<p>Aphids (Hemiptera: Aphididae) are important phloem-feeding pests in global agriculture, and their interactions with plants constitute a typical coevolutionary system involving complex molecular signaling, behavioral regulation, and ecological effects. Aphid–plant interactions can be viewed as a dynamic “arms race” that determines plant resistance levels and aphid adaptive capacity. This review systematically summarizes plant defense mechanisms and aphid counter-defense strategies: plants perceive aphid invasion via pattern recognition receptors and resistance proteins, which activate defense signaling pathways mediated by salicylic acid (SA) and jasmonic acid (JA). In turn, aphids suppress or evade plant defenses by modulating feeding behavior, secreting salivary effectors, undergoing metabolic adaptation, and relying on symbiont assistance. Despite substantial advances to date, current understanding of aphid–plant interactions remains fragmented across molecular, ecological, and environmental hierarchical scales. Knowledge gaps are especially prominent concerning interactive impacts of aphid effectors, endosymbionts, fluctuating environmental conditions, and plant virus transmission. This review delivers an integrated, holistic synthesis bridging molecular mechanisms and ecological consequences. Additionally, the regulatory roles of environmental factors—including temperature, CO<sub>2</sub> concentration, light, water availability, natural enemy pressure, and viral infection on the outcomes of these interactions. It also highlights the potential applications of these insights in aphid-resistant crops, developing RNAi-based control methods, and designing ecological management strategies. A deep understanding of the multilayered mechanisms underlying aphid–plant interactions helps reveal coevolution patterns and provides a theoretical foundation and potential genetic resources for developing novel, environmentally friendly, and sustainable aphid management strategies. Overall, we establish an integrated framework showing that aphid–plant interplay is governed by combined influences of plant defenses, aphid counter-defenses, symbionts, plant viruses and environmental factors, yielding fresh insights for sustainable aphid control.</p>

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Aphid–plant interactions: from molecular games to ecological outcomes

  • Zi-Meng Gui,
  • Liang-De Tang,
  • Lian-Sheng Zang,
  • Ricardo Ramirez-Romero,
  • Tong-Xian Liu

摘要

Aphids (Hemiptera: Aphididae) are important phloem-feeding pests in global agriculture, and their interactions with plants constitute a typical coevolutionary system involving complex molecular signaling, behavioral regulation, and ecological effects. Aphid–plant interactions can be viewed as a dynamic “arms race” that determines plant resistance levels and aphid adaptive capacity. This review systematically summarizes plant defense mechanisms and aphid counter-defense strategies: plants perceive aphid invasion via pattern recognition receptors and resistance proteins, which activate defense signaling pathways mediated by salicylic acid (SA) and jasmonic acid (JA). In turn, aphids suppress or evade plant defenses by modulating feeding behavior, secreting salivary effectors, undergoing metabolic adaptation, and relying on symbiont assistance. Despite substantial advances to date, current understanding of aphid–plant interactions remains fragmented across molecular, ecological, and environmental hierarchical scales. Knowledge gaps are especially prominent concerning interactive impacts of aphid effectors, endosymbionts, fluctuating environmental conditions, and plant virus transmission. This review delivers an integrated, holistic synthesis bridging molecular mechanisms and ecological consequences. Additionally, the regulatory roles of environmental factors—including temperature, CO2 concentration, light, water availability, natural enemy pressure, and viral infection on the outcomes of these interactions. It also highlights the potential applications of these insights in aphid-resistant crops, developing RNAi-based control methods, and designing ecological management strategies. A deep understanding of the multilayered mechanisms underlying aphid–plant interactions helps reveal coevolution patterns and provides a theoretical foundation and potential genetic resources for developing novel, environmentally friendly, and sustainable aphid management strategies. Overall, we establish an integrated framework showing that aphid–plant interplay is governed by combined influences of plant defenses, aphid counter-defenses, symbionts, plant viruses and environmental factors, yielding fresh insights for sustainable aphid control.