AtNUFIP, an essential protein for plant development, reveals the impact of snoRNA gene organisation on the assembly of snoRNPs and rRNA methylation in Arabidopsis thaliana

Julie Rodor, Edouard Jobet, Jonathan Bizarro, Florence Vignols, Cristel Carles, Takamasa Suzuki, Kenzo Nakamura, Manuel Echeverría

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Summary In all eukaryotes, C/D small nucleolar ribonucleoproteins (C/D snoRNPs) are essential for methylation and processing of ribosomal RNAs. They consist of a box C/D small nucleolar RNA (C/D snoRNA) associated with four highly conserved nucleolar proteins. Recent data in HeLa cells and yeast have revealed that assembly of these snoRNPs is directed by NUFIP protein and other auxiliary factors. Nevertheless, the precise function and biological importance of NUFIP and the other assembly factors remains unknown. In plants, few studies have focused on RNA methylation and snoRNP biogenesis. Here, we identify and characterise the AtNUFIP gene that directs assembly of C/D snoRNP. To elucidate the function of AtNUFIP in planta, we characterized atnufip mutants. These mutants are viable but have severe developmental phenotypes. Northern blot analysis of snoRNA accumulation in atnufip mutants revealed a specific degradation of C/D snoRNAs and this situation is correlated with a reduction in rRNA methylation. Remarkably, the impact of AtNUFIP depends on the structure of snoRNA genes: it is essential for the accumulation of those C/D snoRNAs encoded by polycistronic genes, but not by monocistronic or tsnoRNA genes. We propose that AtNUFIP controls the kinetics of C/D snoRNP assembly on nascent precursors to overcome snoRNA degradation of aberrant RNPs. Finally, we show that AtNUFIP has broader RNP targets, controlling the accumulation of scaRNAs that direct methylation of spliceosomal snRNA in Cajal bodies.

Original languageEnglish (US)
Pages (from-to)807-819
Number of pages13
JournalPlant Journal
Volume65
Issue number5
DOIs
StatePublished - Mar 2011
Externally publishedYes

Fingerprint

Small Nucleolar Ribonucleoproteins
Small Nucleolar RNA
Plant Development
Arabidopsis
methylation
Methylation
plant development
Arabidopsis thaliana
ribosomal RNA
mutants
Genes
Proteins
genes
proteins
small nuclear RNA
RNA
ribonucleoproteins
degradation
Plantae
Northern blotting

Keywords

  • atnuf mutants
  • AtNUFIP
  • development
  • rRNA methylation
  • snoRNP assembly

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

AtNUFIP, an essential protein for plant development, reveals the impact of snoRNA gene organisation on the assembly of snoRNPs and rRNA methylation in Arabidopsis thaliana. / Rodor, Julie; Jobet, Edouard; Bizarro, Jonathan; Vignols, Florence; Carles, Cristel; Suzuki, Takamasa; Nakamura, Kenzo; Echeverría, Manuel.

In: Plant Journal, Vol. 65, No. 5, 03.2011, p. 807-819.

Research output: Contribution to journalArticle

Rodor, Julie ; Jobet, Edouard ; Bizarro, Jonathan ; Vignols, Florence ; Carles, Cristel ; Suzuki, Takamasa ; Nakamura, Kenzo ; Echeverría, Manuel. / AtNUFIP, an essential protein for plant development, reveals the impact of snoRNA gene organisation on the assembly of snoRNPs and rRNA methylation in Arabidopsis thaliana. In: Plant Journal. 2011 ; Vol. 65, No. 5. pp. 807-819.
@article{e96961ddefad4c9ba98c6418cdd75504,
title = "AtNUFIP, an essential protein for plant development, reveals the impact of snoRNA gene organisation on the assembly of snoRNPs and rRNA methylation in Arabidopsis thaliana",
abstract = "Summary In all eukaryotes, C/D small nucleolar ribonucleoproteins (C/D snoRNPs) are essential for methylation and processing of ribosomal RNAs. They consist of a box C/D small nucleolar RNA (C/D snoRNA) associated with four highly conserved nucleolar proteins. Recent data in HeLa cells and yeast have revealed that assembly of these snoRNPs is directed by NUFIP protein and other auxiliary factors. Nevertheless, the precise function and biological importance of NUFIP and the other assembly factors remains unknown. In plants, few studies have focused on RNA methylation and snoRNP biogenesis. Here, we identify and characterise the AtNUFIP gene that directs assembly of C/D snoRNP. To elucidate the function of AtNUFIP in planta, we characterized atnufip mutants. These mutants are viable but have severe developmental phenotypes. Northern blot analysis of snoRNA accumulation in atnufip mutants revealed a specific degradation of C/D snoRNAs and this situation is correlated with a reduction in rRNA methylation. Remarkably, the impact of AtNUFIP depends on the structure of snoRNA genes: it is essential for the accumulation of those C/D snoRNAs encoded by polycistronic genes, but not by monocistronic or tsnoRNA genes. We propose that AtNUFIP controls the kinetics of C/D snoRNP assembly on nascent precursors to overcome snoRNA degradation of aberrant RNPs. Finally, we show that AtNUFIP has broader RNP targets, controlling the accumulation of scaRNAs that direct methylation of spliceosomal snRNA in Cajal bodies.",
keywords = "atnuf mutants, AtNUFIP, development, rRNA methylation, snoRNP assembly",
author = "Julie Rodor and Edouard Jobet and Jonathan Bizarro and Florence Vignols and Cristel Carles and Takamasa Suzuki and Kenzo Nakamura and Manuel Echeverr{\'i}a",
year = "2011",
month = "3",
doi = "10.1111/j.1365-313X.2010.04468.x",
language = "English (US)",
volume = "65",
pages = "807--819",
journal = "Plant Journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell",
number = "5",

