Sucrose supply to nematode-induced syncytia depends on the apoplasmic and symplasmic pathways

Abstract

The plant parasitic nematode Heterodera schachtii induces syncytial feeding structures in the roots of host plants. Nematode-induced syncytia become strong sink tissues in the plant solute circulation system as the parasites start withdrawing nutrients. In the present work, the expression pattern of the phloem-specific sucrose transporter AtSUC4 (also described as AtSUT4) is analysed in syncytia induced by H. schachtii and it is compared with that of AtSUC2, another phloem-specific sucrose transporter, which is expressed in syncytia. The temporal expression pattern was monitored by GUS-tests and real-time RT-PCR, while the localization within the syncytia was performed using in situ RT-PCR. In this context, the concentration of sucrose in infection sites was also analysed and, in fact, an increase in response to syncytium development was found. Silencing of the AtSUC4 gene finally resulted in a significant reduction of female nematode development, thus demonstrating a function for this gene for the first time. It is therefore concluded that AtSUC4 plays a significant role in the early phase of syncytium differentiation when functional plasmodesmata to the phloem are not yet established. It is further concluded that, during syncytium establishment, transporters are responsible for sucrose supply and, at a later stage, when a connection to the phloem is established via plasmodesmata, transporters are required for sucrose retrieval.

Starch Serves as Carbohydrate Storage in Nematode-Induced Syncytia

“…Assuming soluble carbohydrates are an essential source of energy, syncytial feeding sites have to contain high levels of sugars that can be taken up by the nematodes. In fact, this has been shown recently (Hofmann et al, 2007). On the other hand, it is improbable that sugar transport into syncytia is entirely adapted to the temporal and quantitative demand of the parasites.…”

“…At first sight, it seems astonishing that it is synthesized in syncytia, which serve as the exclusive nutrient source of the feeding nematodes. In fact, a massive transfer of sugars from the host plant's phloem into syncytia occurs, which leads to the necessary high levels of sugars (Hofmann et al, 2007). Sugar import has been shown to be performed via transporters at the beginning of syncytium formation and via plasmodesmata at later stages (starting around 10 dai; Juergensen et al, 2003;Hoth et al, 2005;Grundler, 2006, 2007a;Hofmann et al, 2007).…”

“…Changes were obtained by comparing 5-, 15-, and 21-d-old micro-aspirated syncytial protoplasts in relation to control roots (con) and displayed as fold change (log 2 ratios; n 5 4 for 5 dai, n 5 3 for 15 dai, n 5 2 for 21 dai, n 5 4 for con). Asterisks indicate significance differences determined by a Benjamini-Hochberg multiple testing correction (* 5 q , 10%; ** 5 q , 5%; see ''Materials and Methods'' for details leading to an excess of sugar in syncytia (Hofmann et al, 2007). In this way, a situation occurs in which starch synthesis is induced as a common response of the plant cells.…”

“…The formation of feeding sites is accompanied by a massive solute import into syncytia, leading to highly elevated Suc levels and, thus, to high osmotic pressure (Bö ckenhoff, 1995;Hofmann et al, 2007). In general, plant cells cope with excessive amounts of sugars by the formation of starch that accumulates in plastids as water-insoluble granules.…”

Differential vascularization of nematode-induced feeding sites

“…After loading of [ 14 C]-sucrose to source leaves of Arabidopsis, radioactive signals could be monitored along the roots, within syncytia, and in the associated nematodes (8). It was postulated that sucrose transporters are responsible for this accumulation (9,10). However, despite of the presence of transcripts for these transporters in syncytia, the proteins were not detected (11).…”