title: Nodule Inception creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production.
abstract: Autoregulatory negative-feedback loops play important roles in fine-balancing tissue and organ development. Such loops are composed of short-range intercellular signaling pathways via cell-cell communications. On the other hand, leguminous plants use a long-distance negative-feedback system involving root-shoot communication to control the number of root nodules, root lateral organs that harbor symbiotic nitrogen-fixing bacteria known as rhizobia. This feedback system, known as autoregulation of nodulation (AON), consists of two long-distance mobile signals: root-derived and shoot-derived signals. Two Lotus japonicus CLAVATA3/endosperm surrounding region (CLE)-related small peptides, CLE root signal1 (CLE-RS1) and CLE-RS2, function as root-derived signals and are perceived by a shoot-acting AON factor, the hypernodulation aberrant root formation1 (HAR1) receptor protein, an ortholog of Arabidopsis CLAVATA1, which is responsible for shoot apical meristem homeostasis. This peptide-receptor interaction is necessary for systemic suppression of nodulation. How the onset of nodulation activates AON and how optimal nodule numbers are maintained remain unknown, however. Here we show that an RWP-RK-containing transcription factor, nodule inception (NIN), which induces nodule-like structures without rhizobial infection when expressed ectopically, directly targets CLE-RS1 and CLE-RS2. Roots constitutively expressing NIN systemically repress activation of endogenous NIN expression in untransformed roots of the same plant in a HAR1-dependent manner, leading to systemic suppression of nodulation and down-regulation of CLE expression. Our findings provide, to our knowledge, the first molecular evidence of a long-distance autoregulatory negative-feedback loop that homeostatically regulates nodule organ formation.
authors.affiliation: National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan; National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan;
authors.forename: Takashi
authors.initials: T
authors.lastname: Soyano
authors.affiliation: Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan; and.
authors.forename: Hideki
authors.initials: H
authors.lastname: Hirakawa
authors.affiliation: Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan; and Graduate School of Life Sciences, Tohoku University, Aoba-ku, Sendai 980-8577, Japan.
authors.forename: Shusei
authors.initials: S
authors.lastname: Sato
authors.affiliation: National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan; makotoh@affrc.go.jp masayosi@nibb.ac.jp.
authors.forename: Makoto
authors.initials: M
authors.lastname: Hayashi
authors.affiliation: National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan; makotoh@affrc.go.jp masayosi@nibb.ac.jp.
authors.forename: Masayoshi
authors.initials: M
authors.lastname: Kawaguchi
mesh_terms: D025461:Feedback, Physiological; D018506:Gene Expression Regulation, Plant; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D054884:Host-Pathogen Interactions; D000070116:Lotus / Q000235:genetics / Q000382:microbiology; D009154:Mutation; D010940:Plant Proteins / Q000235:genetics*; D055170:Plant Root Nodulation / Q000235:genetics*; D018517:Plant Roots / Q000235:genetics / Q000382:microbiology; D018520:Plant Shoots / Q000235:genetics / Q000382:microbiology; D030821:Plants, Genetically Modified; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012231:Rhizobium / Q000502:physiology; D053204:Root Nodules, Plant / Q000235:genetics* / Q000382:microbiology; D015398:Signal Transduction / Q000235:genetics*; D013559:Symbiosis
chemical_list: D010940:Plant Proteins; D049452:Green Fluorescent Proteins