##### PUB RECORD ##### ## 10.1073/pnas.1412716111 25246578 Soyano, Hirakawa et al., 2014 "Soyano T, Hirakawa H, Sato S, Hayashi M, Kawaguchi M. Nodule Inception creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14607-12. doi: 10.1073/pnas.1412716111. Epub 2014 Sep 22. PMID: 25246578; PMCID: PMC4210044." ## PMID- 25246578 OWN - NLM STAT- MEDLINE DCOM- 20150430 LR - 20211021 IS - 1091-6490 (Electronic) IS - 0027-8424 (Print) IS - 0027-8424 (Linking) VI - 111 IP - 40 DP - 2014 Oct 7 TI - Nodule Inception creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. PG - 14607-12 LID - 10.1073/pnas.1412716111 [doi] AB - 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. FAU - Soyano, Takashi AU - Soyano T AD - National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan; National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan; FAU - Hirakawa, Hideki AU - Hirakawa H AD - Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan; and. FAU - Sato, Shusei AU - Sato S AD - Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan; and Graduate School of Life Sciences, Tohoku University, Aoba-ku, Sendai 980-8577, Japan. FAU - Hayashi, Makoto AU - Hayashi M AD - National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan; makotoh@affrc.go.jp masayosi@nibb.ac.jp. FAU - Kawaguchi, Masayoshi AU - Kawaguchi M AD - National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan; makotoh@affrc.go.jp masayosi@nibb.ac.jp. LA - eng PT - Journal Article PT - Research Support, Non-U.S. Gov't DEP - 20140922 PL - United States TA - Proc Natl Acad Sci U S A JT - Proceedings of the National Academy of Sciences of the United States of America JID - 7505876 RN - 0 (Plant Proteins) RN - 147336-22-9 (Green Fluorescent Proteins) SB - IM MH - Feedback, Physiological MH - Gene Expression Regulation, Plant MH - Green Fluorescent Proteins/genetics/metabolism MH - Host-Pathogen Interactions MH - Lotus/genetics/microbiology MH - Mutation MH - Plant Proteins/*genetics MH - Plant Root Nodulation/*genetics MH - Plant Roots/genetics/microbiology MH - Plant Shoots/genetics/microbiology MH - Plants, Genetically Modified MH - Reverse Transcriptase Polymerase Chain Reaction MH - Rhizobium/physiology MH - Root Nodules, Plant/*genetics/microbiology MH - Signal Transduction/*genetics MH - Symbiosis PMC - PMC4210044 COIS- The authors declare no conflict of interest. EDAT- 2014/09/24 06:00 MHDA- 2015/05/01 06:00 PMCR- 2015/04/07 CRDT- 2014/09/24 06:00 PHST- 2014/09/24 06:00 [entrez] PHST- 2014/09/24 06:00 [pubmed] PHST- 2015/05/01 06:00 [medline] PHST- 2015/04/07 00:00 [pmc-release] AID - 1412716111 [pii] AID - 201412716 [pii] AID - 10.1073/pnas.1412716111 [doi] PST - ppublish SO - Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14607-12. doi: 10.1073/pnas.1412716111. Epub 2014 Sep 22. ##### PUB RECORD ##### ## 10.1093/plcell/koab103 33826745 Nishida, Nosaki et al., 2021 "Nishida H, Nosaki S, Suzuki T, Ito M, Miyakawa T, Nomoto M, Tada Y, Miura K, Tanokura M, Kawaguchi M, Suzaki T. Different DNA-binding specificities of NLP and NIN transcription factors underlie nitrate-induced control of root nodulation. Plant Cell. 2021 Aug 13;33(7):2340-2359. doi: 10.1093/plcell/koab103. PMID: 33826745; PMCID: PMC8364233." ## PMID- 33826745 OWN - NLM STAT- MEDLINE DCOM- 20211227 LR - 20220503 IS - 1532-298X (Electronic) IS - 1040-4651 (Print) IS - 1040-4651 (Linking) VI - 33 IP - 7 DP - 2021 Aug 13 TI - Different DNA-binding specificities of NLP and NIN transcription factors underlie nitrate-induced control of root nodulation. PG - 2340-2359 LID - 10.1093/plcell/koab103 [doi] AB - Leguminous plants produce nodules for nitrogen fixation; however, nodule production incurs an energy cost. Therefore, as an adaptive strategy, leguminous plants halt root nodule development when sufficient amounts of nitrogen nutrients, such as nitrate, are present in the environment. Although legume NODULE INCEPTION (NIN)-LIKE PROTEIN (NLP) transcription factors have recently been identified, understanding how nodulation is controlled by nitrate, a fundamental question for nitrate-mediated transcriptional regulation of symbiotic genes, remains elusive. Here, we show that two Lotus japonicus NLPs, NITRATE UNRESPONSIVE SYMBIOSIS 1 (NRSYM1)/LjNLP4 and NRSYM2/LjNLP1, have