40S Ribosome Biogenesis Co-Factors Are Essential for Gametophyte and Embryo Development

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Missbach, Sandra ^a   Weis, Benjamin L ^a   Martin, Roman ^a   Simm, Stefan ^a   Bohnsack, Markus T ^a   Schleiff, Enrico ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ENDONUCLEASE; PROTEIN ENP1; PROTEIN NOB1; PROTEIN NOC4; PROTEIN PWP2; PROTEIN RRP5; RIBOSOME RNA; RNA 18S; RNA 40S; RNA PRECURSOR; T DNA; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BACKCROSSING; BIOGENESIS; CELL NUCLEUS; CONTROLLED STUDY; ENP1 GENE; ENZYME ACTIVITY; FEMALE GAMETOPHYTE; FLOWER; GENE INSERTION; GENETIC CONSERVATION; HETEROZYGOTE; MALE GAMETOPHYTE; NOB1 GENE; NOC4 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DEVELOPMENT; PLANT EMBRYOGENESIS; PLANT GENE; PLANT GENOME; PLANT SEED; PLANT STRUCTURES; POLLEN; PRE RIBOSOMAL COMPLEX; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PWP2 GENE; RIBOSOME; RIBOSOME BIOGENESIS; RNA PROCESSING; RRP5 GENE; SELFING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GERM CELLS, PLANT; NUCLEAR PROTEINS; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RIBOSOMES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEEDS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84873822164     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054084     Document Type: Article

References (69)

1. Venema J, Tollervey D, (1999) Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet 33: 261-311.
2. Kressler D, Linder P, de La Cruz J, (1999) Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol 19: 7897-912.
3. Fromont-Racine M, Senger B, Saveanu C, Fasiolo F, (2003) Ribosome assembly in eukaryotes. Gene 313: 17-42.
4. Henras AK, Soudet J, Gérus M, Lebaron S, Caizergues-Ferrer M, et al. (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 65: 2334-59.
5. Huang Y, Maraia RJ, (2001) Comparison of the RNA polymerase III transcription machinery in Schizosaccharomyces pombe, Saccharomyces cerevisiae and human. Nucleic Acids Res 29: 2675-90.
6. Comella P, Pontvianne F, Lahmy S, Vignols F, Barbezier N, et al. (2008) Characterization of a ribonuclease III-like protein required for cleavage ofthe pre-rRNA in the 3′ETS in Arabidopsis. Nucleic Acids Res 36: 1163-1175.
7. Lange H, Holec S, Cognat V, Pieuchot L, Le Ret M, et al. (2008) Degradation of a polyadenylated rRNA maturation by-product involves one of the three RRP6-like proteins in Arabidopsis thaliana. Mol Cell Biol 28: 3038-44.
8. Zakrzewska-Placzek M, Souret FF, Sobczyk GJ, Green PJ, Kufel J, (2010) Arabidopsis thaliana XRN2 is required for primary cleavage in the pre-ribosomal RNA. Nucleic Acids Res 38: 4487-502.
9. Lange H, Sement FM, Gagliardi D, (2011) MTR4, a putative RNA helicase and exosome co-factor, is required for proper rRNA biogenesis and development in Arabidopsis thaliana. Plant J 68: 51-63.
10. Li N, Yuan L, Liu N, Shi D, Li X, et al. (2009) SLOW WALKER2, a NOC1/MAK21 homologue, is essential for coordinated cell cycle progressionduring female gametophyte development in Arabidopsis. Plant Physiol 151: 1486-97.
11. Kato Y, Konishi M, Shigyo M, Yoneyama T, Yanagisawa S, (2010) Characterization of plant eukaryotic translation initiation factor 6 (eIF6) genes: The essential role in embryogenesis and their differential expression in Arabidopsis and rice. Biochem Biophys Res Commun 397: 673-8.
12. Lahmy S, Guilleminot J, Cheng CM, Bechtold N, Albert S, et al. (2004) DOMINO1, a member of a small plant-specific gene family, encodes a protein essential for nuclear and nucleolar functions. Plant J 39: 809-20.
13. Pontvianne F, Matía I, Douet J, Tourmente S, Medina FJ, et al. (2007) Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis. Mol Biol Cell 18: 369-79.
14. Huang CK, Huang LF, Huang JJ, Wu SJ, Yeh CH, et al. (2010) A DEAD-box protein, AtRH36, is essential for female gametophyte development and is involved in rRNA biogenesis in Arabidopsis. Plant Cell Physiol 51: 694-706.
15. Ren M, Qiu S, Venglat P, Xiang D, Feng L, et al. (2011) Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiol 155: 1367-82.
16. Faure JE, (2001) Double fertilization in flowering plants: discovery, study methods and mechanisms. C R Acad Sci III 324: 551-8.
17. Rotman N, Rozier F, Boavida L, Dumas C, Berger F, et al. (2003) Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol 13: 432-6.
