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A Parasitic Nematode Releases Cytokinin That Controls Cell Division and Orchestrates Feeding Site Formation in Host Plants

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A Parasitic Nematode Releases Cytokinin That Controls Cell Division and Orchestrates Feeding Site Formation in Host Plants A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants Shahid Siddiquea, Zoran S. Radakovica, Carola M. De La Torreb,1, Demosthenis Chronisb,1,2, Ondrej Novákc, Eswarayya Ramireddyd, Julia Holbeina, Christiane Materaa, Marion Hüttena, Philipp Gutbroda, Muhammad Shahzad Anjama, Elzbieta Rozanskae, Samer Habasha, Abdelnaser Elashrya, Miroslaw Sobczake, Tatsuo Kakimotof, Miroslav Strnadc, Thomas Schmüllingd, Melissa G. Mitchumb, and Florian M. W. Grundlera,3 aRheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany; bDivision of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO 65211; cLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University and Institute of Experimental Botany Academy of Sciences of the Czech Republic, CZ-78371 Olomouc, Czech Republic; dInstitute of Biology/Applied Genetics, Dahlem Centre of Plant Sciences, Freie Universität Berlin, D-14195 Berlin, Germany; eDepartment of Botany, Warsaw University of Life Sciences, PL-02787 Warsaw, Poland; and fDepartment of Biology, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0043, Japan Edited by Paul Schulze-Lefert, Max Planck Institute for Plant Breeding Research, Cologne, Germany, and approved August 26, 2015 (received for review February 21, 2015) Sedentary plant-parasitic cyst nematodes are biotrophs that cause the majority of juveniles develop into females. However, when the significant losses in agriculture. Parasitism is based on modifications juveniles are exposed to adverse conditions, as seen in resistant of host root cells that lead to the formation of a hypermetabolic plants, the percentage of males increases considerably. feeding site (a syncytium) from which nematodes withdraw nutri- The mechanism by which nematodes transform root cells into ents. The host cell cycle is activated in an initial cell selected by the highly active feeding sites is not clearly understood. One of the nematode for feeding, followed by activation of neighboring cells first events induced by both RKNs and cyst nematodes during and subsequent expansion of feeding site through fusion of hundreds feeding site development is cell cycle activation (2–5). The of cells. It is generally assumed that nematodes manipulate production feeding cells induced by RKNs hypertrophy and contain multiple and signaling of the plant hormone cytokinin to activate cell division. enlarged nuclei. The multinucleation occurs as a result of re- In fact, nematodes have been showntoproducecytokinininvitro; peated cycles of mitosis and endo-reduplication. In contrast, the however, whether the hormone is secreted into host plants and syncytium forms through the local dissolution of cell walls ac- plays a role in parasitism remained unknown. Here, we analyzed companied by the hypertrophy of incorporated cells and the di- the spatiotemporal activation of cytokinin signaling during in- vision of neighboring cells (2, 5). An expression analysis of key cell cycle genes and cell cycle inhibitors demonstrated that mi- teraction between the cyst nematode, Heterodera schachtii, and SCIENCES tosis is also essential for syncytium development (5). Arabidopsis using cytokinin-responsive promoter:reporter lines. AGRICULTURAL Cytokinin is an adenine derivative carrying an isoprenoid or Our results showed that cytokinin signaling is activated not only aromatic side chain that regulate numerous developmental and in the syncytium but also in neighboring cells to be incorporated into physiological responses in plants, including cell division, sink 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, Significance we identified a cytokinin-synthesizing isopentenyltransferase gene in H. schachtii and show that silencing of this gene in nematodes leads Sedentary plant-parasitic cyst nematodes are microscopic round- to a significant decrease in virulence due to a reduced expansion of worms that cause significant yield losses in agriculture. Successful feeding sites. Our findings demonstrate the ability of a plant-parasitic parasitism is based on the formation of a hypermetabolic feeding nematode to synthesize a functional plant hormone to manipulate site in host roots from which the nematodes withdraw their the host system and establish a long-term parasitic interaction. nutrients. The host cell cycle is activated at the site of infection and contributes to the formation of the syncytium. Here, we Arabidopsis thaliana | cell cycle | cytokinin | cyst