Diurnal Rhythms in Aphid Salivary Effector Expression and Metabolism Influence Their Performance on Wheat Plants

Core Concepts

Aphid feeding behavior, salivary effector expression, and metabolism exhibit distinct diurnal rhythms that shape their performance on wheat plants.

Abstract

The study investigates diurnal rhythms in the bird cherry-oat aphid (Rhopalosiphum padi), a major pest of cereals worldwide. The key findings are:

Aphids exhibit diurnal rhythms in feeding behaviors, particularly in the duration of phloem salivation (E1 phase), with increased salivation occurring during the early night. However, the duration of phloem and xylem sap ingestion (E2 and G phases) showed no significant diurnal variation.

Aphids produced more honeydew droplets at night compared to day, both on wheat plants and artificial diets, suggesting an internal circadian clock-driven mechanism.

Transcriptomic analysis identified 4,460 diurnally rhythmic transcripts in R. padi, with distinct expression patterns enriched in diverse metabolic pathways. Many putative salivary effectors showed diurnal rhythmicity, with 43% peaking in expression during the early night, coinciding with the heightened nighttime salivation.

Silencing key diurnally rhythmic effector genes, such as C002 and E8696, impaired aphid feeding and performance on wheat plants without affecting them on artificial diets, highlighting the time-oriented roles of these effectors in facilitating aphid-plant interactions.

Silencing diurnally rhythmic osmoregulatory genes, AQP1 and SUC1, disrupted the diurnal rhythm in honeydew excretion and reduced aphid survival and fecundity on wheat, but not on artificial diets.

These findings provide novel insights into the diurnal regulation of aphid metabolism and behaviors, and their crucial roles in shaping the aphid-plant relationship. This knowledge can aid in developing targeted pest management strategies that disrupt aphid interactions with their host plants.

Stats

Aphids produced 12.09 ± 0.75 honeydew droplets per aphid during the night compared to 8.42 ± 0.57 during the day on wheat plants.
Aphids produced 0.23 ± 0.05 honeydew droplets per aphid during the night compared to 0.09 ± 0.03 during the day on artificial diet.
Silencing AQP1 and SUC1 genes reduced aphid survival by 29% and 79%, respectively, and fecundity by 56% and 86%, respectively, on wheat plants at 96 hours post-injection.

Quotes

"Diurnal rhythms influence insect behavior and physiology, driving adaptive responses and synchronizing internal processes with daily light-dark cycles."
"Significantly, we identified distinct combinations of putative salivary effectors expressed at different times. Notably, 43% peaked in expression during early nighttime, aligning with the heightened nighttime salivation observed in the aphids using the EPG technique."
"Silencing key effector genes, which peak in expression at night, impaired aphid feeding and performance on wheat plants without impacting aphid performance on diets."

Key Insights Distilled From

Diurnal rhythmicity in salivary effector expression and metabolism shapes aphid performance on wheat plants

by Han,J., Kunk... at www.biorxiv.org 01-23-2024

https://www.biorxiv.org/content/10.1101/2024.01.20.576473v1

Deeper Inquiries

How do the diurnal rhythms in aphid salivary effector expression and metabolism interact with the circadian rhythms of their host plants to shape the aphid-plant relationship

The diurnal rhythms in aphid salivary effector expression and metabolism play a crucial role in shaping the aphid-plant relationship by influencing the interaction dynamics between the two organisms over a 24-hour period. Aphids, being phloem feeders, rely on a continuous supply of phloem sap for their nutrition and reproduction. The diurnal variation in salivary effector expression allows aphids to modulate plant responses to facilitate feeding and colonization. For example, the heightened expression of specific salivary effectors during the night, coinciding with increased phloem salivation, suggests that aphids may adjust their effector secretion to counteract nighttime changes in plant defenses or phloem quality. This temporal coordination between aphid feeding behavior and salivary effector expression likely optimizes their ability to overcome host plant defenses and extract nutrients efficiently.
In parallel, the circadian rhythms of host plants also play a significant role in shaping the aphid-plant relationship. Plants exhibit diurnal variations in various physiological processes, such as photosynthesis, nutrient transport, and defense responses. These daily fluctuations in plant physiology can influence the quality and quantity of phloem sap available to aphids, impacting their feeding behavior and performance. The synchronization of aphid diurnal rhythms with those of their host plants allows aphids to anticipate and respond to changes in plant defenses and nutrient availability, ultimately influencing their fitness and success on the host plant. By aligning their feeding activities and effector expression with the circadian rhythms of the host plant, aphids can optimize their interactions and adapt to the dynamic environment provided by the plant.

What are the potential mechanisms by which aphids sense and respond to the daily changes in their host plant physiology, and how can this knowledge be leveraged for developing novel pest control strategies

Aphids sense and respond to the daily changes in their host plant physiology through a combination of sensory mechanisms and molecular pathways that allow them to adapt their feeding behavior and effector secretion accordingly. One potential mechanism by which aphids sense these changes is through the detection of plant-derived cues, such as changes in phloem sap composition, volatile organic compounds, and secondary metabolites. These cues can trigger specific responses in aphids, leading to adjustments in feeding activities and effector expression to counteract plant defenses or exploit nutrient-rich conditions.
Moreover, aphids possess internal circadian clocks that regulate their physiological processes and behaviors in response to daily light-dark cycles. The circadian rhythms in aphids likely play a role in coordinating the diurnal variation in feeding behavior and effector expression, allowing them to anticipate and adapt to changes in their environment. By understanding the molecular pathways involved in these diurnal responses, novel pest control strategies can be developed to disrupt key regulatory mechanisms and target vulnerabilities in aphid-plant interactions. For instance, disrupting the diurnal regulation of salivary effector expression or osmoregulatory processes could potentially impair aphid fitness and performance, leading to reduced crop damage and improved pest management strategies.

Given the importance of osmoregulation in aphid biology, how can a deeper understanding of the diurnal regulation of osmoregulatory processes be utilized to disrupt aphid fitness and performance on crops

A deeper understanding of the diurnal regulation of osmoregulatory processes in aphids can be leveraged to disrupt aphid fitness and performance on crops by targeting key genes involved in osmoregulation. Osmoregulation is essential for aphids to maintain osmotic balance while feeding on sugar-rich phloem sap, and any disruption in this process can have detrimental effects on aphid survival and reproduction. By identifying and silencing diurnally rhythmic osmoregulatory genes, such as aquaporins and sucrases, it is possible to disrupt the osmoregulatory mechanisms in aphids, leading to increased hemolymph osmotic pressure and impaired feeding efficiency.
Furthermore, the diurnal regulation of osmoregulatory genes can be exploited to develop targeted pest control strategies that disrupt aphid fitness and performance on crops. By manipulating the expression of key osmoregulatory genes at specific times of the day, it may be possible to interfere with aphid feeding behavior, reduce honeydew excretion, and impair their ability to colonize host plants effectively. This targeted approach could offer a sustainable and environmentally friendly method for managing aphid populations and minimizing crop damage, ultimately contributing to improved agricultural practices and crop yield.