overlapping functions in the nitrate-induced control of nodulation and act as master regulators for nitrate-dependent gene expression. We further identify candidate target genes of LjNLP4 by combining transcriptome analysis with a DNA affinity purification-seq approach. We then demonstrate that LjNLP4 and LjNIN, a key nodulation-specific regulator and paralog of LjNLP4, have different DNA-binding specificities. Moreover, LjNLP4-LjNIN dimerization underlies LjNLP4-mediated bifunctional transcriptional regulation. These data provide a basic principle for how nitrate controls nodulation through positive and negative regulation of symbiotic genes. CI - (c) The Author(s) 2021. Published by Oxford University Press on behalf of American Society of Plant Biologists. FAU - Nishida, Hanna AU - Nishida H AUID- ORCID: 0000-0003-3701-4011 AD - Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan. FAU - Nosaki, Shohei AU - Nosaki S AUID- ORCID: 0000-0001-8493-1299 AD - Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan. AD - Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan. AD - Tsukuba Plant-Innovation Research Center, University of Tsukuba, Tsukuba, Ibaraki, Japan. FAU - Suzuki, Takamasa AU - Suzuki T AUID- ORCID: 0000-0002-1977-0510 AD - College of Bioscience and Biotechnology, Chubu University, Kasugai, Aichi, Japan. FAU - Ito, Momoyo AU - Ito M AUID- ORCID: 0000-0003-2704-9034 AD - Tsukuba Plant-Innovation Research Center, University of Tsukuba, Tsukuba, Ibaraki, Japan. FAU - Miyakawa, Takuya AU - Miyakawa T AUID- ORCID: 0000-0001-5957-3549 AD - Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan. FAU - Nomoto, Mika AU - Nomoto M AUID- ORCID: 0000-0002-0544-2321 AD - Center for Gene Research, Nagoya University, Nagoya, Aichi, Japan. FAU - Tada, Yasuomi AU - Tada Y AUID- ORCID: 0000-0001-9900-069X AD - Center for Gene Research, Nagoya University, Nagoya, Aichi, Japan. FAU - Miura, Kenji AU - Miura K AUID- ORCID: 0000-0003-1262-2176 AD - Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan. AD - Tsukuba Plant-Innovation Research Center, University of Tsukuba, Tsukuba, Ibaraki, Japan. FAU - Tanokura, Masaru AU - Tanokura M AUID- ORCID: 0000-0001-5072-2480 AD - Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan. FAU - Kawaguchi, Masayoshi AU - Kawaguchi M AUID- ORCID: 0000-0002-1032-6261 AD - National Institute for Basic Biology, Okazaki, Aichi, Japan. AD - School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi, Japan. FAU - Suzaki, Takuya AU - Suzaki T AUID- ORCID: 0000-0001-9646-0279 AD - Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan. AD - Tsukuba Plant-Innovation Research Center, University of Tsukuba, Tsukuba, Ibaraki, Japan. LA - eng PT - Journal Article PT - Research Support, Non-U.S. Gov't PL - England TA - Plant Cell JT - The Plant cell JID - 9208688 RN - 0 (Plant Proteins) RN - 0 (Transcription Factors) SB - IM CIN - Plant Cell. 2021 Aug 13;33(7):2101-2103. doi: 10.1093/plcell/koab108. PMID: 35233600 MH - Gene Expression Regulation, Plant MH - Lotus/genetics/metabolism MH - Plant Proteins/genetics/metabolism MH - Plant Root Nodulation/genetics/physiology MH - Root Nodules, Plant/genetics/metabolism MH - Symbiosis/genetics/physiology MH - Transcription Factors/genetics/*metabolism PMC - PMC8364233 EDAT- 2021/04/08 06:00 MHDA- 2021/12/28 06:00 PMCR- 2021/04/07 CRDT- 2021/04/07 17:33 PHST- 2020/09/08 00:00 [received] PHST- 2021/04/03 00:00 [accepted] PHST- 2021/04/08 06:00 [pubmed] PHST- 2021/12/28 06:00 [medline] PHST- 2021/04/07 17:33 [entrez] PHST- 2021/04/07 00:00 [pmc-release] AID - 6214494 [pii] AID - koab103 [pii] AID - 10.1093/plcell/koab103 [doi] PST - ppublish SO - Plant Cell. 2021 Aug 13;33(7):2340-2359. doi: 10.1093/plcell/koab103. ##### PUB RECORD ##### ## 10.1093/pcp/pcu168 25416287 Soyano, Shimoda et al., 2015 "Soyano T, Shimoda Y, Hayashi M. NODULE INCEPTION antagonistically regulates gene expression with nitrate in Lotus japonicus. Plant Cell Physiol. 