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CLE peptide signaling and nitrogen interactions in plant root development

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Abstract

The CLAVATA signaling pathway is essential for the regulation of meristem activities in plants. This signaling pathway consists of small signaling peptides of the CLE family interacting with CLAVATA1 and leucine-rich repeat receptor-like kinases (LRR-RLKs). The peptide-receptor relationships determine the specificities of CLE-dependent signals controlling stem cell fate and differentiation that are critical for the establishment and maintenance of shoot and root apical meristems. Plants root systems are highly organized into three-dimensional structures for successful anchoring and uptake of water and mineral nutrients from the soil environment. Recent studies have provided evidence that CLE peptides and CLAVATA signaling pathways play pivotal roles in the regulation of lateral root development and systemic autoregulation of nodulation (AON) integrated with nitrogen (N) signaling mechanisms. Integrations of CLE and N signaling pathways through shoot–root vascular connections suggest that N demand modulates morphological control mechanisms and optimize N uptake as well as symbiotic N fixation in roots.

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References

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y-S, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120. doi:10.1016/j.cell.2004.09.018

    Article  CAS  PubMed  Google Scholar 

  • Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S, Tsuchiya YN, Sawa S, Fukuda H, von Wirén N, Takahashi H (2014a) CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc Natl Acad Sci USA 111:2029–2034. doi:10.1073/pnas.1319953111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Araya T, von Wirén N, Takahashi H (2014b) CLE peptides regulate lateral root development in response to nitrogen nutritional status of plants. Plant Signal Behav 9:e29302. doi:10.4161/psb.29302

    Article  PubMed Central  Google Scholar 

  • Araya T, Kubo T, von Wirén N, Takahashi H (2016) Statistical modeling of nitrogen-dependent modulation of root system architecture in Arabidopsis thaliana. J Integr Plant Biol 58:254–265. doi:10.1111/jipb.12433

    PubMed  Google Scholar 

  • Becraft PW, Stinard PS, McCarty DR (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409

    Article  CAS  PubMed  Google Scholar 

  • Becraft PW, Kang SH, Suh SG (2001) The maize CRINKLY4 receptor kinase controls a cell-autonomous differentiation response. Plant Physiol 127:486–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Betsuyaku S, Takahashi F, Kinoshita A, Miwa H, Shinozaki K, Fukuda H, Sawa S (2011) Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis. Plant Cell Physiol 52:14–29. doi:10.1093/pcp/pcq157

    Article  CAS  PubMed  Google Scholar 

  • Bleckmann A, Weidtkamp-Peters S, Seidel CAM, Simon R (2010) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152:166–176. doi:10.1104/pp.109.149930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouguyon E, Brun F, Meynard D, Kubeš M, Pervent M, Leran S, Lacombe B, Krouk G, Guiderdoni E, Zažímalová E, Hoyerová K, Nacry P, Gojon A (2015) Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat Plants. doi:10.1038/nplants.2015.15

    PubMed  Google Scholar 

  • Casamitjana-Martínez E, Hofhuis HF, Xu J, Liu C-M, Heidstra R, Scheres B (2003) Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr Biol 13:1435–1441

    Article  PubMed  Google Scholar 

  • Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418

    CAS  PubMed  Google Scholar 

  • Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057–2067

    CAS  Google Scholar 

  • Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585

    Article  CAS  PubMed  Google Scholar 

  • Czyzewicz N, Shi C-L, Vu LD, Van De Cotte B, Hodgman C, Butenko MA, De Smet I (2015) Modulation of Arabidopsis and monocot root architecture by CLAVATA3/EMBRYO SURROUNDING REGION 26 peptide. J Exp Bot 66:5229–5243. doi:10.1093/jxb/erv360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, Wang JY, Meuli N, Vanneste S, Friml J, Hilson P, Jürgens G, Ingram GC, Inzé D, Benfey PN, Beeckman T (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594–597. doi:10.1126/science.1160158

