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Peptides Regulating Apical Meristem Development

  • Marc SomssichEmail author
  • Rüdiger Simon
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 16)

Abstract

Small signaling peptides are involved in numerous aspects of plant development. A well-studied group of peptides is the CLE family with its most prominent member CLAVATA 3 (CLV3), a key regulator of apical meristem maintenance during growth and development. Members of the CLE peptide family share a high sequence similarity, but are capable of triggering independent pathways. Recent work has revealed complex networks of interacting receptors that recognize different peptides, as well as various posttranslational modifications of the peptides which could account for the signaling specificities within the family. With the CLV pathway well studied in Arabidopsis, the insight gained in this model plant can now be transferred to other plant species to control meristem development.

Keywords

Shoot Apical Meristem Floral Meristem Shoot Meristem Embryo Surrounding Region Clv1 Mutant 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 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 52:14–29PubMedCrossRefGoogle Scholar
  2. Bleckmann A, Weidtkamp-Peters S, Seidel CA, Simon R (2010) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152:166–176PubMedCrossRefGoogle Scholar
  3. Bommert P, Lunde C, Nardmann J, Vollbrecht E, Running M, Jackson D, Hake S, Werr W (2005) thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132:1235–1245PubMedCrossRefGoogle Scholar
  4. Brand U, Grunewald M, Hobe M, Simon R (2002) Regulation of CLV3 expression by two homeobox genes in Arabidopsis. Plant Physiol 129:565–575PubMedCrossRefGoogle Scholar
  5. Chu H, Qian Q, Liang W, Yin C, Tan H, Yao X, Yuan Z, Yang J, Huang H, Luo D, Ma H, Zhang D (2006) The floral organ number4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant Physiol 142:1039–1052PubMedCrossRefGoogle Scholar
  6. Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418PubMedGoogle Scholar
  7. 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 121:2057–2067Google Scholar
  8. 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 89:575–585PubMedCrossRefGoogle Scholar
  9. Cock JM, McCormick S (2001) A large family of genes that share homology with CLAVATA3. Plant Physiol 126:939–942PubMedCrossRefGoogle Scholar
  10. DeYoung BJ, Clark SE (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180:895–904PubMedCrossRefGoogle Scholar
  11. 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 45:1–16PubMedCrossRefGoogle Scholar
  12. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914PubMedCrossRefGoogle Scholar
  13. Gagne JM, Clark SE (2010) The Arabidopsis stem cell factor POLTERGEIST is membrane localized and phospholipid stimulated. Plant Cell 22:729–743PubMedCrossRefGoogle Scholar
  14. 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 63:889–900PubMedCrossRefGoogle Scholar
  15. Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313:842–845PubMedCrossRefGoogle Scholar
  16. 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 11:1925–1934PubMedGoogle Scholar
  17. Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851PubMedGoogle Scholar
  18. Kieffer M, Stern Y, Cook H, Clerici E, Maulbetsch C, Laux T, Davies B (2006) Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. Plant Cell 18:560–573PubMedCrossRefGoogle Scholar
  19. 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 137:3911–3920PubMedCrossRefGoogle Scholar
  20. Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:845–848PubMedCrossRefGoogle Scholar
  21. Koornneef M, van Eden J, Hanhart CJ, Stam P, Braaksma FJ, Feenstra WJ (1983) Linkage map of Arabidopsis thaliana. J Hered 74:265–272Google Scholar
  22. Laux T, Mayer KF, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96PubMedGoogle Scholar
  23. Leibfried A, To JP, 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 438:1172–1175PubMedCrossRefGoogle Scholar
  24. Leyser HMO, Furner IJ (1992) Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana. Development 116:397–403Google Scholar
  25. Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312:1520–1523PubMedCrossRefGoogle Scholar
  26. Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815PubMedCrossRefGoogle Scholar
  27. Medford JI, Behringer FJ, Callos JD, Feldmann KA (1992) Normal and abnormal development in the Arabidopsis vegetative shoot apex. Plant Cell 4:631–643PubMedGoogle Scholar
  28. Meng L, Feldman LJ (2010) CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis. Planta 232:1061–1074PubMedCrossRefGoogle Scholar
  29. Meng L, Ruth KC, Fletcher JC, Feldman L (2010) The roles of different CLE domains in Arabidopsis CLE polypeptide activity and functional specificity. Mol Plant 3:760–772PubMedCrossRefGoogle Scholar
  30. 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 20:934–946PubMedCrossRefGoogle Scholar
  31. Nardmann J, Werr W (2006) The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. Mol Biol Evol 23:2492–2504PubMedCrossRefGoogle Scholar
  32. Nimchuk ZL, Tarr PT, Ohno C, Qu X, Meyerowitz EM (2011) Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr Biol 21:345–352PubMedCrossRefGoogle Scholar
  33. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294PubMedCrossRefGoogle Scholar
  34. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5:578–580PubMedCrossRefGoogle Scholar
  35. Okada K, Komaki MK, Shimura Y (1989) Mutational analysis of pistil structure and development of Arabidopsis thaliana. Cell Differ Dev 28:27–37PubMedCrossRefGoogle Scholar
  36. Opsahl-Ferstad HG, Le Deunff E, Dumas C, Rogowsky PM (1997) ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant J 12:235–246PubMedCrossRefGoogle Scholar
  37. 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 14:969–977PubMedCrossRefGoogle Scholar
  38. Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens 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 100:635–644PubMedCrossRefGoogle Scholar
  39. Song SK, Clark SE (2005) POL and related phosphatases are dosage-sensitive regulators of meristem and organ development in Arabidopsis. Dev Biol 285:272–284PubMedCrossRefGoogle Scholar
  40. Stuurman J, Jaggi F, Kuhlemeier C (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev 16:2213–2218PubMedCrossRefGoogle Scholar
  41. Suzaki T, Ohneda M, Toriba T, Yoshida A, Hirano HY (2009) FON2 SPARE1 redundantly regulates floral meristem maintenance with FLORAL ORGAN NUMBER2 in rice. PLoS Genet 5:e1000693PubMedCrossRefGoogle Scholar
  42. Taguchi-Shiobara F, Yuan Z, Hake S, Jackson D (2001) The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev 15:2755–2766PubMedCrossRefGoogle Scholar
  43. Whitford R, Fernandez A, De Groodt R, Ortega E, Hilson P (2008) Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc Natl Acad Sci USA 105:18625–18630PubMedCrossRefGoogle Scholar
  44. Williams RW, Wilson JM, Meyerowitz EM (1997) A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. Proc Natl Acad Sci USA 94:10467–10472PubMedCrossRefGoogle Scholar
  45. Yaginuma H, Hirakawa Y, Kondo Y, Ohashi-Ito K, Fukuda H (2011) A novel function of TDIF-related peptides: promotion of axillary bud formation. Plant Cell Physiol 52:1354–1364PubMedCrossRefGoogle Scholar
  46. Yu LP, Simon EJ, Trotochaud AE, Clark SE (2000) POLTERGEIST functions to regulate meristem development downstream of the CLAVATA loci. Development 127:1661–1670PubMedGoogle Scholar
  47. Yu LP, Miller AK, Clark SE (2003) POLTERGEIST encodes a protein phosphatase 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems. Curr Biol 13:179–188PubMedCrossRefGoogle Scholar
  48. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU (2010) Hormonal control of the shoot stem-cell niche. Nature 465:1089–1092PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Institut für EntwicklungsgenetikHeinrich-Heine-Universität DüsseldorfDüsseldorfGermany

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