Viruses have long been regarded as obligate parasites, notorious for plundering nutrients from their hosts and causing detrimental effects. However, recent scientific breakthroughs are challenging this conventional wisdom, revealing that under certain circumstances, viruses can bestow unexpected benefits upon their hosts. A prime example lies in the growing body of research indicating that viral infections can significantly enhance a plant’s ability to withstand drought, although the underlying mechanisms have remained elusive—until now.
A groundbreaking study published in Plant Cell & Environment, titled “+RNA viruses enhance plant drought tolerance through modulation of phospholipase Dα1 (PLDα1)-derived phosphatidic acid (PA),” has shed light on this fascinating phenomenon. The research team discovered that +RNA viruses enhance plant drought tolerance by modulating phospholipase Dα1 (PLDα1) and its product, phosphatidic acid (PA), thereby activating the abscisic acid (ABA) signaling pathway.
The researchers focused on Potato virus Y (PVY) and found that upon infecting its host, PVY continuously induced downstream transcriptional activation of ABA and stomatal closure. Stomatal closure, a critical mechanism for reducing water loss, began three days post-inoculation and persisted until the plant’s demise. An intriguing finding emerged when chemical inhibitors were used to suppress ABA synthesis or degradation. While these inhibitors significantly altered the water loss rate in control plants, they had no impact on the water loss rate of infected leaves, indicating that the virus-induced drought tolerance is independent of ABA accumulation. On the other hand, treating infected leaves with 1-butanol, an inhibitor of PLD, nearly completely suppressed virus-induced stomatal closure and transcriptional activation, suggesting a crucial role for PLD and PA in this process.
Further experiments demonstrated that the sole expression of the viral 6K2 protein was sufficient to induce downstream transcriptional activation of ABA and enhance drought tolerance. Knocking out PLDα1 significantly inhibited virus-induced transcriptional activation, stomatal closure, and drought tolerance. Moreover, point mutations that disrupted the interaction between 6K2 and PLDα1 caused 6K2 to lose its ability to induce transcriptional activation and stomatal closure. These results strongly indicate that PVY enhances plant drought tolerance by regulating PLDα1 and PA through its encoded 6K2 protein.
The study also revealed that PA binds to ABI, a negative regulator of ABA. Overexpressing ABI point mutants insensitive to PA significantly suppressed virus-induced drought tolerance, suggesting that virus-induced PA activates the downstream ABA signaling pathway by weakening ABI’s inhibitory effect on the ABA pathway, thus enhancing drought tolerance. Additionally, knocking out PLDα1 significantly inhibited the expression of genes related to virus-induced ABA synthesis and transport. This indicates that the downstream ABA pathway activated by PA induces ABA synthesis through positive feedback, explaining why viruses can increase ABA levels while the induced drought tolerance remains independent of ABA accumulation.
The researchers further validated their findings using Turnip mosaic virus and Tomato bushy stunt virus, demonstrating that virus-induced drought tolerance is a conserved downstream response to viral hijacking of PA. They propose that during the assembly of viral replication complexes, viruses require the enrichment of PA, which inadvertently activates the ABA signaling pathway and enhances plant drought tolerance. Therefore, enhanced drought tolerance can be considered an unexpected benefit for plants during viral infections. Given that this trait also improves plant survival under drought conditions, it has been preserved throughout the long-term co-evolution of plants and viruses.
This study not only challenges our understanding of plant-virus interactions but also opens up new possibilities for developing strategies to enhance plant resilience to drought. As climate change continues to pose significant challenges to global agriculture, uncovering such unexpected mechanisms could provide valuable insights for sustainable crop production. Future research could explore the potential of harnessing these viral-induced mechanisms to engineer drought-tolerant crops, offering hope for more resilient agricultural systems in the face of a changing climate.