The Arabidopsis eukaryotic translation initiation factor 3, subunit F (AteIF3f), is required for pollen germination and embryogenesis

Plant Journal

Volumn 63, Issue 2, 2010, Pages 189-202

  Xia, Chuan ^a   Wang, Yu Jiao ^a   Li, Wen Qing ^a   Chen, Yi Ran ^a   Deng, Yi ^a   Zhang, Xue Qin ^a   Chen, Li Qun ^a   Ye, De ^a,b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

Arabidopsis; AteIF3f; embryogenesis; male gametophyte; MPN domain; translation initiation

Indexed keywords

ARABIDOPSIS; EMBRYO DEVELOPMENT; EUKARYOTIC TRANSLATION; IN-CELL; IN-PLANTS; INITIATION FACTORS; MALE GAMETOPHYTES; POLLEN GERMINATION; POLLEN GRAINS; POLLEN TUBE GROWTH; ROOT TIP;

CELL GROWTH; GROWTH KINETICS; PROTEINS;

GENE EXPRESSION;

ARABIDOPSIS PROTEIN; BACTERIAL DNA; INITIATION FACTOR 3; PLANT RNA; T DNA; T-DNA;

ARABIDOPSIS; ARTICLE; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; POLLEN; PRENATAL DEVELOPMENT; EMBRYOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA, BACTERIAL; EUKARYOTIC INITIATION FACTOR-3; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; GERMINATION; MUTAGENESIS, INSERTIONAL; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLLEN; RNA, PLANT;

ARABIDOPSIS; EUKARYOTA;

EID: 77954440023     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04237.x     Document Type: Article

References (57)