18. Berger F, Hamamura Y, Ingouff M, Higashiyama T, (2008) Double fertilization- caught in the act. Trends Plant Sci 13: 437-43.
19. Ingouff M, Jullien PE, Berger F, (2006) The female gametophyte and the endosperm control cell proliferation and differentiation of the seed coat in Arabidopsis. Plant Cell 18: 3491-501.
20. Chaudhury AM, Berger F, (2001) Maternal control of seed development. Semin Cell Dev Biol 12: 381-6.
21. Donohue K, (2009) Completing the cycle: maternal effects as the missing link in plant life histories. Philos Trans R Soc Lond B Biol Sci 364: 1059-74.
22. Yadegari R, Drews GN, (2004) Female gametophyte development. Plant Cell 16: S133-41.
23. McCormick S, (2004) Control of male gametophyte development. Plant Cell 16: S142-53.
24. Xia C, Wang YJ, Li WQ, Chen YR, Deng Y, et al. (2010) The Arabidopsis eukaryotic translation initiation factor 3, subunit F (AteIF3f), is required for pollen germination and embryogenesis. Plant J 63: 189-202.
25. Harrison-Lowe NJ, Olsen LJ, (2008) Autophagy Protein 6 (ATG6) is Required for Pollen Germination in Arabidopsis thaliana. Autophagy 4: 339-348.
26. Zeng Q, Chen JG, Ellis BE, (2011) AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis. Plant J 67: 895-906.
27. De Storme N, Geelen D, (2011) The Arabidopsis mutant jason produces unreduced first division restitution male gametes through a parallel/fused spindle mechanism in meiosis II. Plant Physiol 155: 1403-15.
28. Drews GN, Yadegari R, (2002) Development and function of the angiosperm female gametophyte. Annu Rev Genet 36: 9-124.
29. Devic M, (2008) The importance of being essential: EMBRYO-DEFECTIVE genes in Arabidopsis. C R Biol 331: 726-36.
30. de Boer P, Vos HR, Faber AW, Vos JC, Raué HA, (2006) Rrp5p, a trans-acting factor in yeast ribosome biogenesis, is an RNA-binding protein with a pronounced preference for U-rich sequences. RNA 12: 263-71.
31. Vos HR, Faber AW, de Gier MD, Vos JC, Raué HA, (2004) Deletion of the three distal S1 motifs of Saccharomyces cerevisiae Rrp5p abolishes pre-rRNA processing at site A(2) without reducing the production of functional 40S subunits. Eukaryot Cell 3: 1504-12.
32. Young CL, Karbstein K, (2011) The roles of S1 RNA-binding domains in Rrp5's interactions with pre-rRNA. RNA 17: 512-21.
33. Pérez-Fernández J, Román A, De Las Rivas J, Bustelo XR, Dosil M, (2007) The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Molecular Cell Biology 27: 5414-29.
34. Dosil M, Bustelo XR, (2004) Functional characterization of Pwp2, a WD family protein essential for the assembly of the 90 S pre-ribosomal particle. J Biol Chem 279: 37385-97.
35. Fatica A, Tollervey D, Dlakić M, (2004) PIN domain of Nob1p is required for D-site cleavage in 20S pre-rRNA. RNA 10: 1698-701.
36. Lamanna AC, Karbstein K, (2009) Nob1 binds the single-stranded cleavage site D at the 3′-end of 18S rRNA with its PIN domain. Proc Natl Acad Sci USA 106: 14259-14264.
37. Pertschy B, Schneider C, Gnädig M, Schäfer T, Tollervey D, et al. (2009) RNA helicase Prp43 and its co-factor Pfa1 promote 20S to 18S rRNA processing catalyzed by the endonuclease Nob1. J Biol Chem 284: 35079-35091.
38. Schneider C, Leung E, Brown J, Tollervey D, (2009) The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37: 1127-40.
39. Glavan F, Behm-Ansmant I, Izaurralde E, Conti E, (2006) Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J 25: 5117-25.
40. Chen W, Bucaria J, Band DA, Sutton A, Sternglanz R, (2003) Enp1, a yeast protein associated with U3 and U14 snoRNAs, is required for pre-rRNA processing and 40S subunit synthesis. Nucleic Acids Res 31: 690-9.
41. Kühn H, Hierlmeier T, Merl J, Jakob S, Aguissa-Touré AH, et al. (2009) The Noc-domain containing C-terminus of Noc4p mediates both formation of the Noc4p-Nop14p submodule and its incorporation into the SSU processome. PLoS One 4: e8370.
42. Milkereit P, Strauss D, Bassler J, Gadal O, Kühn H, et al. (2003) A Noc complex specifically involved in the formation and nuclear export of ribosomal 40 S subunits. J Biol Chem 278: 4072-81.
