title: The Arabidopsis eukaryotic translation initiation factor 3, subunit F (AteIF3f), is required for pollen germination and embryogenesis.
abstract: Previous studies have shown that subunits E (eIF3e), F (eIF3f) and H (elF3h) of eukaryotic translation initiation factor 3 play important roles in cell development in humans and yeast. eIF3e and eIF3h have also been reported to be important for normal cell growth in Arabidopsis. However, the functions of subunit eIF3f remain largely unknown in plant species. Here we report characterization of mutants for the Arabidopsis eIF3f (AteIF3f) gene. AteIF3f encodes a protein that is highly expressed in pollen grains, developing embryos and root tips, and interacts with Arabidopsis eIF3e and eIF3h proteins. A Ds insertional mutation in AteIF3f disrupted pollen germination and embryo development. Expression of some of the genes that are essential for pollen tube growth and embryogenesis is down-regulated in ateif3f-1 homozygous seedlings obtained by pollen rescue. These results suggested that AteIF3f might play important roles in Arabidopsis cell growth and differentiation in combination with eIF3e and eIF3h.
authors.affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
authors.forename: Chuan
authors.initials: C
authors.lastname: Xia
authors.affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
authors.forename: Yu-Jiao
authors.initials: YJ
authors.lastname: Wang
authors.affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
authors.forename: Wen-Qing
authors.initials: WQ
authors.lastname: Li
authors.affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
authors.forename: Yi-Ran
authors.initials: YR
authors.lastname: Chen
authors.affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
authors.forename: Yi
authors.initials: Y
authors.lastname: Deng
authors.affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
authors.forename: Xue-Qin
authors.initials: XQ
authors.lastname: Zhang
authors.affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
authors.forename: Li-Qun
authors.initials: LQ
authors.lastname: Chen
authors.affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.|National Center for Plant Gene Research (Beijing), Beijing 100101, China.
authors.forename: De
authors.lastname: Ye
mesh_terms: D017360:Arabidopsis / Q000196:embryology* / Q000235:genetics; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D004269:DNA, Bacterial / Q000235:genetics; D039621:Eukaryotic Initiation Factor-3 / Q000235:genetics / Q000378:metabolism*; D020869:Gene Expression Profiling; D018507:Gene Expression Regulation, Developmental; D018506:Gene Expression Regulation, Plant; D005816:Genetic Complementation Test; D018525:Germination; D016254:Mutagenesis, Insertional; D009154:Mutation; D020411:Oligonucleotide Array Sequence Analysis; D011058:Pollen / Q000254:growth & development*; D018749:RNA, Plant / Q000235:genetics
chemical_list: D029681:Arabidopsis Proteins; D004269:DNA, Bacterial; D039621:Eukaryotic Initiation Factor-3; D018749:RNA, Plant; C036483:T-DNA
references.citation: Albrecht, V., Ingenfeld, A. and 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.
references.citation: Asano, K., Kinzy, T.G., Merrick, W.C. and Hershey, J.W. (1997a) Conservation and diversity of eukaryotic translation initiation factor eIF3. J. Biol. Chem. 272, 1101-1109.
references.citation: Asano, K., Vornlocher, H.P., Richter-Cook, N.J., Merrick, W.C., Hinnebusch, A.G. and 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.
references.citation: Asano, K., Phan, L., Anderson, J. and 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.
references.citation: Bandyopadhyay, A., Matsumoto, T. and 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.
references.citation: Bechtold, N. and Pelletier, G. (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82, 259-266.
references.citation: Burks, E.A., Bezerra, P.P., Le, H., Gallie, D.R. and 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.
references.citation: Chang, E.C. and Schwechheimer, C. (2004) ZOMES III: the interface between signalling and proteolysis. EMBO Rep. 5, 1041-1045.
references.citation: Chaudhuri, J., Chowdhury, D. and 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.
references.citation: Csibi, A., Tintignac, L.A., Leibovitch, M.P. and Leibovitch, S.A. (2008) eIF3-f function in skeletal muscles: to stand at the crossroads of atrophy and hypertrophy. Cell Cycle, 7, 1698-1701.