2015 Feb;56(2):368-76. doi: 10.1093/pcp/pcu168. Epub 2014 Nov 20. PMID: 25416287." ## PMID- 25416287 OWN - NLM STAT- MEDLINE DCOM- 20151105 LR - 20181202 IS - 1471-9053 (Electronic) IS - 0032-0781 (Linking) VI - 56 IP - 2 DP - 2015 Feb TI - NODULE INCEPTION antagonistically regulates gene expression with nitrate in Lotus japonicus. PG - 368-76 LID - 10.1093/pcp/pcu168 [doi] AB - Legumes produce root nodules as symbiotic organs where nitrogen-fixing bacteria are accommodated. Lotus japonicus NODULE INCEPTION (NIN) is an essential factor that specifically and positively regulates nodulation processes, and has evolved from a member of the NIN-like proteins, of which Arabidopsis homologs target nitrate-responsive elements (NREs), and activate gene expression in response to nitrate. It is therefore assumed that the NIN-mediated transcriptional network overlaps with those regulated by NLPs, because of their common DNA-binding RWP-RK domains. However, nodulation is inhibited in the presence of nitrate, and involvement of NIN in nitrate responses has remained largely unknown. Here we determined a consensus of NIN-binding nucleotide sequences (NBSs) by in vitro experiments, and revealed that the sequence pattern was very similar to those of NREs. Chromatin immunoprecitiation (ChIP)-PCR analyses showed that NIN targeted NREs in L. japonicus nitrate-inducible gene promoters, including LjNIR1, LjNRT2.1 and LjNRT2.2. Affinities of NIN binding to the NREs were comparable with that to NBS-yB1a, an NBS on the symbiotic LjNF-YB1 promoter, indicating that NREs are potential targets of NIN. However, rhizobial infection did not activate LjNIR1, LjNRT2.1 and LjNRT2.2. NIN ectopic expression interfered with nitrate-dependent activation of these genes. Nitrate treatment followed by NIN activation down-regulated expression of symbiotic NIN target genes. Our results showed that NIN and nitrate antagonistically regulate expression of genes that are activated by nitrate and NIN, respectively. We propose that this antagonistic relationship prevents inappropriate activation of genes in response to nitrate and rhizobial infection. CI - (c) The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com. FAU - Soyano, Takashi AU - Soyano T AD - National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, 305-8602 Japan. Present address: National Institute for Basic Biology, Okazaki, Aichi, 444-8585 Japan. FAU - Shimoda, Yoshikazu AU - Shimoda Y AD - National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, 305-8602 Japan. FAU - Hayashi, Makoto AU - Hayashi M AD - National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, 305-8602 Japan. Present address: RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa, 230-0045 Japan. makotoh@affrc.go.jp. LA - eng PT - Journal Article PT - Research Support, Non-U.S. Gov't DEP - 20141120 PL - Japan TA - Plant Cell Physiol JT - Plant & cell physiology JID - 9430925 RN - 0 (Nitrates) RN - 0 (Plant Proteins) SB - IM MH - Base Sequence MH - Consensus Sequence/genetics MH - Gene Expression Regulation, Plant/*drug effects MH - Genes, Plant MH - Lotus/drug effects/*genetics/microbiology MH - Molecular Sequence Data MH - Nitrates/*pharmacology MH - Plant Proteins/*metabolism MH - Promoter Regions, Genetic MH - Protein Binding/drug effects MH - Rhizobium/drug effects/physiology MH - Transcription, Genetic/drug effects OTO - NOTNLM OT - Lotus japonicus OT - NIN-binding nucleotide sequence OT - NIN-like protein OT - NODULE INCEPTION OT - Nitrate OT - Nitrate-responsive element OT - Root nodule symbiosis EDAT- 2014/11/25 06:00 MHDA- 2015/11/06 06:00 CRDT- 2014/11/23 06:00 PHST- 2014/11/23 06:00 [entrez] PHST- 2014/11/25 06:00 [pubmed] PHST- 2015/11/06 06:00 [medline] AID - pcu168 [pii] AID - 10.1093/pcp/pcu168 [doi] PST - ppublish SO - Plant Cell Physiol. 2015 Feb;56(2):368-76. doi: 10.1093/pcp/pcu168. Epub 2014 Nov 20. ##### PUB RECORD ##### ## 10.1104/pp.113.233379 24722550 Yoro, Suzaki et al., 2014 "Yoro E, Suzaki T, Toyokura K, Miyazawa H, Fukaki H, Kawaguchi M. A Positive Regulator of Nodule Organogenesis, NODULE INCEPTION, Acts as a Negative Regulator of Rhizobial Infection in Lotus japonicus. Plant Physiol. 