1. Albrecht, V., Ingenfeld, A. Apel, K. (2006) Characterization of the snowy cotyledon 1 mutant of Arabidopsis thaliana: the impact of chloroplast elongation factor G on chloroplast development and plant vitality. Plant Mol. Biol. 60, 507 518.
2. Asano, K., Kinzy, T.G., Merrick, W.C. Hershey, J.W. (1997a) Conservation and diversity of eukaryotic translation initiation factor eIF3. J. Biol. Chem. 272, 1101 1109.
3. Asano, K., Vornlocher, H.P., Richter-Cook, N.J., Merrick, W.C., Hinnebusch, A.G. Hershey, J.W. (1997b) Structure of cDNAs encoding human eukaryotic initiation factor 3 subunits. Possible roles in RNA binding and macromolecular assembly. J. Biol. Chem. 272, 27042 27052.
4. Asano, K., Phan, L., Anderson, J. Hinnebusch, A.G. (1998) Complex formation by all five homologues of mammalian translation initiation factor 3 subunits from yeast Saccharomyces cerevisiae. J. Biol. Chem. 273, 18573 18585.
5. Bandyopadhyay, A., Matsumoto, T. Maitra, U. (2000) Fission yeast Int6 is not essential for global translation initiation, but deletion of int6(+) causes hypersensitivity to caffeine and affects spore formation. Mol. Biol. Cell, 11, 4005 4018.
6. Bechtold, N. Pelletier, G. (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82, 259 266.
7. Burks, E.A., Bezerra, P.P., Le, H., Gallie, D.R. Browning, K.S. (2001) Plant initiation factor 3 subunit composition resembles mammalian initiation factor 3 and has a novel subunit. J. Biol. Chem. 276, 2122 2131.
8. Chang, E.C. Schwechheimer, C. (2004) ZOMES III: the interface between signalling and proteolysis. EMBO Rep. 5, 1041 1045.
9. Chaudhuri, J., Chowdhury, D. Maitra, U. (1999) Distinct functions of eukaryotic translation initiation factors eIF1A and eIF3 in the formation of the 40S ribosomal preinitiation complex. J. Biol. Chem. 274, 17975 17980.
10. Csibi, A., Tintignac, L.A., Leibovitch, M.P. Leibovitch, S.A. (2008) eIF3-f function in skeletal muscles: to stand at the crossroads of atrophy and hypertrophy. Cell Cycle, 7, 1698 1701. (Pubitemid 351988733)
11. Dever, T.E. (2002) Gene-specific regulation by general translation factors. Cell, 108, 545 556.
12. Doldan, A., Chandramouli, A., Shanas, R., Bhattacharyya, A., Cunningham, J.T., Nelson, M.A. Shi, J. (2008a) Loss of the eukaryotic initiation factor 3f in pancreatic cancer. Mol. Carcinog. 47, 235 244.
13. Doldan, A., Chandramouli, A., Shanas, R., Bhattacharyya, A., Leong, S.P., Nelson, M.A. Shi, J. (2008b) Loss of the eukaryotic initiation factor 3f in melanoma. Mol. Carcinog. 47, 806 813.
14. Dumas, C. Gaude, T. (2006) Fertilization in plants: is calcium a key player? Semin. Cell Dev. Biol. 17, 244 253.
15. Espineda, C.E., Linford, A.S., Devine, D. Brusslan, J.A. (1999) The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 96, 10507 10511.
16. Goubet, F., Misrahi, A., Park, S.K., Zhang, Z., Twell, D. Dupree, P. (2003) AtCSLA7, a cellulose synthase-like putative glycosyltransferase, is important for pollen tube growth and embryogenesis in Arabidopsis. Plant Physiol. 131, 547 557.
17. Hanson, J., Hanssen, M., Wiese, A., Hendriks, M.M. Smeekens, S. (2008) The sucrose-regulated transcription factor bZIP11 affects amino acid metabolism by regulating the expression of ASPARAGINE SYNTHETASE1 and PROLINE DEHYDROGENASE2. Plant J. 53, 935 949.
18. Harris, T.E., Chi, A., Shabanowitz, J., Hunt, D.F., Rhoads, R.E. Lawrence, J.C. Jr. (2006) mTOR-dependent stimulation of the association of eIF4G and eIF3 by insulin. EMBO J. 25, 1659 1668.
19. Hinnebusch, A.G. (2006) eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem. Sci. 31, 553 562.
20. Hofmann, K. Bucher, P. (1998) The PCI domain: a common theme in three multiprotein complexes. Trends Biochem. Sci. 23, 204 205.
21. Holz, M.K., Ballif, B.A., Gygi, S.P. Blenis, J. (2005) mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell, 123, 569 580.
22. Huang, X., Hetfeld, B.K., Seifert, U., Kahne, T., Kloetzel, P.M., Naumann, M., Bech-Otschir, D. Dubiel, W. (2005) Consequences of COP9 signalosome and 26S proteasome interaction. FEBS J. 272, 3909 3917.
23. Jiang, L., Yang, S.L., Xie, L.F., Puah, C.S., Zhang, X.Q., Yang, W.C., Sundaresan, V. Ye, D. (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell, 17, 584 596.
24. Karniol, B., Yahalom, A., Kwok, S., Tsuge, T., Matsui, M., Deng, X.W. Chamovitz, D.A. (1998) The Arabidopsis homologue of an eIF3 complex subunit associates with the COP9 complex. FEBS Lett. 439, 173 179.
25. Kawaguchi, R. Bailey-Serres, J. (2002) Regulation of translational initiation in plants. Curr. Opin. Plant Biol. 5, 460 465.
26. Kim, T., Hofmann, K., von Arnim, A.G. Chamovitz, D.A. (2001) PCI complexes: pretty complex interactions in diverse signaling pathways. Trends Plant Sci. 6, 379 386.
27. Kim, T.H., Kim, B.H., Yahalom, A., Chamovitz, D.A. von Arnim, A.G. (2004) Translational regulation via 5′ mRNA leader sequences revealed by mutational analysis of the Arabidopsis translation initiation factor subunit eIF3h. Plant Cell, 16, 3341 3356.
28. Kim, B.H., Cai, X., Vaughn, J.N. von Arnim, A.G. (2007) On the functions of the h subunit of eukaryotic initiation factor 3 in late stages of translation initiation. Genome Biol. 8, R60.
