Skip to main content
SpringerLink
Log in

The function of the RNA-binding protein TEL1 in moss reveals ancient regulatory mechanisms of shoot development

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The shoot represents the basic body plan in land plants. It consists of a repeated structure composed of stems and leaves. Whereas vascular plants generate a shoot in their diploid phase, non-vascular plants such as mosses form a shoot (called the gametophore) in their haploid generation. The evolution of regulatory mechanisms or genetic networks used in the development of these two kinds of shoots is unclear. TERMINAL EAR1-like genes have been involved in diploid shoot development in vascular plants. Here, we show that disruption of PpTEL1 from the moss Physcomitrella patens, causes reduced protonema growth and gametophore initiation, as well as defects in gametophore development. Leafy shoots formed on ΔTEL1 mutants exhibit shorter stems with more leaves per shoot, suggesting an accelerated leaf initiation (shortened plastochron), a phenotype shared with the Poaceae vascular plants TE1 and PLA2/LHD2 mutants. Moreover, the positive correlation between plastochron length and leaf size observed in ΔTEL1 mutants suggests a conserved compensatory mechanism correlating leaf growth and leaf initiation rate that would minimize overall changes in plant biomass. The RNA-binding protein encoded by PpTEL1 contains two N-terminus RNA-recognition motifs, and a third C-terminus non-canonical RRM, specific to TEL proteins. Removal of the PpTEL1 C-terminus (including this third RRM) or only 16–18 amino acids within it seriously impairs PpTEL1 function, suggesting a critical role for this third RRM. These results show a conserved function of the RNA-binding PpTEL1 protein in the regulation of shoot development, from early ancestors to vascular plants, that depends on the third TEL-specific RRM.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Anastasiou E, Kenz S, Gerstung M, MacLean D, Timmer J, Fleck C, Lenhard M (2007) Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Dev Cell 13:843–856

    Article  PubMed  CAS  Google Scholar 

  • Anderson GH, Alvarez ND, Gilman C, Jeffares DC, Trainor VC, Hanson MR, Veit B (2004) Diversification of genes encoding mei2-like RNA binding proteins in plants. Plant Mol Biol 54:653–670

    Article  PubMed  CAS  Google Scholar 

  • Burd CG, Dreyfuss G (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615–621

    Article  PubMed  CAS  Google Scholar 

  • Campalans A, Kondorosi A, Crespi M (2004) Enod40, a short open reading frame-containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula. Plant Cell 16:1047–1059

    Article  PubMed  CAS  Google Scholar 

  • Charon C, Vivancos J, Mazubert C, Paquet N, Pilate G, Dron M (2010) Structure and vascular tissues expression of duplicated TERMINAL EAR1-like paralogues in poplar. Planta 231:525–535

    Article  PubMed  CAS  Google Scholar 

  • Cléry A, Blatter M, Allain FH-T (2008) RNA recognition motifs: boring? Not quite. Curr Opin Struc Biol 18:290–298

    Article  Google Scholar 

  • Cove D, Bezanilla M, Harries P, Quatrano R (2006) Mosses as model systems for the study of metabolism and development. Annu Rev Plant Biol 57:497–520

    Article  PubMed  CAS  Google Scholar 

  • Dolan L (2009) Body building on land–morphological evolution of land plants. Curr Opin Plant Biol 12:4–8

    Article  PubMed  CAS  Google Scholar 

  • Dreyfuss G, Kim VN, Kataoka N (2002) Messenger-RNA-binding proteins and the messages they carry. Natl Rev Mol Cell Biol 3:195–205

    Article  CAS  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  PubMed  CAS  Google Scholar 

  • Floyd SK, Bowman JL (2007) The ancestral developmental tool kit of land plants. Int J Plant Sci 168:1–35

    Article  CAS  Google Scholar 

  • Frank W, Decker EL, Reski R (2005) Molecular tools to study Physcomitrella patens. Plant Biol 7:220–227

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) PHYML-A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Harigaya Y, Tanaka H, Yamanaka S, Tanaka K, Watanabe Y, Tsutsumi C, Chikashige Y, Hiraoka Y, Yamashita A, Yamamoto M (2006) Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442:45–50

    Article  PubMed  CAS  Google Scholar 

  • Harrison CJ, Corlay SB, Moylan EC, Alexander DL, Scotland RW, Langdale JA (2005) Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434:509–514

    Article  PubMed  CAS  Google Scholar 

  • Hasson A, Blein T, Laufs P (2010) Leaving the meristems behind: the genetic and molecular control of leaf patterning and morphogenesis. C R Biol 333:350–360