references.citation: Dever, T.E. (2002) Gene-specific regulation by general translation factors. Cell, 108, 545-556.
references.citation: Doldan, A., Chandramouli, A., Shanas, R., Bhattacharyya, A., Cunningham, J.T., Nelson, M.A. and Shi, J. (2008a) Loss of the eukaryotic initiation factor 3f in pancreatic cancer. Mol. Carcinog. 47, 235-244.
references.citation: Doldan, A., Chandramouli, A., Shanas, R., Bhattacharyya, A., Leong, S.P., Nelson, M.A. and Shi, J. (2008b) Loss of the eukaryotic initiation factor 3f in melanoma. Mol. Carcinog. 47, 806-813.
references.citation: Dumas, C. and Gaude, T. (2006) Fertilization in plants: is calcium a key player? Semin. Cell Dev. Biol. 17, 244-253.
references.citation: Espineda, C.E., Linford, A.S., Devine, D. and 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.
references.citation: Goubet, F., Misrahi, A., Park, S.K., Zhang, Z., Twell, D. and 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.
references.citation: Hanson, J., Hanssen, M., Wiese, A., Hendriks, M.M. and 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.
references.citation: Harris, T.E., Chi, A., Shabanowitz, J., Hunt, D.F., Rhoads, R.E. and Lawrence, J.C. Jr (2006) mTOR-dependent stimulation of the association of eIF4G and eIF3 by insulin. EMBO J. 25, 1659-1668.
references.citation: Hinnebusch, A.G. (2006) eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem. Sci. 31, 553-562.
references.citation: Hofmann, K. and Bucher, P. (1998) The PCI domain: a common theme in three multiprotein complexes. Trends Biochem. Sci. 23, 204-205.
references.citation: Holz, M.K., Ballif, B.A., Gygi, S.P. and 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.
references.citation: Huang, X., Hetfeld, B.K., Seifert, U., Kahne, T., Kloetzel, P.M., Naumann, M., Bech-Otschir, D. and Dubiel, W. (2005) Consequences of COP9 signalosome and 26S proteasome interaction. FEBS J. 272, 3909-3917.
references.citation: Jiang, L., Yang, S.L., Xie, L.F., Puah, C.S., Zhang, X.Q., Yang, W.C., Sundaresan, V. and 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.
references.citation: Karniol, B., Yahalom, A., Kwok, S., Tsuge, T., Matsui, M., Deng, X.W. and Chamovitz, D.A. (1998) The Arabidopsis homologue of an eIF3 complex subunit associates with the COP9 complex. FEBS Lett. 439, 173-179.
references.citation: Kawaguchi, R. and Bailey-Serres, J. (2002) Regulation of translational initiation in plants. Curr. Opin. Plant Biol. 5, 460-465.
references.citation: Kim, T., Hofmann, K., von Arnim, A.G. and Chamovitz, D.A. (2001) PCI complexes: pretty complex interactions in diverse signaling pathways. Trends Plant Sci. 6, 379-386.
references.citation: Kim, T.H., Kim, B.H., Yahalom, A., Chamovitz, D.A. and 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.
references.citation: Kim, B.H., Cai, X., Vaughn, J.N. and 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.
references.citation: Kolupaeva, V.G., Unbehaun, A., Lomakin, I.B., Hellen, C.U. and 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.
references.citation: Krichevsky, A., Kozlovsky, S.V., Tian, G.W., Chen, M.H., Zaltsman, A. and Citovsky, V. (2007) How pollen tubes grow. Dev. Biol. 303, 405-420.
references.citation: Liu, Y.G. and 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.
references.citation: Liu, Y.G., Mitsukawa, N., Oosumi, T. and 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.
references.citation: Lukaszewicz, M., Feuermann, M., Jerouville, B., Stas, A. and Boutry, M. (2000) In vivo evaluation of the context sequence of the translation initiation codon in plants. Plant Sci. 154, 89-98.