    Article  PubMed  Google Scholar 

  • Delay C, Imin N, Djordjevic MA (2013) Regulation of Arabidopsis root development by small signaling peptides. Front Plant Sci 4:352. doi:10.3389/fpls.2013.00352

    Article  PubMed  PubMed Central  Google Scholar 

  • DeYoung BJ, Clark SE (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180:895–904. doi:10.1534/genetics.108.091108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16. doi:10.1111/j.1365-313X.2005.02592.x

    Article  CAS  PubMed  Google Scholar 

  • Diévart A, Dalal M, Tax FE, Lacey AD, Huttly A, Li J, Clark SE (2003) CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell 15:1198–1211

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci USA 107:12046–12051. doi:10.1073/pnas.1000672107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Djordjevic MA, Mohd-Radzman NA, Imin N (2015) Small-peptide signals that control root nodule number, development, and symbiosis. J Exp Bot 66:5171–5181. doi:10.1093/jxb/erv357

    Article  CAS  PubMed  Google Scholar 

  • Endo S, Betsuyaku S, Fukuda H (2014) Endogenous peptide ligand-receptor systems for diverse signaling networks in plants. Curr Opin Plant Biol 21:140–146. doi:10.1016/j.pbi.2014.07.011

    Article  CAS  PubMed  Google Scholar 

  • Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu C-M (2005) The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 17:2542–2553. doi:10.1105/tpc.105.034009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914

    Article  CAS  PubMed  Google Scholar 

  • Forde BG (2014) Nitrogen signalling pathways shaping root system architecture: an update. Curr Opin Plant Biol 21:30–36. doi:10.1016/j.pbi.2014.06.004

    Article  CAS  PubMed  Google Scholar 

  • Forzani C, Aichinger E, Sornay E, Willemsen V, Laux T, Dewitte W, Murray JAH (2014) WOX5 suppresses CYCLIN D activity to establish quiescence at the center of the root stem cell niche. Curr Biol CB 24:1939–1944. doi:10.1016/j.cub.2014.07.019

    Article  CAS  PubMed  Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057. doi:10.1038/nature06206

    Article  CAS  PubMed  Google Scholar 

  • Giehl RFH, von Wirén N (2014) Root nutrient foraging. Plant Physiol 166:509–517. doi:10.1104/pp.114.245225

    Article  PubMed  PubMed Central  Google Scholar 

  • Gifford ML, Dean S, Ingram GC (2003) The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development. Development 130:4249–4258

    Article  CAS  PubMed  Google Scholar 

  • Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179. doi:10.1104/pp.113.218453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Y, Han L, Hymes M, Denver R, Clark SE (2010) CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J 63:889–900. doi:10.1111/j.1365-313X.2010.04295.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668. doi:10.1242/dev.00963

    Article  CAS  PubMed  Google Scholar 

  • Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194. doi:10.1016/j.cell.2009.07.004

    Article  CAS  PubMed  Google Scholar 

  • Hobe M, Müller R, Grünewald M, Brand U, Simon R (2003) Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol 213:371–381. doi:10.1007/s00427-003-0329-5

    Article  CAS  PubMed  Google Scholar 

  • Hord CLH, Chen C, Deyoung BJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18:1667–1680. doi:10.1105/tpc.105.036871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–1934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji H, Wang S, Li K, Szakonyi D, Koncz C, Li X (2015) PRL1 modulates root stem cell niche activity and meristem size through WOX5 and PLTs in Arabidopsis. Plant J 81:399–412. doi:10.1111/tpj.12733

    Article  CAS  PubMed  Google Scholar 

  • Jin P, Guo T, Becraft PW (2000) The maize CR4 receptor-like kinase mediates a growth factor-like differentiation response. Genesis 27:104–116