2014 Jun;165(2):747-758. doi: 10.1104/pp.113.233379. Epub 2014 Apr 10. PMID: 24722550; PMCID: PMC4043699." ## PMID- 24722550 OWN - NLM STAT- PubMed-not-MEDLINE LR - 20211021 IS - 1532-2548 (Electronic) IS - 0032-0889 (Print) IS - 0032-0889 (Linking) VI - 165 IP - 2 DP - 2014 Jun TI - A Positive Regulator of Nodule Organogenesis, NODULE INCEPTION, Acts as a Negative Regulator of Rhizobial Infection in Lotus japonicus. PG - 747-758 AB - Legume-rhizobium symbiosis occurs in specialized root organs called nodules. To establish the symbiosis, two major genetically controlled events, rhizobial infection and organogenesis, must occur. For a successful symbiosis, it is essential that the two phenomena proceed simultaneously in different root tissues. Although several symbiotic genes have been identified during genetic screenings of nonsymbiotic mutants, most of the mutants harbor defects in both infection and organogenesis pathways, leading to experimental difficulty in investigating the molecular genetic relationships between the pathways. In this study, we isolated a novel nonnodulation mutant, daphne, in Lotus japonicus that shows complete loss of nodulation but a dramatically increased numbers of infection threads. Characterization of the locus responsible for these phenotypes revealed a chromosomal translocation upstream of NODULE INCEPTION (NIN) in daphne. Genetic analysis using a known nin mutant revealed that daphne is a novel nin mutant allele. Although the daphne mutant showed reduced induction of NIN after rhizobial infection, the spatial expression pattern of NIN in epidermal cells was broader than that in the wild type. Overexpression of NIN strongly suppressed hyperinfection in daphne, and daphne phenotypes were partially rescued by cortical expression of NIN. These observations suggested that the daphne mutation enhanced the role of NIN in the infection pathway due to a specific loss of the role of NIN in nodule organogenesis. Based on these results, we provide evidence that the bifunctional transcription factor NIN negatively regulates infection but positively regulates nodule organogenesis during the course of the symbiosis. CI - (c) 2014 American Society of Plant Biologists. All Rights Reserved. FAU - Yoro, Emiko AU - Yoro E AD - Division of Symbiotic Systems, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Basic Biology, School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan (K.T., H.F.); andResearch Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan (H.M.). FAU - Suzaki, Takuya AU - Suzaki T AD - Division of Symbiotic Systems, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Basic Biology, School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan (K.T., H.F.); andResearch Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan (H.M.). FAU - Toyokura, Koichi AU - Toyokura K AD - Division of Symbiotic Systems, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Basic Biology, School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan (K.T., H.F.); andResearch Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan (H.M.). FAU - Miyazawa, Hikota AU - Miyazawa H AD - Division of Symbiotic Systems, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Basic Biology, School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan (K.T., H.F.); andResearch Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan (H.M.). FAU - Fukaki, Hidehiro AU - Fukaki H AD - Division of Symbiotic Systems, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Basic Biology, School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan (K.T., H.F.); andResearch Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan (H.M.). FAU - Kawaguchi, Masayoshi AU - Kawaguchi M AD - Division of Symbiotic Systems, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Basic Biology, School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi 444-8585, Japan (E.Y., T.S., M.K.);Department of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan (K.T., H.F.); andResearch Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan (H.M.) masayosi@nibb.ac.jp. LA - eng PT - Journal Article DEP - 20140410 PL - United States TA - Plant Physiol JT - Plant physiology JID - 0401224 PMC - PMC4043699 EDAT- 2014/04/12 06:00 MHDA- 2014/04/12 06:01 PMCR- 2015/06/01 CRDT- 2014/04/12 06:00 PHST- 2014/04/12 06:00 [entrez] PHST- 2014/04/12 06:00 [pubmed] PHST- 2014/04/12 06:01 [medline] PHST- 2015/06/01 00:00 [pmc-release] AID - pp.113.233379 [pii] AID - 233379 [pii] AID - 10.1104/pp.113.233379 [doi] PST - ppublish SO - Plant Physiol. 2014 Jun;165(2):747-758. doi: 10.1104/pp.113.233379. Epub 2014 Apr 10.