references.citation: Malho, R., Liu, Q., Monteiro, D., Rato, C., Camacho, L. and Dinis, A. (2006) Signalling pathways in pollen germination and tube growth. Protoplasma, 228, 21-30.
references.citation: Masutani, M., Sonenberg, N., Yokoyama, S. and Imataka, H. (2007) Reconstitution reveals the functional core of mammalian eIF3. EMBO J. 26, 3373-3383.
references.citation: Muschietti, J., Dircks, L., Vancanneyt, G. and 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.
references.citation: Nielsen, K.H., Szamecz, B., Valasek, L., Jivotovskaya, A., Shin, B.S. and Hinnebusch, A.G. (2004) Functions of eIF3 downstream of 48S assembly impact AUG recognition and GCN4 translational control. EMBO J. 23, 1166-1177.
references.citation: Preuss, D., Rhee, S.Y. and Davis, R.W. (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science, 264, 1458-1460.
references.citation: Ray, A., Bandyopadhyay, A., Matsumoto, T., Deng, H. and 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.
references.citation: Rook, F., Gerrits, N., Kortstee, A., van Kampen, M., Borrias, M., Weisbeek, P. and Smeekens, S. (1998) Sucrose-specific signalling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J. 15, 253-263.
references.citation: Scheel, H. and Hofmann, K. (2005) Prediction of a common structural scaffold for proteasome lid, COP9-signalosome and eIF3 complexes. BMC Bioinformatics, 6, 71.
references.citation: Shi, J., Feng, Y., Goulet, A.C., Vaillancourt, R.R., Sachs, N.A., Hershey, J.W. and 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.
references.citation: Shi, J., Kahle, A., Hershey, J.W., Honchak, B.M., Warneke, J.A., Leong, S.P. and Nelson, M.A. (2006) Decreased expression of eukaryotic initiation factor 3f deregulates translation and apoptosis in tumor cells. Oncogene, 25, 4923-4936.
references.citation: Shi, J., Hershey, J.W. and Nelson, M.A. (2009) Phosphorylation of the eukaryotic initiation factor 3f by cyclin-dependent kinase 11 during apoptosis. FEBS Lett. 583, 971-977.
references.citation: Sonenberg, N., Hershey, J.W.B. and Mathews, M. (2000) Translational Control of Gene Expression, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
references.citation: Sundaresan, V., Springer, P., Volpe, T., Haward, S., Jones, J.D., Dean, C., Ma, H. and Martienssen, R. (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9, 1797-1810.
references.citation: Valasek, L., Nielsen, K.H., Zhang, F., Fekete, C.A. and 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.
references.citation: Wettenhall, J.M., Simpson, K.M., Satterley, K. and Smyth, G.K. (2006) affylmGUI: a graphical user interface for linear modeling of single channel microarray data. Bioinformatics, 22, 897-899.
references.citation: Wiese, A., Elzinga, N., Wobbes, B. and Smeekens, S. (2004) A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell, 16, 1717-1729.
references.citation: Xiao, H., Xu, L.H., Yamada, Y. and Liu, D.X. (2008) Coronavirus spike protein inhibits host cell translation by interaction with eIF3f. PLoS ONE, 3, e1494.
references.citation: Xu, X.M. and 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.
references.citation: Yahalom, A., Kim, T.H., Winter, E., Karniol, B., von Arnim, A.G. and Chamovitz, D.A. (2001) Arabidopsis eIF3e associates with both eIF3c (INT-6) and the COP9 signalosome subunit CSN7. J. Biol. Chem. 276, 334-340.
references.citation: Yahalom, A., Kim, T.H., Roy, B., Singer, R., von Arnim, A.G. and 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.
references.citation: Yamasato, A., Tanaka, R. and 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.
references.citation: Yang, W.C., Ye, D., Xu, J. and 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.
references.citation: Zhou, C., Arslan, F., Wee, S., Krishnan, S., Ivanov, A.R., Oliva, A., Leatherwood, J. and Wolf, D.A. (2005) PCI proteins eIF3e and eIF3m define distinct translation initiation factor 3 complexes. BMC Biol. 3, 14.
references.citation: 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.