    Article  CAS  PubMed  Google Scholar 

  • Jobbágy EG, Jackson RB (2001) The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry 53:51–77. doi:10.1023/A:1010760720215

    Article  Google Scholar 

  • Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851

    CAS  PubMed  Google Scholar 

  • Kinoshita A, Nakamura Y, Sasaki E, Kyozuka J, Fukuda H, Sawa S (2007) Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol 48:1821–1825. doi:10.1093/pcp/pcm154

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, Simon R, Yamaguchi-Shinozaki K, Fukuda H, Sawa S (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–3920. doi:10.1242/dev.048199

    Article  CAS  PubMed  Google Scholar 

  • Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937. doi:10.1016/j.devcel.2010.05.008

    Article  CAS  PubMed  Google Scholar 

  • Krouk G, Ruffel S, Gutiérrez RA, Gojon A, Crawford NM, Coruzzi GM, Lacombe B (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16:178–182. doi:10.1016/j.tplants.2011.02.004

    Article  CAS  PubMed  Google Scholar 

  • Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426. doi:10.1038/nature01207

    Article  CAS  PubMed  Google Scholar 

  • Laux T, Mayer KF, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96

    CAS  PubMed  Google Scholar 

  • Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18:450–458. doi:10.1016/j.tplants.2013.04.006

    Article  CAS  PubMed  Google Scholar 

  • Leibfried A, To JPC, Busch W, Stehling S, Kehle A, Demar M, Kieber JJ, Lohmann JU (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438:1172–1175. doi:10.1038/nature04270

    Article  CAS  PubMed  Google Scholar 

  • Lima JE, Kojima S, Takahashi H, von Wirén N (2010) Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell 22:3621–3633. doi:10.1105/tpc.110.076216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  Google Scholar 

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049. doi:10.1104/pp.111.175414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112:347–357. doi:10.1093/aob/mcs293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma W, Li J, Qu B, He X, Zhao X, Li B, Fu X, Tong Y (2014) Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis. Plant J 78:70–79. doi:10.1111/tpj.12448

    Article  CAS  PubMed  Google Scholar 

  • Matsubayashi Y (2014) Posttranslationally modified small-peptide signals in plants. Annu Rev Plant Biol 65:385–413. doi:10.1146/annurev-arplant-050312-120122

    Article  PubMed  Google Scholar 

  • Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815

    Article  CAS  PubMed  Google Scholar 

  • McKelvie AD (1961) A list of mutant genes in Arabidopsis thaliana (L.) Heynh. Radiat Bot 1:233–241. doi:10.1016/S0033-7560(61)80032-X

    Article  Google Scholar 

  • Meyer MR, Lichti CF, Townsend RR, Rao AG (2011) Identification of in vitro autophosphorylation sites and effects of phosphorylation on the Arabidopsis CRINKLY4 (ACR4) receptor-like kinase intracellular domain: insights into conformation, oligomerization, and activity. Biochemistry (Mosc) 50:2170–2186. doi:10.1021/bi101935x

    Article  CAS  Google Scholar 

  • Meyer MR, Shah S, Zhang J, Rohrs H, Rao AG (2015) Evidence for intermolecular interactions between the intracellular domains of the Arabidopsis receptor-like kinase ACR4, its homologs and the Wox5 transcription factor. PLoS One 10:e0118861. doi:10.1371/journal.pone.0118861

    Article  PubMed  PubMed Central  Google Scholar 

  • Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H, Sawa S (2008) The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol 49:1752–1757. doi:10.1093/pcp/pcn148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyahara A, Hirani TA, Oakes M, Kereszt A, Kobe B, Djordjevic MA, Gresshoff PM (2008) Soybean nodule autoregulation receptor kinase phosphorylates two kinase-associated protein phosphatases in vitro. J Biol Chem 283:25381–25391. doi:10.1074/jbc.M800400200