nematode | IPT provide genetic evidence that nematode-derived cytokinin is in- volved in activating the host cell cycle during infection. Our findings show the ability of an animal to synthesize and secrete a lant-parasitic nematodes are a significant threat to almost all functional plant hormone to establish long-term parasitism. Peconomically important crops. International surveys revealed an average annual crop yield loss of more than 10% due to Author contributions: S.S., M.G.M., and F.M.W.G. designed research; S.S., Z.S.R., C.M.D.L.T., nematode infestation and up to 20% for certain crops, e.g., ba- D.C., O.N., J.H., C.M., M.H., P.G., M.S.A., E. Rozanska, S.H., A.E., M. Sobczak, T.K., M. Strnad, nanas (1). Most of this damage is caused by the sedentary root- and M.G.M. performed research; E. Ramireddy and T.S. contributed new reagents/analytic knot (Meloidogyne spp.) and cyst nematodes (Globodera spp. and tools; S.S., Z.S.R., C.M.D.L.T., D.C., O.N., A.E., M. Sobczak, M. Strnad, T.S., and M.G.M. ana- lyzed data; and S.S., M. Sobczak, T.S., M.G.M., and F.M.W.G. wrote the paper. Heterodera spp.). Infective second-stage juveniles (J2) of both root- The authors declare no conflict of interest. knot nematodes (RKNs) and cyst nematodes invade plant roots This article is a PNAS Direct Submission. near the tip and move toward the vascular cylinder. On reaching the vascular cylinder, RKNs induce the formation of several giant Freely available online through the PNAS open access option. cells, whereas cyst nematodes induce the formation of a syncytium. Data deposition: The sequences reported in this paper have been deposited in the Gen- ’ Bank database (accession nos. KT717690 and KT726964). These feeding sites serve as the nematode s sole source of nutrients 1C.M.D.L.T. and D.C. contributed equally to this work. throughout its life cycle for several weeks. Cyst nematodes are 2Present address: Department of Plant Pathology and Plant-Microbe Biology, Cornell dimorphic, but the mechanism of sex determination is not clearly University, Ithaca, NY 14853. understood. It has, nonetheless, been observed that the environ- 3To whom correspondence should be addressed. Email: [email protected]. ment strongly influences the outcome of the sex ratio in cyst This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. nematodes. Under favorable conditions with plenty of nutrients, 1073/pnas.1503657112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1503657112 PNAS | October 13, 2015 | vol. 112 | no. 41 | 12669–12674 Downloaded by guest on September 28, 2021 tissue establishment, root growth, branching, senescence, seed A GFP Merge germination, and stress responses (6, 7). Plants have two classes of isopentenyltransferase (IPT) enzymes that act on adenine: ATP/ADP-IPTs and tRNA-IPTs. In Arabidopsis, ATP/ADP-IPTs are encoded by seven genes (AtIPT1, AtIPT3, AtIPT4, AtIPT5, AtIPT6, AtIPT7,andAtIPT8) and contribute to the bulk of cyto- kinin synthesis. tRNA-IPTs are encoded by two genes (AtIPT2 and AtIPT9), and they are primarily responsible for producing the cZ-type cytokinin (8). Cytokinin signaling is mediated by a com- plex two-component system in which the signal is perceived by membrane-located histidine kinases (AHKs) and transmitted to the nucleus through a phosphorelay system via phospho- transmitter proteins. Inside the nucleus, transcription factors known as type B response regulators (ARRs) become activated and induce the transcription of cytokinin target genes. In Arabidopsis thaliana, cytokinin receptor kinases are encoded by three genes: AHK2, AHK3, and CRE1/AHK4. AHK4 is predominantly expressed in roots, whereas AHK2 and AHK3 are more abundant in above- ground plant parts (9–12). A few studies have explored the role of cytokinin in plant in- teractions with the RKN Meloidogyne incognita (13–15). However, the mechanism underlying their role is still not well understood. Nevertheless, because giant-cell formation involves the reentry of plant cells into the cell cycle, the role of cytokinin in this aspect of B the plant-nematode interaction has long been suspected. Similarly, the ability of cytokinin to mobilize nutrients and delay senescence led to the hypothesis that cytokinin may also be involved in the maintenance and function of nematode feeding sites as sinks (16, 17). It has also been speculated that nematodes produce cytokinin that might be injected into plants to establish parasitism (18). In contrast to RKNs, no studies have investigated the involvement of cytokinin in cyst nematode feeding site development. In the ahk2/3 ahk2/4 ahk3/4 present study, we investigated the contribution of cytokinin to Fig. 1. Activation of cytokinin signaling in Arabidopsis
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