    Article  PubMed  CAS  Google Scholar 

  • Hejatko J, Blilou I, Brewer PB, Friml J, Scheres B, Benkova E (2006) In situ hybridization technique for mRNA detection in whole mount Arabidopsis samples. Nat Protoc 1:1939–1946

    Article  PubMed  CAS  Google Scholar 

  • Hirayama T, Ishida C, Kuromori T, Obata S, Shimoda C, Yamamoto M, Shinozaki K, Ohto C (1997) Functional cloning of a cDNA encoding Mei2-like protein from Arabidopsis thaliana using a fission yeast pheromone receptor deficient mutant. FEBS Lett 413:16–20

    Article  PubMed  CAS  Google Scholar 

  • Itoh JI, Hasegawa A, Kitano H, Nagato Y (1998) A recessive heterochronic mutation, plastochron1, shortens the plastochron and elongates the vegetative phase in rice. Plant Cell 10:1511–1522

    Article  PubMed  CAS  Google Scholar 

  • Jeffares DC, Phillips MJ, Moore S, Veit B (2004) A description of the Mei2-like protein family; structure, phylogenetic distribution and biological context. Dev Genes Evol 214:149–158

    Article  PubMed  CAS  Google Scholar 

  • Katsumata K, Fukazawa J, Magome H, Jikumaru Y, Kamiya Y, Natsume M, Kawaide H, Yamaguchi S (2011) Involvement of the CYP78A subfamily of cytochrome P450 monooxygenases in protonema growth and gametophores formation in the moss Physcomitrella patens. Biosci Biotechnol Biochem 75:331–336

    Article  PubMed  CAS  Google Scholar 

  • Kaur J, Sebastian J, Siddiqi I (2006) The Arabidopsis-mei2-like genes play a role in meiosis and vegetative growth in Arabidopsis. Plant Cell 18:545–559

    Article  PubMed  CAS  Google Scholar 

  • Kawakatsu T, Itoh J-I, Miyoshi K, Kurata N, Alvarez N, Veit B, Nagato Y (2006) PLASTOCHRON2 regulates leaf initiation and maturation in rice. Plant Cell 18:612–625

    Article  PubMed  CAS  Google Scholar 

  • Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39

    Article  CAS  Google Scholar 

  • Langdale JA (2008) Evolution of developmental mechanisms in plants. Curr Opin Genet Dev 18:368–373

    Article  PubMed  CAS  Google Scholar 

  • Lorkovic ZJ (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci 14:229–236

    Article  PubMed  CAS  Google Scholar 

  • Lorkovic ZJ, Barta A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res 30:623–635

    Article  PubMed  CAS  Google Scholar 

  • Lyndon RF (1998) The shoot apical meristem: its growth and development. Cambridge University Press, Cambridge

    Google Scholar 

  • Maris C, Dominguez C, Allain FH-T (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272:2118–2131

    Article  PubMed  CAS  Google Scholar 

  • Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Scharfer DG, Dolan L (2007) An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316:1477–1480

    Article  PubMed  CAS  Google Scholar 

  • Miyoshi K, Ahn B-O, Kawakatsu T, Ito Y, Itoh J-I, Nagato Y, Kurata N (2004) PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc Natl Acad Sci USA 101:875–880

    Article  PubMed  CAS  Google Scholar 

  • Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Paquet N, Bernadet M, Morin H, Traas J, Dron M, Charon C (2005) Expression patterns of TEL genes in Poaceae suggest a conserved association with cell differentiation. J Exp Bot 56:1605–1614

    Article  PubMed  CAS  Google Scholar 

  • Poethig RS (2009) Small RNAs and developmental timing in plants. Curr Opin Genet Dev 19:374–378

    Article  PubMed  CAS  Google Scholar 

  • Quatrano RS, McDaniel SF, Khandelwal A, Perroud PF, Cove DJ (2007) Physcomitrella patens: mosses enter the genomic age. Curr Opin Plant Biol 10:182–189

    Article  PubMed  CAS  Google Scholar 

  • Raven PH, Evert RF, Eichhorn SE (2005) The biology of plants. New York and Basingstoke, New York

    Google Scholar 

  • Rensing SA et al (2008) The Physcomitrella patens genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–68

    Article  PubMed  CAS  Google Scholar 

  • Rouhier N, Gelhaye E, Jacquot J-P (2004) Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61:1266–1277

