PI3K-Mediated Regulation of Glycogen Metabolism To Facilitate Tomato chlorosis Virus Transmission by Bemisia tabaci MED.

Abstract

Tomato chlorosis virus (ToCV), transmitted by whiteflies (Bemisia tabaci), threatens global tomato production. However, the molecular mechanisms underlying the ToCV transmission by whiteflies remain largely unknown. Previous studies have shown that several key regulators of glycometabolism, downstream of the phosphoinositide 3-kinase (PI3K) pathway, are significantly increased in B. tabaci MED infected with ToCV. We demonstrate that ToCV activates PI3K in whiteflies, as evidenced by upregulated PI3K gene expression and increased PI3K enzyme activity. RNA interference-mediated knockdown of PI3K significantly reduced ToCV acquisition, retention, and transmission. Similarly, feeding whiteflies with the PI3K inhibitor PI3K-IN-1 decreased ToCV transmission, while the PI3K activator Recilisib enhanced it. Further analysis showed that the activation of PI3K enhances glycogen synthesis by upregulating genes related to glycogen synthesis, including serine/threonine kinase (AKT), glycogen synthase (GS), and glycogenin (Gly), and thus leads to an increase in glycogen content while reducing glucose levels. Conversely, the inhibition of PI3K disrupts glycogen metabolism, consequently impairing viral transmission. These findings highlight that PI3K is crucial for facilitating ToCV transmission by whiteflies and offer a potential target for controlling vector-borne plant viruses.