Abstract
Plant parasitic cyst nematodes induce specific hypermetabolic syncytial nurse cell structures in host roots. A characteristic feature of syncytia is the lack of the central vacuole and the formation of numerous small and larger vesicles. We show that these structures are formed de novo via widening of ER cisternae during the entire development of syncytium, whereas in advanced stages of syncytium development, larger vacuoles are also formed via fusion of vesicles/tubules surrounding organelle-free pre-vacuole regions. Immunogold transmission electron microscopy of syncytia localised the vacuolar markers E subunit of vacuolar H+-adenosinetriphosphatase (V-ATPase) complex and tonoplast intrinsic protein (γ-TIP1;1) mostly in membranes surrounding syncytial vesicles, thus indicating that these structures are vacuoles and that some of them have a lytic character. To study the function of syncytial vacuoles, changes in expression of AtVHA-B1, AtVHA-B2 and AtVHA-B3 (coding for isoforms of subunit B of V-ATPase), and TIP1;1 and TIP1;2 (coding for γ-TIP proteins) genes were analysed. RT-qPCR revealed significant downregulation of AtVHA-B2, TIP1;1 and TIP1;2 at the examined stages of syncytium development compared to uninfected roots. Expression of VHA-B1 and VHA-B3 decreased at 3 dpi but reached the level of control at 7 dpi. These results were confirmed for TIP1;1 by monitoring At-γ-TIP-YFP reporter construct expression. Infection test conducted on tip1;1 mutant plants showed formation of larger syncytia and higher numbers of females in comparison to wild-type plants indicating that reduced levels or lack of TIP1;1 protein promote nematode development.
Highlights
Plant parasitic cyst-forming nematodes are obligate biotrophic parasites of a number of important crops such as potato (Solanum tuberosum), soybean (Glycine max), wheat (Triticum sp.) and beet (Beta vulgaris) throughout the world (Atkinson et al 2003)
With re-differentiation of the central vacuole, new small vacuoles/vesicles were formed de novo in the paramural regions of syncytial cytoplasm in elements located in the deeper regions of syncytia and close to nematode’s head (Fig. 1b, c)
We were unable to provide a detailed and univocal description of how the central vacuole is re-differentiated and whether this process occurs before incorporation of the ‘candidate’ cell into syncytium or after its incorporation
Summary
Plant parasitic cyst-forming nematodes are obligate biotrophic parasites of a number of important crops such as potato (Solanum tuberosum), soybean (Glycine max), wheat (Triticum sp.) and beet (Beta vulgaris) throughout the world (Atkinson et al 2003). Worldwide losses resulting from nematode infestations are estimated at 125 billion US$ per year (Chitwood 2003). Infective second-stage juveniles (J2) of the nematode induce the formation of a hyperplastic and hypermetabolic syncytium in the root vascular cylinder. Syncytium formation starts from a single cell and expands by successive integration of vascular cylinder cells via formation of local cell wall dissolutions (Grundler et al 1998; Ohtsu et al 2017). Characteristic features of syncytia are proliferation of cytoplasm and general increase in the number of organelles. Central vacuoles typical for differentiated parenchymatic vascular cylinder cells become replaced by a system of numerous vesicles of different sizes (Jones and Northcote 1972; Golinowski et al 1996; Sobczak et al 1997)
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