Characterization of AtNUC-L1 Reveals a Central Role of Nucleolin in Nucleolus Organization and Silencing of AtNUC-L2 Gene in Arabidopsis

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2006 Nov 17

PMID 17108323

Citations 73

Authors

Frederic Pontvianne

Isabel Matia

Julien Douet

Sylvette Tourmente

Francisco J Medina

Manuel Echeverria

Julio Saez-Vasquez

Affiliations

Soon will be listed here.

Abstract

Nucleolin is one of the most abundant protein in the nucleolus and is a multifunctional protein involved in different steps of ribosome biogenesis. In contrast to animals and yeast, the genome of the model plant Arabidopsis thaliana encodes two nucleolin-like proteins, AtNUC-L1 and AtNUC-L2. However, only the AtNUC-L1 gene is ubiquitously expressed in normal growth conditions. Disruption of this AtNUC-L1 gene leads to severe plant growth and development defects. AtNUC-L1 is localized in the nucleolus, mainly in the dense fibrillar component. Absence of this protein in Atnuc-L1 plants induces nucleolar disorganization, nucleolus organizer region decondensation, and affects the accumulation levels of pre-rRNA precursors. Remarkably, in Atnuc-L1 plants the AtNUC-L2 gene is activated, suggesting that AtNUC-L2 might rescue, at least partially, the loss of AtNUC-L1. This work is the first description of a higher eukaryotic organism with a disrupted nucleolin-like gene and defines a new role for nucleolin in nucleolus structure and rDNA chromatin organization.

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References

Gruendler P, Unfried I, Pointner R, Schweizer D . Nucleotide sequence of the 25S-18S ribosomal gene spacer from Arabidopsis thaliana. Nucleic Acids Res. 1989; 17(15):6395-6. PMC: 318296. DOI: 10.1093/nar/17.15.6395. View

Risueno M, Medina F . The nucleolar structure in plant cells. Revis Biol Celular. 1986; 7:1-154. View

Lee W, Zabetakis D, Melese T . NSR1 is required for pre-rRNA processing and for the proper maintenance of steady-state levels of ribosomal subunits. Mol Cell Biol. 1992; 12(9):3865-71. PMC: 360260. DOI: 10.1128/mcb.12.9.3865-3871.1992. View

Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M . An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J. 1994; 13(14):3378-88. PMC: 395235. DOI: 10.1002/j.1460-2075.1994.tb06640.x. View

Gulli M, Girard J, Zabetakis D, Lapeyre B, Melese T, Caizergues-Ferrer M . gar2 is a nucleolar protein from Schizosaccharomyces pombe required for 18S rRNA and 40S ribosomal subunit accumulation. Nucleic Acids Res. 1995; 23(11):1912-8. PMC: 306962. DOI: 10.1093/nar/23.11.1912. View

Testillano P, Gonzalez-Melendi P, Ahmadian P, Risueno M . The methylation-acetylation method: an ultrastructural cytochemistry for nucleic acids compatible with immunogold studies. J Struct Biol. 1995; 114(2):123-39. DOI: 10.1006/jsbi.1995.1012. View

Shaw P, Jordan E . The nucleolus. Annu Rev Cell Dev Biol. 1995; 11:93-121. DOI: 10.1146/annurev.cb.11.110195.000521. View

Bogre L, Jonak C, Mink M, Meskiene I, Traas J, Ha D . Developmental and cell cycle regulation of alfalfa nucMs1, a plant homolog of the yeast Nsr1 and mammalian nucleolin. Plant Cell. 1996; 8(3):417-28. PMC: 161110. View

Gulli M, Faubladier M, Sicard H, Caizergues-Ferrer M, Gas N . Ultrastructural changes in the Schizosaccharomyces pombe nucleolus following the disruption of the gar2+ gene, which encodes a nucleolar protein structurally related to nucleolin. Chromosoma. 1997; 105(7-8):542-52. DOI: 10.1007/BF02510491. View

10.

Tong C, Reichler S, Blumenthal S, Balk J, Hsieh H, Roux S . Light regulation of the abundance of mRNA encoding a nucleolin-like protein localized in the nucleoli of pea nuclei. Plant Physiol. 1997; 114(2):643-52. PMC: 158348. DOI: 10.1104/pp.114.2.643. View

11.

Caparros-Ruiz D, Lahmy S, Piersanti S, Echeverria M . Two ribosomal DNA-binding factors interact with a cluster of motifs on the 5' external transcribed spacer, upstream from the primary pre-rRNA processing site in a higher plant. Eur J Biochem. 1997; 247(3):981-9. DOI: 10.1111/j.1432-1033.1997.00981.x. View

12.

Saez-Vasquez J, Pikaard C . Extensive purification of a putative RNA polymerase I holoenzyme from plants that accurately initiates rRNA gene transcription in vitro. Proc Natl Acad Sci U S A. 1997; 94(22):11869-74. PMC: 23640. DOI: 10.1073/pnas.94.22.11869. View

13.

Ginisty H, Amalric F, Bouvet P . Nucleolin functions in the first step of ribosomal RNA processing. EMBO J. 1998; 17(5):1476-86. PMC: 1170495. DOI: 10.1093/emboj/17.5.1476. View

14.

Bouvet P, Diaz J, Kindbeiter K, Madjar J, Amalric F . Nucleolin interacts with several ribosomal proteins through its RGG domain. J Biol Chem. 1998; 273(30):19025-9. DOI: 10.1074/jbc.273.30.19025. View

15.

Oakes M, Aris J, Brockenbrough J, Wai H, Vu L, Nomura M . Mutational analysis of the structure and localization of the nucleolus in the yeast Saccharomyces cerevisiae. J Cell Biol. 1998; 143(1):23-34. PMC: 2132813. DOI: 10.1083/jcb.143.1.23. View

16.

Ginisty H, Sicard H, Roger B, Bouvet P . Structure and functions of nucleolin. J Cell Sci. 1999; 112 ( Pt 6):761-72. DOI: 10.1242/jcs.112.6.761. View

17.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

18.

Hernandez-Verdun D . Nucleolus in the spotlight. Cell Cycle. 2004; 4(1):106-8. DOI: 10.4161/cc.4.1.1355. View

19.

Lam Y, Trinkle-Mulcahy L, Lamond A . The nucleolus. J Cell Sci. 2005; 118(Pt 7):1335-7. DOI: 10.1242/jcs.01736. View

20.

Thiry M, Lafontaine D . Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol. 2005; 15(4):194-9. DOI: 10.1016/j.tcb.2005.02.007. View