    Article  PubMed  CAS  Google Scholar 

  • Sakakibara K, Nishiyama T, Deguchi H, Hasebe M (2008) Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development. Evol Dev 10:555–566

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Frisch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schaefer D (2002) A new moss genetics: targeted mutagenesis in Physcomitrella patens. Annu Rev Plant Biol 53:477–501

    Article  PubMed  CAS  Google Scholar 

  • Schaefer DG, Zrÿd JP (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206

    Article  PubMed  CAS  Google Scholar 

  • Schaefer DG, Delacote F, Charlot F, Vrielynck N, Guyon-Debast A, Le Guin S, Neuhaus JM, Doutriaux MP, Nogué F (2010) RAD51 loss of function abolishes gene targeting and de-represses illegitimate integration in the moss Physcomitrella patens. DNA Repair 9:526–533

    Article  PubMed  CAS  Google Scholar 

  • Steeves TA, Sussex IM (1989) Patterns in plant development. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Tanahashi T, Sumikawa N, Kato M, Hasebe M (2005) Diversification of gene function: homologs of the floral regulator FLO/FLY control the first zygotic cell division in the moss Physcomitrella patens. Development 132:1727–1736

    Article  PubMed  CAS  Google Scholar 

  • Thompson JF, Gibson F, Plewmiak F, Jenamougin F, Higgins DG (1997) The ClustalX window interface: flexible strategies for multiple sequence alignment aided by quality analysis tool. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Trouiller B, Schaefer DG, Charlot F, Nogué F (2006) MSH2 is essential for the preservation of genome integrity and prevents homeologous recombination in the moss Physcomitrella patens. Nucleic Acids Res 34:232–242

    Article  PubMed  CAS  Google Scholar 

  • Veit B, Briggs SP, Schmidt RJ, Yanofsky MF, Hake S (1998) Regulation of leaf initiation by the terminal ear1 gene of maize. Nature 393:166–168

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Schwab R, Czech B, Mica E, Weigel D (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20:1231–1243

    Article  PubMed  CAS  Google Scholar 

  • Watanabe Y, Yamamoto M (1994) S. pombe mei2 + encodes an RNA-binding protein essential for premeiotic DNA synthesis and meiosis I, which cooperates with a novel RNA species meiRNA. Cell 78:487–498

    Article  PubMed  CAS  Google Scholar 

  • Watanabe Y, Shinozaki-Yabana S, Chikashige Y, Hiraoka Y, Yamamoto M (1997) Phosphorylation of RNA-binding protein controls cell cycle switch from mitotic to meiotic in fission yeast. Nature 386:187–190

    Article  PubMed  CAS  Google Scholar 

  • Xiong GS, Hu XM, Jiao YQ, Yu YC, Chu CC, Li JY, Qian Q, Wang YH (2006) LEAFY HEAD2, which encodes a putative RNA-binding protein, regulates shoot development of rice. Cell Res 16:267–276

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge Pr. Didier Schaefer for help with moss phenotype analyses and sporogenesis, Dr. Christian Raquin for technical help regarding moss sterilization, and Dr. Martin Crespi for careful reading of the manuscript and useful discussions. We also thank Séverine Domenichini, Olivier Catrice and the IRF87 “Imagery and cellular biology” platform for scanning electron microscopy and flow cytometry. This work was supported by grants from the Ministère Français de l’Enseignement Supérieur et de la Recherche (JV and NP).

Author information

Authors and Affiliations

  1. Institut de Biologie des Plantes-CNRS (UMR8618), Université Paris-Sud 11, Saclay Plant Sciences (SPS), 91405, Orsay Cedex, France

    Julien Vivancos, Lara Spinner, Christelle Mazubert, Nicolas Paquet, Vincent Thareau, Michel Dron & Céline Charon

  2. Station de Génétique et d’Amélioration des Plantes, INRA, Route de St Cyr, 78026, Versailles, France

    Lara Spinner, Florence Charlot & Fabien Nogué

Authors
  1. Julien Vivancos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lara Spinner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christelle Mazubert
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Florence Charlot
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicolas Paquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vincent Thareau
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michel Dron
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fabien Nogué
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Céline Charon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Céline Charon.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 24 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vivancos, J., Spinner, L., Mazubert, C. et al. The function of the RNA-binding protein TEL1 in moss reveals ancient regulatory mechanisms of shoot development. Plant Mol Biol 78, 323–336 (2012). https://doi.org/10.1007/s11103-011-9867-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-011-9867-9

Keywords

Search

Navigation