29. Kolupaeva, V.G., Unbehaun, A., Lomakin, I.B., Hellen, C.U. Pestova, T.V. (2005) Binding of eukaryotic initiation factor 3 to ribosomal 40S subunits and its role in ribosomal dissociation and anti-association. RNA, 11, 470 486.
30. Krichevsky, A., Kozlovsky, S.V., Tian, G.W., Chen, M.H., Zaltsman, A. Citovsky, V. (2007) How pollen tubes grow. Dev. Biol. 303, 405 420.
31. Liu, Y.G. Whittier, R.F. (1995) Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics, 25, 674 681.
32. Liu, Y.G., Mitsukawa, N., Oosumi, T. Whittier, R.F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457 463.
33. Lukaszewicz, M., Feuermann, M., Jerouville, B., Stas, A. Boutry, M. (2000) In vivo evaluation of the context sequence of the translation initiation codon in plants. Plant Sci. 154, 89 98.
34. Malho, R., Liu, Q., Monteiro, D., Rato, C., Camacho, L. Dinis, A. (2006) Signalling pathways in pollen germination and tube growth. Protoplasma, 228, 21 30.
35. Masutani, M., Sonenberg, N., Yokoyama, S. Imataka, H. (2007) Reconstitution reveals the functional core of mammalian eIF3. EMBO J. 26, 3373 3383.
36. Muschietti, J., Dircks, L., Vancanneyt, G. McCormick, S. (1994) LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. Plant J. 6, 321 338. (Pubitemid 124000387)
37. Nielsen, K.H., Szamecz, B., Valasek, L., Jivotovskaya, A., Shin, B.S. Hinnebusch, A.G. (2004) Functions of eIF3 downstream of 48S assembly impact AUG recognition and GCN4 translational control. EMBO J. 23, 1166 1177.
38. Preuss, D., Rhee, S.Y. Davis, R.W. (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science, 264, 1458 1460.
39. Ray, A., Bandyopadhyay, A., Matsumoto, T., Deng, H. Maitra, U. (2008) Fission yeast translation initiation factor 3 subunit eIF3h is not essential for global translation initiation, but deletion of eif3h+ affects spore formation. Yeast, 25, 809 823.
40. Rook, F., Gerrits, N., Kortstee, A., van Kampen, M., Borrias, M., Weisbeek, P. Smeekens, S. (1998) Sucrose-specific signalling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J. 15, 253 263.
41. Scheel, H. Hofmann, K. (2005) Prediction of a common structural scaffold for proteasome lid, COP9-signalosome and eIF3 complexes. BMC Bioinformatics, 6, 71.
42. Shi, J., Feng, Y., Goulet, A.C., Vaillancourt, R.R., Sachs, N.A., Hershey, J.W. Nelson, M.A. (2003) The p34cdc2-related cyclin-dependent kinase 11 interacts with the p47 subunit of eukaryotic initiation factor 3 during apoptosis. J. Biol. Chem. 278, 5062 5071.
43. Shi, J., Kahle, A., Hershey, J.W., Honchak, B.M., Warneke, J.A., Leong, S.P. Nelson, M.A. (2006) Decreased expression of eukaryotic initiation factor 3f deregulates translation and apoptosis in tumor cells. Oncogene, 25, 4923 4936.
44. Shi, J., Hershey, J.W. Nelson, M.A. (2009) Phosphorylation of the eukaryotic initiation factor 3f by cyclin-dependent kinase 11 during apoptosis. FEBS Lett. 583, 971 977.
45. Sonenberg, N., Hershey, J.W.B. Mathews, M. (2000) Translational Control of Gene Expression, 2nd edn.
46. Sundaresan, V., Springer, P., Volpe, T., Haward, S., Jones, J.D., Dean, C., Ma, H. Martienssen, R. (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9, 1797 1810.
47. Valasek, L., Nielsen, K.H., Zhang, F., Fekete, C.A. Hinnebusch, A.G. (2004) Interactions of eukaryotic translation initiation factor 3 (eIF3) subunit NIP1/c with eIF1 and eIF5 promote preinitiation complex assembly and regulate start codon selection. Mol. Cell. Biol. 24, 9437 9455.
48. Wettenhall, J.M., Simpson, K.M., Satterley, K. Smyth, G.K. (2006) affylmGUI: a graphical user interface for linear modeling of single channel microarray data. Bioinformatics, 22, 897 899.
49. Wiese, A., Elzinga, N., Wobbes, B. Smeekens, S. (2004) A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell, 16, 1717 1729.
50. Xiao, H., Xu, L.H., Yamada, Y. Liu, D.X. (2008) Coronavirus spike protein inhibits host cell translation by interaction with eIF3f. PLoS ONE, 3, e1494.
51. Xu, X.M. Moller, S.G. (2004) AtNAP7 is a plastidic SufC-like ATP-binding cassette/ATPase essential for Arabidopsis embryogenesis. Proc. Natl Acad. Sci. USA, 101, 9143 9148.
52. Yahalom, A., Kim, T.H., Winter, E., Karniol, B., von Arnim, A.G. Chamovitz, D.A. (2001) Arabidopsis eIF3e associates with both eIF3c (INT-6) and the COP9 signalosome subunit CSN7. J. Biol. Chem. 276, 334 340.
53. Yahalom, A., Kim, T.H., Roy, B., Singer, R., von Arnim, A.G. Chamovitz, D.A. (2008) Arabidopsis eIF3e is regulated by the COP9 signalosome and has an impact on development and protein translation. Plant J. 53, 300 311.
54. Yamasato, A., Tanaka, R. Tanaka, A. (2008) Loss of the N-terminal domain of chlorophyllide a oxygenase induces photodamage during greening of Arabidopsis seedlings. BMC Plant Biol. 8, 64.
55. Yang, W.C., Ye, D., Xu, J. Sundaresan, V. (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13, 2108 2117.
56. Zhou, C., Arslan, F., Wee, S., Krishnan, S., Ivanov, A.R., Oliva, A., Leatherwood, J. Wolf, D.A. (2005) PCI proteins eIF3e and eIF3m define distinct translation initiation factor 3 complexes. BMC Biol. 3, 14.
57. Zhou, M., Sandercock, A.M., Fraser, C.S. et al. (2008) Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc. Natl Acad. Sci. USA, 105, 18139 18144.