    Article  CAS  PubMed  Google Scholar 

  • Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D’Haeseleer K, Holsters M, Goormachtig S (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153:222–237. doi:10.1104/pp.110.153718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mortier V, De Wever E, Vuylsteke M, Holsters M, Goormachtig S (2012) Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. Plant J 70:367–376. doi:10.1111/j.1365-313X.2011.04881.x

    Article  CAS  PubMed  Google Scholar 

  • Müller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–946. doi:10.1105/tpc.107.057547

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy E, De Smet I (2014) Understanding the RALF family: a tale of many species. Trends Plant Sci 19:664–671. doi:10.1016/j.tplants.2014.06.005

    Article  CAS  PubMed  Google Scholar 

  • Murphy E, Smith S, De Smet I (2012) Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24:3198–3217. doi:10.1105/tpc.112.099010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nimchuk ZL, Zhou Y, Tarr PT, Peterson BA, Meyerowitz EM (2015) Plant stem cell maintenance by transcriptional cross-regulation of related receptor kinases. Development 142:1043–1049. doi:10.1242/dev.119677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura R, Hayashi M, Wu G-J, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kawaguchi M (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429. doi:10.1038/nature01231

    Article  CAS  PubMed  Google Scholar 

  • Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294. doi:10.1126/science.1150083

    Article  CAS  PubMed  Google Scholar 

  • Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5:578–580. doi:10.1038/nchembio.182

    Article  CAS  PubMed  Google Scholar 

  • Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50:67–77. doi:10.1093/pcp/pcn194

    Article  CAS  PubMed  Google Scholar 

  • Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M (2013) Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat Commun 4:2191. doi:10.1038/ncomms3191

    Article  PubMed  Google Scholar 

  • Pallakies H, Simon R (2014) The CLE40 and CRN/CLV2 signaling pathways antagonistically control root meristem growth in Arabidopsis. Mol Plant 7:1619–1636. doi:10.1093/mp/ssu094

    Article  CAS  PubMed  Google Scholar 

  • Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010) Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant, Cell Environ 33:1486–1501. doi:10.1111/j.1365-3040.2010.02158.x

    CAS  Google Scholar 

  • Reid DE, Ferguson BJ, Gresshoff PM (2011) Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant Microbe Interact 24:606–618. doi:10.1094/MPMI-09-10-0207

    Article  CAS  PubMed  Google Scholar 

  • Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103:19206–19211. doi:10.1073/pnas.0605275103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Villalon A, Hardtke CS (2014) Auxin and its Henchmen: hormonal cross talk in root growth and development. In: Zažímalová E, Petrášek J, Benková E (eds) Auxin and its role in plant development. Springer, Vienna, pp 245–264

    Chapter  Google Scholar 

  • Rojo E, Sharma VK, Kovaleva V, Raikhel NV, Fletcher JC (2002) CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14:969–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply versus demand. Proc Natl Acad Sci USA 108:18524–18529. doi:10.1073/pnas.1108684108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanders PL, Markhart AH (1992) Interspecific grafts demonstrate root system control of leaf water status in water-stressed Phaseolus. J Exp Bot 43:1563–1567. doi:10.1093/jxb/43.12.1563

    Article  Google Scholar 

  • Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814. doi:10.1038/nature05703

    Article  CAS  PubMed  Google Scholar 

  • Satbhai SB, Ristova D, Busch W (2015) Underground tuning: quantitative regulation of root growth. J Exp Bot 66:1099–1112. doi:10.1093/jxb/eru529

    Article  CAS  PubMed  Google Scholar 

  • Saur IML, Oakes M, Djordjevic MA, Imin N (2011) Crosstalk between the nodulation signaling pathway and the autoregulation of nodulation in Medicago truncatula. New Phytol 190:865–874. doi:10.1111/j.1469-8137.2011.03738.x

    Article  CAS  PubMed  Google Scholar 

  • Scheible W-R, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499. doi:10.1104/pp.104.047019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnabel E, Journet E-P, de Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 58:809–822. doi:10.1007/s11103-005-8102-y

