Arabinogalactan Proteins in the Digestive Glands of Dionaea muscipula J.Ellis Traps

Abstract

The arabinogalactan proteins (AGP) play important roles in plant growth and developmental processes. However, to the best of our knowledge, there is no information on the spatial distribution of AGP in the plant organs and tissues of carnivorous plants during their carnivorous cycle. The Dionaea muscipula trap forms an “external stomach” and is equipped with an effective digestive-absorbing system. Because its digestive glands are composed of specialized cells, the hypothesis that their cell walls are also very specialized in terms of their composition (AGP) compared to the cell wall of the trap epidermal and parenchyma cells was tested. Another aim of this study was to determine whether there is a spatio-temporal distribution of the AGP in the digestive glands during the secretory cycle of D. muscipula. Antibodies that act against AGPs, including JIM8, JIM13 and JIM14, were used. The localization of the examined compounds was determined using immunohistochemistry techniques and immunogold labeling. In both the un-fed and fed traps, there was an accumulation of AGP in the cell walls of the gland secretory cells. The epitope, which is recognized by JIM14, was a useful marker of the digestive glands. The secretory cells of the D. muscipula digestive glands are transfer cells and an accumulation of specific AGP was at the site where the cell wall labyrinth occurred. Immunogold labeling confirmed an occurrence of AGP in the cell wall ingrowths. There were differences in the AGP occurrence (labeled with JIM8 and JIM13) in the cell walls of the gland secretory cells between the unfed and fed traps.

Immunocytochemical Analysis of the Wall Ingrowths in the Digestive Gland Transfer Cells in Aldrovanda vesiculosa L. (Droseraceae)

“…We showed that the cell wall ingrowths in the transfer cells of A. vesiculosa glands were rich in AGPs. The wall ingrowths were similar in their AGP composition (JIM8, JIM13, JIM14) to the wall ingrowths in the transfer cells of D. muscipula digestive glands [ 18 ]. It was shown that the epitope recognized by JIM14 was a useful marker of the digestive glands of D. muscipula .…”

“…In both D. muscipula and A. vesiculosa , the cell wall ingrowths in the gland cells were rich in AGPs in mature traps. It is known that AGPs play various roles in plants: developmental processes, calcium capacitor, signaling, response to biotic and abiotic stress, and sexual reproduction [ 18 , 63 , 64 , 65 , 66 , 67 , 68 ]. In Dionaea muscipula , we found differences in the occurrence of AGPs (labeled with JIM8 and JIM13) in the walls of gland secretory cells between unfed and fed traps.…”

“…Schulze et al [ 70 ] and Bemm et al [ 71 ] proposed that Dionaea uses stress pathway-related processes to form an active digestive system. Hence, Płachno et al [ 18 ] suggested that this could explain the accumulation of AGPs in the digestive glands, especially given the evidence for AGP overproduction under stress [ 64 ]. A similar mechanism may operate in the A. vesiculosa digestive glands and in other carnivorous plant species; however, more research is needed.…”

“…A common characteristic of glandular cells of carnivorous plant digestive glands is the occurrence of cell wall ingrowths; hence, these cells are transfer cells [Juniper et al 1989]. Glandular transfer cells have been detected in the digestive gland of species from nonrelated families of carnivorous plants e.g., in Droseraceae [ 13 , 14 , 15 , 16 , 17 , 18 ] and Lentibularaceae [ 19 , 20 , 21 ]. The transfer cells are characterized by the occurrence of secondary wall ingrowths, which are scaffolds for an amplified surface area of plasma membrane rich in nutrient transporters [ 22 , 23 , 24 , 25 ].…”

“…We proposed carnivorous plants as an excellent model for studies of wall ingrowths/transfer cells. In our previous paper [ 18 ], we showed the presence of arabinogalactan proteins (AGPs) in cell wall ingrowths in the digestive glands of Dionaea muscipula J.Ellis. The genus Aldrovanda (with one recent species Aldrovanda vesiculosa L., waterwheel plant) is a sister genus to D. muscipula , and both produce the snapping traps for catching small invertebrates [ 1 , 46 , 47 , 48 , 49 , 50 ].…”