The Actin Cytoskeleton Mediates Transmission of “Candidatus Liberibacter solanacearum” by the Carrot Psyllid

ABSTRACT

Several vector-borne plant pathogens have evolved mechanisms to exploit and to hijack vector host cellular, molecular, and defense mechanisms for their transmission. In the past few years, Liberibacter species, which are transmitted by several psyllid vectors, have become an economically important group of pathogens that have devastated the citrus industry and caused tremendous losses to many other important crops worldwide. The molecular mechanisms underlying the interactions of Liberibacter species with their psyllid vectors are poorly studied. “Candidatus Liberibacter solanacearum,” which is associated with important vegetable diseases, is transmitted by the carrot psyllid Bactericera trigonica in a persistent manner. Here, we elucidated the role of the B. trigonica Arp2/3 protein complex, which plays a major role in regulation of the actin cytoskeleton, in the transmission of “Ca. Liberibacter solanacearum.” “Ca. Liberibacter solanacearum” colocalized with ArpC2, a key protein in this complex, and this colocalization was strongly associated with actin filaments. Silencing of the psyllid ArpC2 disrupted the colocalization and the dynamics of F-actin. Silencing of RhoGAP21 and Cdc42, which act in the signaling cascade leading to upregulation of Arp2/3 and F-actin bundling, showed similar results. On the other hand, silencing of ArpC5, another component of the complex, did not induce any significant effects on F-actin formation. Finally, ArpC2 silencing caused a 73.4% reduction in “Ca. Liberibacter solanacearum” transmission by psyllids, strongly suggesting that transmission of “Ca. Liberibacter solanacearum” by B. trigonica is cytoskeleton dependent and “Ca. Liberibacter solanacearum” interacts with ArpC2 to exploit the intracellular actin nucleation process for transmission. Targeting this unique interaction could lead to the development of a novel strategy for the management of Liberibacter-associated diseases.

IMPORTANCE Plant diseases caused by vector-borne pathogens are responsible for tremendous losses and threaten some of the most important agricultural crops. A good example is the citrus greening disease, which is caused by bacteria of the genus Liberibacter and is transmitted by psyllids; it has devastated the citrus industry in the United States, China, and Brazil. Here, we show that psyllid-transmitted “Candidatus Liberibacter solanacearum” employs the actin cytoskeleton of psyllid gut cells, specifically the ArpC2 protein in the Arp2/3 complex of this system, for movement and transmission in the vector. Silencing of ArpC2 dramatically influenced the interaction of “Ca. Liberibacter solanacearum” with the cytoskeleton and decreased the bacterial transmission to plants. This system could be targeted to develop a novel approach for the control of Liberibacter-associated diseases.