Abstract
Huanglongbing, the most destructive citrus disease worldwide, is caused by the bacterium ‘Candidatus Liberibacter asiaticus’ (CLas) and is vectored by the Asian citrus psyllid (ACP). Very little is known about the form and distribution of CLas in infected psyllids, especially at the ultrastructural level. Here, we examined these aspects by transmission electron microscopy, combined with immunogold labeling. In CLas-exposed ACP adults, the CLas bacterial cells were found to be pleomorphic taking tubular, spherical, or flask-shaped forms, some of which seemed to divide further. Small or large aggregates of CLas were found in vacuolated cytoplasmic pockets of most ACP organs and tissues examined, including the midgut, filter chamber, hindgut, Malpighian tubules, and secretory cells of the salivary glands, in addition to fat tissues, epidermis, muscle, hemocytes, neural tissues, bacteriome, and walls of the female spermatheca and oviduct. Large aggregates of CLas were found outside the midgut within the filter chamber and between the sublayers of the basal lamina of the hindgut and Malpighian tubules. Novel intracytoplasmic structures that we hypothesized as ‘putative CLas multiplication sites’ were found in the cells of the midgut, salivary glands, and other tissues in CLas-exposed ACP. These structures, characterized by containing a granular matrix and closely packed bacterial cells, were unbound by membranes and were frequently associated with rough endoplasmic reticulum. Our results point to the close association between CLas and its psyllid vector, and provide support for a circulative-propagative mode of transmission.
Highlights
Huanglongbing (HLB, known as citrus greening), the most destructive disease to citrus plants in the world, is putatively caused in Asia and the Americas by the phloem-restricted gram-negative bacteria Candidatus Liberibacter asiaticus (CLas), vectored by the Asian citrus psyllid (ACP, Diaphorina citri, Hemiptera: Liviidae) [1,2]
D. citri guts, CLas accumulates inside Liberibacter containing vacuoles (LCVs), and that these vacuoles associate with the host cell rough endoplasmic reticulum (RER), suggesting that CLas can accumulate intracellularly in the psyllid cells
Our results showed that CLas is abundantly found in tubular/filamentous and quasispherical forms in many different ACP organs and tissues, indicating a systemic infection
Summary
Huanglongbing (HLB, known as citrus greening), the most destructive disease to citrus plants in the world, is putatively caused in Asia and the Americas by the phloem-restricted gram-negative bacteria Candidatus Liberibacter asiaticus (CLas), vectored by the Asian citrus psyllid (ACP, Diaphorina citri, Hemiptera: Liviidae) [1,2]. Results showing that the CLso bacteria were present in various organs including the gut and the salivary gland, pointed to a systemic invasion of potato psyllids by CLso and supported a propagative, circulative mode of transmission [11]. D. citri guts, CLas accumulates inside Liberibacter containing vacuoles (LCVs), and that these vacuoles associate with the host cell rough endoplasmic reticulum (RER), suggesting that CLas can accumulate intracellularly in the psyllid cells. We used transmission electron microscopy (TEM) and immunogold labeling to study the ultrastructural morphology and localization of CLas, inside different organs and tissues of infected ACP. Our results point to the close cellular and subcellular association between CLas and its psyllid vector, and provide a strong support for a circulative-propagative mode of CLas transmission by ACP
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