    Article  PubMed  Google Scholar 

  • Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644

    Article  CAS  PubMed  Google Scholar 

  • Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109–112. doi:10.1126/science.1077937

    Article  CAS  PubMed  Google Scholar 

  • Shimizu N, Ishida T, Yamada M, Shigenobu S, Tabata R, Kinoshita A, Yamaguchi K, Hasebe M, Mitsumasu K, Sawa S (2015) BAM 1 and RECEPTOR-LIKE PROTEIN KINASE 2 constitute a signaling pathway and modulate CLE peptide-triggered growth inhibition in Arabidopsis root. New Phytol 208:1104–1113. doi:10.1111/nph.13520

    Article  CAS  PubMed  Google Scholar 

  • Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914. doi:10.1016/j.cub.2009.03.060

    Article  CAS  PubMed  Google Scholar 

  • Stahl Y, Grabowski S, Bleckmann A, Kühnemuth R, Weidtkamp-Peters S, Pinto KG, Kirschner GK, Schmid JB, Wink RH, Hülsewede A, Felekyan S, Seidel CAM, Simon R (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol 23:362–371. doi:10.1016/j.cub.2013.01.045

    Article  CAS  PubMed  Google Scholar 

  • Strabala TJ, O’donnell PJ, Smit A-M, Ampomah-Dwamena C, Martin EJ, Netzler N, Nieuwenhuizen NJ, Quinn BD, Foote HCC, Hudson KR (2006) Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiol 140:1331–1344. doi:10.1104/pp.105.075515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka H, Watanabe M, Watanabe D, Tanaka T, Machida C, Machida Y (2002) ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant Cell Physiol 43:419–428

    Article  CAS  PubMed  Google Scholar 

  • Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45:1097–1102. doi:10.1038/ng.2725

    Article  CAS  PubMed  Google Scholar 

  • Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:4477–4482. doi:10.1073/pnas.0909571107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vidal EA, Moyano TC, Riveras E, Contreras-López O, Gutiérrez RA (2013) Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proc Natl Acad Sci USA 110:12840–12845. doi:10.1073/pnas.1310937110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe M, Tanaka H, Watanabe D, Machida C, Machida Y (2004) The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. Plant J 39:298–308. doi:10.1111/j.1365-313X.2004.02132.x

    Article  CAS  PubMed  Google Scholar 

  • Yadav RK, Perales M, Gruel J, Girke T, Jönsson H, Reddy GV (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25:2025–2030. doi:10.1101/gad.17258511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Jiao Y, Liu Z, Zhu Y-X (2015) ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells. Nat Commun 6:6003. doi:10.1038/ncomms7003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Wang Y, Li R, Song X, Wang Q, Huang S, Jin JB, Liu C-M, Lin J (2010) Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J 61:223–233. doi:10.1111/j.1365-313X.2009.04049.x

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors receive funding support from the National Science Foundation (IOS-1444549 to H.T.) and the Deutsche Forschungsgemeinschaft (WI1728/13-2 to N.v.W.).

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Authors and Affiliations

  1. Leibniz Institute of Plant Genetics and Crop Plant Research, 06466, Gatersleben, Germany

    Takao Araya & Nicolaus von Wirén

  2. Department of Biochemistry and Molecular Biology, Michigan State University, 603 Wilson Road, East Lansing, MI, 48824, USA

    Hideki Takahashi

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  1. Takao Araya
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  2. Nicolaus von Wirén
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  3. Hideki Takahashi
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Correspondence to Hideki Takahashi.

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Araya, T., von Wirén, N. & Takahashi, H. CLE peptide signaling and nitrogen interactions in plant root development. Plant Mol Biol 91, 607–615 (2016). https://doi.org/10.1007/s11103-016-0472-9

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  • DOI: https://doi.org/10.1007/s11103-016-0472-9

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