As a reaction to a nematode infection, specific changes in the expression of plant cell wall enzymes occur within the NFS. However, whether these alterations are due to the innate immune response of the host or are caused by the pathogen itself is hard to distinguish. What are the triggers that cause these massive changes? It is known that nematodes use different ways to control the genetic machinery of the plant. They secrete effectors that can activate plant enzymes, as described in the previous section (Ding et al.1998; Hewezi et al.2008). Alternatively, they are able to change the hormonal balance, and they thereby potentially affect host hormone-responsive genes (Goverse et al. 2000; Karczmarek et al. 2004; Grunewald et al. 2008, Grunewald et al.2009a; Grunewald et al.2009b; Lee et al. 2011). On the other hand, assuming the plant senses nematodes via various receptors and gauges the integrity of its own wall, it can be predicted that at least a part of the changes is based on the host response. The above-mentioned activation of certain MAP kinases and their regulators during the early stages of syncytium development could certainly play an important role in this process (Hofmann, unpublished results).
During the nematode infection, these different triggers affect a vast number of different groups of cell wall–related genes, including genes involved in the biosyn- thesis, degradation, and remodeling of the cell wall. In several studies mostly based on gene chip analysis, changes in the expression of CesA and different classes of CSL genes were described (Ithal et al.2007b; Hudson2008; Szakasits et al.2009;
Barcala et al. 2009). It seems that the cellulose biosynthesis in giant cells and syncytia differs because most of the corresponding genes in RKN feeding sites were downregulated, whereas in CN-induced syncytia, they were mostly upregulated.
This is supported by the functional analysis of CesA mutants (CesA1-8), as the development of the RKN females on these plants was decreased (Hudson2008), while on selected CesA lines, there was a significant increase in the number of CN females (Wieczorek, unpublished results).
Early studies indicating that glucanases might be involved in the formation of the NFS were done on CN Globodera tabacumand RKN Meloidogyne incognita in tobacco roots (Goellner et al. 2001). Subsequently, further evidence came from studies using various other nematode species and different plants, including Arabidopsis (Sukno et al. 2006; Wang et al. 2007; Karczmarek et al. 2008;
Wieczorek et al.2008; Swiecicka et al.2009). In one of these reports, mutants of two endo-1,4-b-glucanases,kor3 and cel2, showed a reduction in the number of developing females by 45% and 48%, respectively (Wieczorek et al.2008). Further- more, there are examples of pectin-degrading and pectin-modifying enzymes of plant origin that are differentially expressed in the NFS, such as pectin acetylesterase (Vercauteren et al.2002), pectate lyases (Puthoff et al.2003, Jammes et al.2005;
Wieczorek, unpublished results), and polygalacturonases (Mahalingham et al.1999).
Finally, not only expansins secreted by the nematode play a role in the parasitism process, but also plant expansins are crucial for the development of the feeding site and the parasite. Apart from several microarray studies showing different expression of expansin isoforms (Jammes et al.2005; Bar-Or et al.2005; Gal et al.2006; Ithal et al.2007a,2007b, Puthoff et al.2007; Tucker et al.2007), expression of these cell wall–modifying proteins expressed in NFS has been investigated in more detail. It was shown that certainArabidopsisand tomato expansin isoforms are specifically expressed in syncytia induced by H. schachtii (Wieczorek et al. 2006) and G. rostochiensis (Fudali et al. 2008). In case of Arabidopsis, the study revealed that EXPA3 and EXPA16 are and are not present in other parts of the root. In tomato, it was shown that EXPA5 might be involved in the cell wall relaxation that supports the hypertrophy of the feeding site.
6 Summary
CWI signaling in yeast provides a paradigm that helps to envisage analogous pathways in plants. Being a presumably far more complex signaling network, only some components of plant cell wall performance and integrity control are presently known. However, genome-wide alterations in transcript levels of
enzymes related to cell wall biosynthesis and remodeling are hallmarks of activa- tion of this elusive signaling pathway. How cell wall performance and integrity control is involved in the interaction between host plants and sedentary plant- parasitic nematodes still remains largely unknown. However, there are first hints about the changes to the cell wall caused by infecting nematodes and which cell wall enzymes they secrete to facilitate the migration within the root tissue. Further- more, nematode effectors that are injected into the feeding site were found to interact with plant cell wall–remodeling enzymes. Many microarray studies provided information about how genes encoding plant cell wall–synthesizing, cell wall–degrading, and cell wall–remodeling enzymes as well as genes involved directly in the cell wall signaling process are affected by the nematode infection.
On the one hand, there are some suggestions how nematodes could trigger these massive changes in gene expression. On the other hand, knowledge about possible receptors and further signal transduction pathways is still very limited. Thus, there are still gaps in knowledge about the signaling role of the cell wall in the parasitic process of sedentary plant-parasitic nematodes, and therefore, more experimental work is needed to shed more light on this fascinating topic.
Acknowledgment The authors receive financial support of the Austrian Science Fund (FWF) grants P19778, P21782, and P21067.
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