title: 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.
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany;
authors.forename: Shahid
authors.initials: S
authors.lastname: Siddique
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany;
authors.forename: Zoran S
authors.initials: ZS
authors.lastname: Radakovic
authors.affiliation: Division of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO 65211;
authors.forename: Carola M
authors.initials: CM
authors.lastname: De La Torre
authors.affiliation: Division of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO 65211;
authors.forename: Demosthenis
authors.initials: D
authors.lastname: Chronis
authors.affiliation: Laboratory 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;
authors.forename: Ondřej
authors.identifier: http://orcid.org/0000-0003-3452-0154
authors.initials: O
authors.lastname: Novák
authors.affiliation: Institute of Biology/Applied Genetics, Dahlem Centre of Plant Sciences, Freie Universität Berlin, D-14195 Berlin, Germany;
authors.forename: Eswarayya
authors.initials: E
authors.lastname: Ramireddy
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany;
authors.forename: Julia
authors.initials: J
authors.lastname: Holbein
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany;
authors.forename: Christiane
authors.initials: C
authors.lastname: Matera
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany;
authors.forename: Marion
authors.initials: M
authors.lastname: Hütten
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany;
authors.forename: Philipp
authors.initials: P
authors.lastname: Gutbrod
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany;
authors.forename: Muhammad Shahzad
authors.initials: MS
authors.lastname: Anjam
authors.affiliation: Department of Botany, Warsaw University of Life Sciences, PL-02787 Warsaw, Poland;
authors.forename: Elzbieta
authors.initials: E
authors.lastname: Rozanska
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany;
authors.forename: Samer
authors.initials: S
authors.lastname: Habash
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany;
authors.forename: Abdelnaser
authors.initials: A
authors.lastname: Elashry
authors.affiliation: Department of Botany, Warsaw University of Life Sciences, PL-02787 Warsaw, Poland;
authors.forename: Miroslaw
authors.initials: M
authors.lastname: Sobczak
authors.affiliation: Department of Biology, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0043, Japan.
authors.forename: Tatsuo
authors.initials: T
authors.lastname: Kakimoto
authors.affiliation: Laboratory 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;
authors.forename: Miroslav
authors.initials: M
authors.lastname: Strnad
authors.affiliation: Institute of Biology/Applied Genetics, Dahlem Centre of Plant Sciences, Freie Universität Berlin, D-14195 Berlin, Germany;
authors.forename: Thomas
authors.initials: T
authors.lastname: Schmülling
authors.affiliation: Division of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO 65211;
authors.forename: Melissa G
authors.initials: MG
authors.lastname: Mitchum
authors.affiliation: Rheinische Friedrich-Wilhelms-University of Bonn, Department of Molecular Phytomedicine, D-53115 Bonn, Germany; grundler@uni-bonn.de.
authors.forename: Florian M W
authors.initials: FM
authors.lastname: Grundler
mesh_terms: D000818:Animals; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism / Q000469:parasitology; D001483:Base Sequence; D003583:Cytokinins / Q000235:genetics / Q000378:metabolism*; D006790:Host-Parasite Interactions / Q000502:physiology*; D008969:Molecular Sequence Data; D009348:Nematoda / Q000502:physiology*; D010935:Plant Diseases / Q000469:parasitology*; D015398:Signal Transduction
chemical_list: D003583:Cytokinins
keywords: Arabidopsis thaliana; IPT; cell cycle; cyst nematode; cytokinin