Endophytic entomopathogenic fungi remodel phyllosphere microbiome and metabolome to suppress Spodoptera frugiperda and enhance parasitoid biocontrol

In the vast fields of agriculture, plants are not merely passive victims of hungry insects; they are active participants in a complex chemical war. When a plant is attacked, it often responds by producing defensive compounds or by altering its internal chemistry to make itself less appetizing or more toxic to the invader. However, plants do not fight these battles alone. They host communities of microscopic organisms on their leaves and within their tissues, known as the microbiome. These tiny residents can influence the plant's health, sometimes boosting its growth or helping it resist disease. Scientists have long wondered if we could harness these natural allies to protect crops without relying on harsh chemical sprays. One promising avenue involves using beneficial fungi that live inside plants without harming them, known as endophytes. These fungi can act as invisible bodyguards, changing the plant's internal environment in ways that confuse or weaken pests.

A recent study from researchers at Guizhou University in China explores how two specific strains of these friendly fungi might help protect maize, a vital global crop, from the fall armyworm. This pest is a voracious eater that has spread rapidly across the world, causing massive damage to corn fields. The researchers wanted to understand not just if these fungi could stop the worms, but how they did it. They looked at the entire system: the growth of the corn plant, the tiny bacteria and fungi living on its leaves, the chemical compounds the plant produced, and how these changes affected both the pest and a natural enemy of the pest, a tiny wasp that lays its eggs inside the worm. The goal was to see if these fungi could make the plant a better fortress and a better ally for the wasp, creating a three-way partnership to control the infestation.

The researchers began by introducing two different fungal strains, named GL-5 and H8, into young maize seedlings. They did this by pouring a liquid containing fungal spores onto the soil around the roots, allowing the fungi to grow inside the plant. As the seedlings grew, the team measured their size and health. Both fungal strains helped the plants grow taller and develop longer roots and leaves compared to plants that received no treatment. The plants treated with the fungi were visibly more vigorous, suggesting that these microscopic guests were not just living there but were actively helping their host thrive. This initial boost in growth set the stage for the next phase of the experiment, where the researchers introduced the fall armyworm larvae to the treated plants.

When the armyworms ate the leaves of the fungus-treated plants, their development was thrown into chaos. The worms that fed on the plants with the GL-5 strain took much longer to grow through their early stages, and many died before they could become adults. The worms that ate the H8-treated plants also struggled, particularly in their later larval stages and as pupae. The physical size of the worms that did survive was smaller, and they weighed significantly less than those that ate untreated leaves. For the worms that did manage to become adults, their ability to reproduce was severely hampered. Those fed on GL-5-treated plants laid far fewer eggs, and the time it took for them to start laying eggs was much longer. Essentially, the fungi had turned the corn plants into a difficult diet that slowed the worms down, stunted their growth, and reduced their ability to have offspring.

The study also looked at what was happening inside the plant and the pest to explain these results. The researchers found that the fungi changed the chemical makeup of the corn leaves. The GL-5 strain caused the plant to build up higher levels of certain defensive chemicals, specifically flavonoids and phenolic acids, which are known to deter insects. At the same time, the fungi altered the community of bacteria living on the leaf surface. The GL-5 strain encouraged the growth of a specific type of bacteria called Enterobacter, which is linked to the production of these defensive chemicals. In contrast, the H8 strain encouraged a different bacterium called Chryseobacterium and changed the plant's sugar metabolism. These changes in the plant's chemistry and its microbial neighbors disrupted the worm's own internal systems. The worms that ate the treated plants had trouble processing toxins, with their detoxification enzymes either overworked or suppressed, leaving them vulnerable and unable to develop properly.

Perhaps the most surprising finding was how these changes affected a natural enemy of the fall armyworm: a parasitic wasp called Microplitis manilae. This wasp hunts the worms by laying its eggs inside them, eventually killing the host. The researchers wanted to know if the fungi-treated plants would help or hurt these helpful wasps. They found that the GL-5 strain actually made the wasps more effective. When wasps were allowed to hunt worms that had been feeding on GL-5-treated plants, they successfully parasitized more of them, and the wasp cocoons they produced were heavier and stronger. This suggests that the changes in the plant made the worms easier targets for the wasps, perhaps by weakening the worms or changing the signals they sent out. However, the H8 strain did not provide the same benefit to the wasps, highlighting that different fungal strains can have very specific and distinct effects on the entire ecosystem.

The study concludes that these endophytic fungi are powerful tools for managing pests, but they work in different ways depending on the strain used. The GL-5 strain appears to be the superior choice for a combined strategy, as it not only weakens the pest directly but also boosts the performance of the natural predators that help control it. By reshaping the plant's internal chemistry and the community of microbes on its leaves, these fungi create an environment where the pest struggles to survive and reproduce, while its natural enemies thrive. This research offers a glimpse into a future where farmers might use these microscopic allies to protect their crops, relying on the complex relationships between plants, fungi, insects, and bacteria to maintain healthy fields without the need for heavy chemical intervention. The findings provide a clear mechanism for how these interactions work, paving the way for more sustainable and effective ways to fight one of agriculture's most destructive pests.