Gaming the system: how hungry nematodes get plants to produce feeding sites for them.

A hungry little sugar beet nematode (Heterodera schachtii) slithers in the soil looking for food. The only way it can eat is to force its way into the root of a nearby susceptible plant (such as Arabidopsis thaliana) and coax it into forming a syncytium. This enlarged, multinucleate feeding site is formed by the fusion of several hundred root cells, which undergo massive changes in cellular machinery and vascular transport to accommodate the little parasite. How does the nematode get the plant to do all this? It starts by secreting effectors into the host cell (most likely in the cytoplasm). By manipulating the host nuclear transport machinery, these effectors are able to localize to the nucleus and perhaps to other cellular compartments as well (Hewezi and Baum, 2013). One way this may take place is through host-mediated posttranslational modification of the effectors, a process that occurs in some bacterial pathogenic systems (e.g., Coaker et al., 2005). Thus, the host plant is somehow tricked into modifying the nematode’s effectors, allowing them to reach the nucleus, where they subvert essential cellular functioning in favor of the hungry parasite. How this process may occur is the subject of a fascinating study by Hewezi et al. (2015). The authors began their investigation by identifying an H. schachtii homolog of 10A07, an effector gene from soybean cyst nematode (Heterodera glycines), and confirming its expression during H. schachtii development. A fusion protein containing a region of 10A07 harboring a putative nuclear localization signal fused to green fluorescent protein localized exclusively to the nuclei of transiently transfected onion (Allium cepa) epidermal cells. Expression of high levels of 10A07 in Arabidopsis produced plants with dramatically stunted growth and hypersusceptibility to nematodes, demonstrating the potency of this effector. Yeast two-hybrid analysis and bimolecular fluorescence complementation assays revealed that interacting protein kinase (IPK) and the auxin-responsive transcription factor INDOLE-3-ACETIC ACID INDUCIBLE16 (IAA16) strongly interact (and colocalize) with 10A07. Moreover, the promoters of both IPK and IAA16 were strongly upregulated in nematode-induced syncytia (see figure), where the 10A07 effector is presumably delivered by the nematode, strongly suggesting that 10A07 indeed interacts with IPK and IAA16 during nematode infection. The authors then went on to investigate the nature of this interaction. Based on the inherent activity of IPK, they reasoned that posttranslational modification of the effector involves phosphorylation, which they confirmed to be the case. Indeed, only phosphorylated 10A07 localized to the nucleus in onion epidermal cell assays. Once in the nucleus, 10A07 encounters and binds to the transcription factor IAA16. What role does IAA16 play in syncytium formation? Arabidopsis plants overexpressing IAA16 or IPK exhibited increased susceptibility to H. schachtii, while cosilencing of these genes resulted in reduced susceptibility. It appears that when 10A07 binds to IAA16, it interferes with auxin signaling in the plant; in transgenic Arabidopsis plants overexpressing 10A07 or IAA16, auxin response factor (ARF) genes were downregulated, but they were upregulated upon nematode parasitism. These findings suggest that the nematode co-opts IAA16 to alter the expression of specific ARFs, which in turn redirects the transcriptional programs of specific downstream auxin-responsive genes, leading to profound physiological and developmental changes that benefit the hungry nematode.