A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants

Abstract

Sedentary plant-parasitic cyst nematodes are biotrophs that cause significant losses in agriculture. Parasitism is based on modifications of host root cells that lead to the formation of a hypermetabolic feeding site (a syncytium) from which nematodes withdraw nutrients. The host cell cycle is activated in an initial cell selected by the nematode for feeding, followed by activation of neighboring cells and subsequent expansion of feeding site through fusion of hundreds of cells. It is generally assumed that nematodes manipulate production and signaling of the plant hormone cytokinin to activate cell division. In fact, nematodes have been shown to produce cytokinin in vitro; however, whether the hormone is secreted into host plants and plays a role in parasitism remained unknown. Here, we analyzed the spatiotemporal activation of cytokinin signaling during interaction between the cyst nematode, Heterodera schachtii, and Arabidopsis using cytokinin-responsive promoter:reporter lines. Our results showed that cytokinin signaling is activated not only in the syncytium but also in neighboring cells to be incorporated into syncytium. An analysis of nematode infection on mutants that are deficient in cytokinin or cytokinin signaling revealed a significant decrease in susceptibility of these plants to nematodes. Further, we identified a cytokinin-synthesizing isopentenyltransferase gene in H. schachtii and show that silencing of this gene in nematodes leads to a significant decrease in virulence due to a reduced expansion of feeding sites. Our findings demonstrate the ability of a plant-parasitic nematode to synthesize a functional plant hormone to manipulate the host system and establish a long-term parasitic interaction.Arabidopsis thaliana | cell cycle | cytokinin | cyst nematode | IPT P lant-parasitic nematodes are a significant threat to almost all economically important crops. International surveys revealed an average annual crop yield loss of more than 10% due to nematode infestation and up to 20% for certain crops, e.g., bananas (1). Most of this damage is caused by the sedentary rootknot (Meloidogyne spp.) and cyst nematodes (Globodera spp. and Heterodera spp.). Infective second-stage juveniles (J2) of both rootknot nematodes (RKNs) and cyst nematodes invade plant roots near the tip and move toward the vascular cylinder. On reaching the vascular cylinder, RKNs induce the formation of several giant cells, whereas cyst nematodes induce the formation of a syncytium. These feeding sites serve as the nematode's sole source of nutrients throughout its life cycle for several weeks. Cyst nematodes are dimorphic, but the mechanism of sex determination is not clearly understood. It has, nonetheless, been observed that the environment strongly influences the outcome of the sex ratio in cyst nematodes. Under favorable conditions with plenty of nutrients, the majority of juveniles develop into females. However, when the juveniles are exposed to adverse conditions, as seen in resistant plants, the percentage of males increase...

Interspecies hormonal control of host root morphology by parasitic plants

“…Well-known plant pathogens that induce cytokinin production include the crown gall-inducing bacterium Agrobacterium tumefaciens (6), the fungal rice blast pathogen Magnaporthe oryzae (7), and phytopathogenic nematodes such as Heterodera schachtii (8). Interspecies cytokinin transport thus may be a widely used mechanism for infectivity, and in parasitic plants, we suggest a scenario whereby multiple transport routes at the haustorium contribute to the bidirectional transfer of molecules that affects both host and parasite physiology.…”

“…In addition to water and nutrients, other small substances are transferred across haustoria, including RNAs and proteins (3)(4)(5), but the biological relevance for this movement is not clear. Beyond parasitic plants, various plant-pathogenic microbes, insects, and nematodes produce compounds that move into the host and contribute to their virulence, including the plant hormone cytokinin (6)(7)(8).…”

Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes

“…The infection assays with cyst nematodes were performed as previously described [41]. Briefly, 60–70 J2s of H .…”

Plant hormones: a fungal point of view

“…As the tRNA‐IPT gene identified in M. oryzae is well conserved, this mutation could be studied in other fungi as a potential tool to distinguish fungal CKs from plant CKs in other plant–fungus interactions. Recently, the deletion of a tRNA‐IPT gene has also been performed in the nematode H. schachtii , confirming the conservation of the role of this enzyme in CK production among different organisms (Siddique et al ., ).…”