title: Effector-Triggered Immunity Determines Host Genotype-Specific Incompatibility in Legume-Rhizobium Symbiosis.
abstract: Symbiosis between legumes and rhizobia leads to the formation of N2-fixing root nodules. In soybean, several host genes, referred to as Rj genes, control nodulation. Soybean cultivars carrying the Rj4 gene restrict nodulation by specific rhizobia such as Bradyrhizobium elkanii We previously reported that the restriction of nodulation was caused by B. elkanii possessing a functional type III secretion system (T3SS), which is known for its delivery of virulence factors by pathogenic bacteria. In the present study, we investigated the molecular basis for the T3SS-dependent nodulation restriction in Rj4 soybean. Inoculation tests revealed that soybean cultivar BARC-2 (Rj4/Rj4) restricted nodulation by B. elkanii USDA61, whereas its nearly isogenic line BARC-3 (rj4/rj4) formed nitrogen-fixing nodules with the same strain. Root-hair curling and infection threads were not observed in the roots of BARC-2 inoculated with USDA61, indicating that Rj4 blocked B. elkanii infection in the early stages. Accumulation of H2O2 and salicylic acid (SA) was observed in the roots of BARC-2 inoculated with USDA61. Transcriptome analyses revealed that inoculation of USDA61, but not its T3SS mutant in BARC-2, induced defense-related genes, including those coding for hypersensitive-induced responsive protein, which act in effector-triggered immunity (ETI) in Arabidopsis. These findings suggest that B. elkanii T3SS triggers the SA-mediated ETI-type response in Rj4 soybean, which consequently blocks symbiotic interactions. This study revealed a common molecular mechanism underlying both plant-pathogen and plant-symbiont interactions, and suggests that establishment of a root nodule symbiosis requires the evasion or suppression of plant immune responses triggered by rhizobial effectors.
authors.affiliation: International Environmental and Agricultural Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509 Japan.
authors.forename: Michiko
authors.initials: M
authors.lastname: Yasuda
authors.affiliation: International Environmental and Agricultural Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509 Japan.
authors.forename: Hiroki
authors.initials: H
authors.lastname: Miwa
authors.affiliation: International Environmental and Agricultural Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509 Japan.
authors.forename: Sachiko
authors.initials: S
authors.lastname: Masuda
authors.affiliation: Plant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science 1-7-22, Suehiro, Tsurumi, Yokohama, 230-0045 Japan.
authors.forename: Yumiko
authors.initials: Y
authors.lastname: Takebayashi
authors.affiliation: Plant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science 1-7-22, Suehiro, Tsurumi, Yokohama, 230-0045 Japan.
authors.forename: Hitoshi
authors.initials: H
authors.lastname: Sakakibara
authors.affiliation: International Environmental and Agricultural Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509 Japan sokazaki@cc.tuat.ac.jp.
authors.forename: Shin
authors.initials: S
authors.lastname: Okazaki
mesh_terms: D020369:Bradyrhizobium / Q000166:cytology / Q000235:genetics / Q000502:physiology*; D015536:Down-Regulation; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D005838:Genotype; D006861:Hydrogen Peroxide / Q000378:metabolism; D020411:Oligonucleotide Array Sequence Analysis; D010937:Plant Growth Regulators / Q000378:metabolism*; D057865:Plant Immunity; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D055170:Plant Root Nodulation; D018517:Plant Roots / Q000166:cytology / Q000235:genetics / Q000382:microbiology / Q000502:physiology; D013025:Glycine max / Q000166:cytology / Q000235:genetics* / Q000382:microbiology / Q000502:physiology; D013559:Symbiosis / Q000235:genetics / Q000276:immunology*; D059467:Transcriptome; D000069296:Type III Secretion Systems; D015854:Up-Regulation
chemical_list: D010937:Plant Growth Regulators; D010940:Plant Proteins; D000069296:Type III Secretion Systems; D006861:Hydrogen Peroxide
keywords: Defense signaling; Effector-triggered immunity; Nodulation; Soybean; Symbiosis; Type III secretion system