Ultrastructure of compatible and incompatible interactions in phloem sieve elements during the stylet penetration by cotton aphids in melon

Abstract

Resistance of the melon line TGR-1551 to the aphid Aphis gossypii is based on preventing aphids from ingesting phloem sap. In electrical penetration graphs (EPGs), this resistance has been characterized with A. gossypii showing unusually long phloem salivation periods (waveform E1) mostly followed by pathway activities (waveform C) or if followed by phloem ingestion (waveform E2), ingestion was not sustained for more than 10 min. Stylectomy with aphids on susceptible and resistant plants was performed during EPG recording while the stylet tips were phloem inserted. This was followed by dissection of the penetrated leaf section, plant tissue fixation, resin embedding, and ultrathin sectioning for transmission electron microscopic observation in order to study the resistance mechanism in the TGR. The most obvious aspect appeared to be the coagulation of phloem proteins inside the stylet canals and the punctured sieve elements. Stylets of 5 aphids per genotype were amputated during sieve element (SE) salivation (E1) and SE ingestion (E2). Cross-sections of stylet bundles in susceptible melon plants showed that the contents of the stylet canals were totally clear and also, no coagulated phloem proteins occurred in their punctured sieve elements. In contrast, electron-dense coagulations were found in both locations in the resistant plants. Due to calcium binding, aphid saliva has been hypothesized to play an essential role in preventing/suppressing such coagulations that cause occlusion of sieves plate and in the food canal of the aphid's stylets. Doubts about this role of E1 salivation are discussed on the basis of our results.

Sieve element occlusion provides resistance against Aphis gossypii in TGR‐1551 melons

“…The presence of protein coagulation occluding sieve elements (this study) as well as in the food canal and around the maxillary stylet tips (Garzo et al ., ) when aphids fed on TGR‐1551 and the low frequency of occlusion when aphids fed on susceptible melon cultivars demonstrate that protein occlusion is associated with inhibition of phloem sap ingestion on TGR‐1551. The lanthanum experiments provide evidence that the relationship is causal, not merely correlative.…”

“…Examples of E1 appear in Tjallingii (, , ) and Garzo et al . (), and many other publications from Tjallingii and collaborators. These published examples are generally used as the standard for comparison when identifying E1 in EPG recordings, and in general are similar to the waveforms in the right half of Fig.…”

“…Additional support for this hypothesis was provided by Garzo et al . (). In that study, A. gossypii stylets were severed by stylectomy during phloem phase and the tissue was subjected to slow, gentle chemical fixation followed by examination with transmission electron microscopy.…”

“…Recently, Garzo et al . () found coagulations in the stylet food canal of A. gossypii feeding on TGR‐1551 and lumps of electron‐dense material around the maxillary stylet tips in the sieve element in contrast to clear food canals and sieve elements in aphids feeding on a susceptible melon variety. The main objectives of the present study were to (i) verify the results of Garzo et al .…”

Vector mediated transmission of Candidatus Liberibacter solanacearum and epidemiological consequences

“…Accordingly Lso is inoculated with the watery saliva secreted by the psyllid when the insect reaches the phloem sieve elements before any sap ingestion (Sandanayaka et al, 2014;Mustafa et al, 2015;Munyaneza et al, 2016). The reason why hemipteran insects salivate into the sieve elements before sap ingestion is not completely understood but previous publications have suggested that components in the secreted saliva help to suppress wound responses triggered by the stylet penetration process into the plant (Tjallingii, 2006;Garzo et al, 2017). It is very likely that this feeding behaviour has favored the evolution of phloem restricted pathogens transmitted in a propagative-circulative manner (Perilla-Henao and Casteel, 2016).…”