
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