43. Harscoët E, Dubreucq B, Palauqui JC, Lepiniec L, (2010) NOF1 encodes an Arabidopsis protein involved in the control of rRNA expression. PLoS One 5: e12829.
44. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-10.
45. Edwards K, Johnstone C, Thompson C, (1991) A simple and rapid method for the preparation of genomic plant DNA for PCR analysis. Nucleic Acids Res 19: 1349.
46. Thole V, Alves SC, Worland B, Bevan MW, Vain P, (2009) A protocol for efficiently retrieving and characterizing flanking sequence tags (FSTs) in Brachypodium distachyon T-DNA insertional mutants. Nature Protoc 4: 650-61.
47. Holsters M, de Waele D, Depicker A, Messens E, van Montagu M, et al. (1978) Transfection and transformation of Agrobacterium tumefaciens. Mol Gen Genet 163: 181-7.
48. Clough SJ, Bent AF, (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-43.
49. Vicient CM, Delseny M, (1999) Isolation of total RNA from Arabidopsis thaliana seeds. Anal Biochem 268: 412-3.
50. Sambrook J, Russel DW (2001) Molecular Cloning: A Laboratory Manual 3rd edn. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
51. Bohnsack MT, Kos M, Tollervey D, (2008) Quantitative analysis of snoRNA association with pre-ribosomes and release of snR30 by Rok1 helicase. EMBO Rep 9: 1230-6.
52. Anderson LE, (1954) Hoyer's Solution as a Rapid Permanent Mounting Medium for Bryophytes. The Bryologist 57: 242-244.
53. Sommer MS, Daum B, Gross LE, Weis BL, Mirus O, et al. (2011) Chloroplast Omp85 proteins change orientation during evolution. Proc Natl Acad Sci USA 108: 13841-6.
54. Sauer M, Paciorek T, Benkova E, Friml J, (2006) Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nature Protoc 1: 98-103.
55. Forreiter C, Kirschner M, Nover L, (1997) Stable transformation of an Arabidopsis cell suspension culture with firefly luciferase providing a cellular system for analysis of chaperone activity in vivo. Plant Cell 9: 2171-81.
56. Veith T, Martin R, Wurm JP, Weis B, Duchardt-Ferner E, et al. (2011) Structural and functional analysis of the archaeal endonuclease Nob1. Nucleic Acid Res 40: 3259-3274.
57. Im CH, Hwang SM, Son YS, Heo JB, Bang WY, et al. (2011) Nuclear/nucleolar GTPase 2 proteins as a subfamily of YlqF/YawGGTPases function in pre-60S ribosomal subunit maturation of mono- and dicotyledonous plants. J Biol Chem 286: 8620-32.
58. Brown JW, Shaw PJ, (1998) Small nucleolar RNAs and pre-rRNA processing in plants. Plant Cell 10: 649-57.
59. Fatica A, Oeffinger M, Dlakić M, Tollervey D, (2003) Nob1p is required for cleavage of the 3′ end of 18S rRNA. Mol Cell Biol 23: 1798-807.
60. Guo J, Jin Z, Yang X, Li JF, Chen JG, (2011) Eukaryotic initiation factor 6, an evolutionarily conserved regulator of ribosome biogenesis and protein translation. Plant Signal Behav 6: 766-71.
61. Bollenbach TJ, Lange H, Gutierrez R, Erhardt M, Stern DB, et al. (2005) RNR1, a 3′-5′ exoribonuclease belonging to the RNR superfamily, catalyzes 3′ maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana. Nucleic Acids Res 12: 2751-63.
62. Feldmann KA, Coury DA, Christianson ML, (1997) Exceptional segregation of a selectable marker (KanR) in Arabidopsis identifies genes important for gametophytic growth and development. Genetics 147: 1411-22.
63. Howden R, Park SK, Moore JM, Orme J, Grossniklaus U, et al. (1998) Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149: 621-31.
64. Yamamoto Y, Nishimura M, Hara-Nishimura I, Noguchi T, (2003) Behavior of vacuoles during microspore and pollen development in Arabidopsis thaliana. Plant Cell Physiol 44: 1192-201.
65. Roos J, Luz JM, Centoducati S, Sternglanz R, Lennarz WJ, (1997) ENP1, an essential gene encoding a nuclear protein that is highly conserved from yeast to humans. Gene 185: 137-46.
66. Campbell MG, Karbstein K, (2011) Protein-protein interactions within late pre-40S ribosomes. PLoS One 6: e16194.
67. Liu J, Qu LJ, (2008) Meiotic and mitotic cell cycle mutants involved in gametophyte development in Arabidopsis. Mol Plant 1: 564-74.
68. Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, et al. (2005) SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17: 2340-54.
69. Raissig MT, Baroux C, Grossniklaus U, (2011) Regulation and flexibility of genomic imprinting during seed development. Plant Cell. 23: 16-26.