Saliva of Therioaphis trifolii (Drepanosiphidae) Activates the SA Plant Hormone Pathway, Inhibits the JA Plant Hormone Pathway, and Improves Aphid Survival Rate

The spotted alfalfa aphid (<i>Therioaphis trifolii</i>) is a kind of destructive pest of cultivated alfalfa (<i>Medicago sativa</i>) that results in significant financial losses for the livestock sector. To understand how <i>T. trifolii</i> navigates the biochemical defenses of its host, we investigated the effects of susceptible and resistant aphid strains on two alfalfa cultivars. <i>T. trifolii</i> was reared for over 50 generations on two cultivars-WL343, which is susceptible to <i>T. trifolii</i>, and Zhongmu No. 1, which is resistant-resulting in the development of a resistant aphid strain (R-aphid) and a susceptible aphid strain (S-aphid). The results showed that the survival rate of R-aphids was significantly higher than that of S-aphids (<i>p</i> = 0.039) on the resistant cultivar Zhongmu No. 1, while there was no significant difference in survival rates between the two aphid strains on WL343 (<i>p</i> = 0.139). This suggests that S- and R-aphids differ in their ability to modulate plant defense mechanisms, influencing their survival rates. The application of saliva from R-aphids reared on Zhongmu No. 1 (R-saliva) reduced the repellency and toxicity of treated plants, improving aphid survival. Furthermore, R-aphid infestation and R-saliva application activated the salicylic acid (SA) signaling pathway while suppressing the jasmonic acid (JA) pathway, enhancing the host plant's suitability for aphid colonization. We propose that R-aphids may use their saliva to activate the SA pathway, which in turn inhibits JA synthesis, weakening the plant's defenses. These findings provide valuable insights into how <i>T. trifolii</i> interacts with host plant defense systems.