}

TY - JOUR

T1 - AtNUFIP, an essential protein for plant development, reveals the impact of snoRNA gene organisation on the assembly of snoRNPs and rRNA methylation in Arabidopsis thaliana

AU - Rodor, Julie

AU - Jobet, Edouard

AU - Bizarro, Jonathan

AU - Vignols, Florence

AU - Carles, Cristel

AU - Suzuki, Takamasa

AU - Nakamura, Kenzo

AU - Echeverría, Manuel

PY - 2011/3

Y1 - 2011/3

N2 - Summary In all eukaryotes, C/D small nucleolar ribonucleoproteins (C/D snoRNPs) are essential for methylation and processing of ribosomal RNAs. They consist of a box C/D small nucleolar RNA (C/D snoRNA) associated with four highly conserved nucleolar proteins. Recent data in HeLa cells and yeast have revealed that assembly of these snoRNPs is directed by NUFIP protein and other auxiliary factors. Nevertheless, the precise function and biological importance of NUFIP and the other assembly factors remains unknown. In plants, few studies have focused on RNA methylation and snoRNP biogenesis. Here, we identify and characterise the AtNUFIP gene that directs assembly of C/D snoRNP. To elucidate the function of AtNUFIP in planta, we characterized atnufip mutants. These mutants are viable but have severe developmental phenotypes. Northern blot analysis of snoRNA accumulation in atnufip mutants revealed a specific degradation of C/D snoRNAs and this situation is correlated with a reduction in rRNA methylation. Remarkably, the impact of AtNUFIP depends on the structure of snoRNA genes: it is essential for the accumulation of those C/D snoRNAs encoded by polycistronic genes, but not by monocistronic or tsnoRNA genes. We propose that AtNUFIP controls the kinetics of C/D snoRNP assembly on nascent precursors to overcome snoRNA degradation of aberrant RNPs. Finally, we show that AtNUFIP has broader RNP targets, controlling the accumulation of scaRNAs that direct methylation of spliceosomal snRNA in Cajal bodies.

AB - Summary In all eukaryotes, C/D small nucleolar ribonucleoproteins (C/D snoRNPs) are essential for methylation and processing of ribosomal RNAs. They consist of a box C/D small nucleolar RNA (C/D snoRNA) associated with four highly conserved nucleolar proteins. Recent data in HeLa cells and yeast have revealed that assembly of these snoRNPs is directed by NUFIP protein and other auxiliary factors. Nevertheless, the precise function and biological importance of NUFIP and the other assembly factors remains unknown. In plants, few studies have focused on RNA methylation and snoRNP biogenesis. Here, we identify and characterise the AtNUFIP gene that directs assembly of C/D snoRNP. To elucidate the function of AtNUFIP in planta, we characterized atnufip mutants. These mutants are viable but have severe developmental phenotypes. Northern blot analysis of snoRNA accumulation in atnufip mutants revealed a specific degradation of C/D snoRNAs and this situation is correlated with a reduction in rRNA methylation. Remarkably, the impact of AtNUFIP depends on the structure of snoRNA genes: it is essential for the accumulation of those C/D snoRNAs encoded by polycistronic genes, but not by monocistronic or tsnoRNA genes. We propose that AtNUFIP controls the kinetics of C/D snoRNP assembly on nascent precursors to overcome snoRNA degradation of aberrant RNPs. Finally, we show that AtNUFIP has broader RNP targets, controlling the accumulation of scaRNAs that direct methylation of spliceosomal snRNA in Cajal bodies.

KW - atnuf mutants

KW - AtNUFIP

KW - development

KW - rRNA methylation

KW - snoRNP assembly

UR - http://www.scopus.com/inward/record.url?scp=79952043809&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79952043809&partnerID=8YFLogxK

U2 - 10.1111/j.1365-313X.2010.04468.x

DO - 10.1111/j.1365-313X.2010.04468.x

M3 - Article

C2 - 21261762

AN - SCOPUS:79952043809

VL - 65

SP - 807

EP - 819

JO - Plant Journal

JF - Plant Journal

SN - 0960-7412

IS - 5

ER -