Abstract
A predominantly plant-based family of genes encoding RNA binding proteins is defined by the presence of a highly conserved RNA binding motif first described in the mei2 gene of the fission yeast Schizosaccharomyces pombe. In silico analyses reveal nine mei2-like genes in Arabidopsis thaliana and six in Oryza sativa. These predicted genes group into four distinct clades, based on overall sequence similarity and subfamily-specific sequence elements. In situ analysis show that Arabidopsis genes from one of these clades, TEL1 and TEL2, are specifically expressed in central zone of the shoot apical meristem and the quiescent center of the root apical meristem, suggesting that they may somehow function to maintain indeterminacy in these tissues. By contrast, members of two sister clades, AML1 through AML5, are expressed more broadly, a trend that was confirmed by Q-PCR analysis. mei2-like transcripts with similar sequences showed similar expression patterns, suggesting functional redundancy within the four clades. Phenotypic analyses of lines that contain T-DNA insertions to individual mei2-like genes reveal no obvious phenotypes, further suggesting redundant activities for these gene products.
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References
AGI. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
Altschul, S., Madden, T., Schäffer, A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
Birney, E., Kumar, S. and Krainer, A. 1993. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 21: 5803-5816.
Bozdech, Z., Zhu, J., Joachimiak, M.P., Cohen, F.E., Pulliam, B. and DeRisi, J.L. 2003. Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a longoligonucleotide microarray. Genome Biol. 4(2).
Burd, C. and Dreyfuss, G. 1994. Conserved structures and diversity of functions of RNA-binding proteins. Science 265: 615-621.
Casamitjana-Martinez, E., Hofhuis, H., Xu, J., Liu, C., Heidstra, R. and Scheres, B. 2003. Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr. Biol. 13: 1435-1441.
Crespi, M.D., Jurkevitch, E., Poiret, M., d'Aubenton-Carafa, Y., Petrovics, G., Kondorosi, E. and Kondorosi, A. 1994. enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO 13: 5099-5112.
de la Fuente van Bentem, S., Vossen, J.H., Vermeer, J.E., de Vroomen, M.J., Gadella, T.W. Jr., Haring, M.A. and Cornelissen, B.J. 2003. The subcellular localization of plant protein phosphatase 5 isoforms is determined by alternative splicing. Plant Physiol. 133: 702-712.
Goff, S.A., Ricke, D., Lan, T.H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H, et al. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296(5565): 92-100.
Guhaniyogi, J. and Brewer, G. 2001. Regulation of mRNA stability in mammalian cells. Gene 265: 11-23.
Hirayama, T., Ishida, C., Kuromori, T., Obata, S., Shimoda, C., Yamamoto, M., Shinozaki, K. and Ohto, C. 1997. Functional cloning of a cDNA encoding Mei2-like protein from Arabidopsis thaliana using a fission yeast pheromone receptor deficient mutant. FEBS Lett. 413: 16-20.
Hobe, M., Muller, R., Grunewald, M., Brand, U. and Simon, R. 2003. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev. Genes Evol. 213: 371-381.
Hunter, C. and Poethig, R.S. 2003. miSSING LINKS: miRNAs and plant development. Curr. Opin. Genet. Dev. 13: 372-378.
Jackson, D., Veit, B. and Hake, S. 1994. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405-413.
Jasinski, S., Perennes, C., Bergounioux, C. and Glab, N. 2002. Comparative molecular and functional analyses of the tobacco cyclin-dependent kinase inhibitor NtKIS1a and its spliced variant NtKIS1b. Plant Physiol. 130: 1871-1882.
Jeffares, D.C., Phillips, M.J., Moore, S. and Veit, B. 2004. A description of the Mei2-like protein family; structure, phylogenetic distribution and biological context. Dev. Genes Evol. 214(3): 149-158.
Kamiya, N., Nagasaki, H., Morikami, A., Sato, Y. and Matsuoka, M. 2003. Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J. 35: 429-441.
Kaya, H., Shibahara, K.I., Taoka, K.I., Iwabuchi, M., Stillman, B. and Araki, T. 2001. FASCIATA genes for Chromatin Assembly Factor-1 in arabidopsis maintain the cellular organization of apical meristems. Cell 104: 131-142.
Kazan, K. 2003. Alternative splicing and proteome diversity in plants: the tip of the iceberg has just emerged. Trends Plant Sci. 8: 468-471.
Keddie, J.S., Carrol, B.J., Thomas, C., Reyes, M., Klimyuk, V., Holtan, H., Gruissem, W. and Jones, J.D. 1998. Transposon tagging of the Defective embryo and meristems gene of tomato. Plant Cell 10: 877-888.
Kikuchi, S., Satoh, K., Nagata, T., Kawagashira, N. Doi, K., Kishimoto, N., Yazaki, J., Ishikawa, M., Yamada, H., Ooka, H., et al. 2003. Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301: 376-379.
Le Roch, K.G., Zhou, Y., Blair, P.L., Grainger, M., Moch, J.K., Haynes, J.D., De La Vega, P., Holder, A.A., Batalov, S., Carucci, D.J., et al., 2003. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503-1508.
Li, P. and McLeod, M. 1996. Molecular mimicry in development: identification of ste11 + as a substrate and mei3 + as a pseudosubstrate inhibitor of ran1 + kinase. Cell 87: 869-880.
Lopato, S., Kalyna, M., Dorner, S., Kobayashi, R., Krainer, A. R. and Barta, A. 1999. atSRp30, one of two SF2/ASF-like proteins from Arabidopsis thaliana, regulates splicing of specific plant genes. Genes Dev. 13: 987-1001.
Lorković, Z.J. and Barta, A. 2002. Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res. 30: 623-635.
MacIntosh, G., Wilkerson, C. and Green, P. 2001. Identification and analysis of Arabidopsis expressed sequence tags characteristic of non-coding RNAs. Plant Physiol. 127: 765-776.
Macknight, R., Bancroft, I., Page, T., Lister, C., Schmidt, R., Love, K., Westphal, L., Murphy, G., Sherson, S., Cobbett, C., et al. 1997. FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89(5): 737-745.
Macknight, R., Duroux, M., Laurie, R., Dijkwel, P., Simpson, G., Dean, C. 2002. Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA. Plant Cell 14: 877-888.
Mallory, A.C. and Vaucheret, H. 2004. MicroRNAs: something important between the genes. Curr. Opin. Plant Biol. 7: 120-125.
Mano, S., Hayashi, M. and Nishimura, M. 1999. Light regulates alternative splicing of hydroxypyruvate reductase in pumpkin. Plant J. 17: 309-320.
McLeod, M. and Beach, D. 1988. A specific inhibitor of ran1 + protein kinase regulates entry into meiosis in Schizosaccharomyces pombe. Nature 322: 509-514.
Mizuno, K., Hasemi, T., Ubukata, T., Yamada, T., Lehmann, E., Kohli, J., Watanabe, Y., Iino, Y., Yamamoto, M., Fox, M.E., et al. 2001. Counteracting regulation of chromatin remodeling at a fission yeast cAMP response element-related recombination hotspot by stress-activated protein kinase, cAMP-dependent kinase and meiosis regulators. Genetics 159: 1467-1478.
Nicholas, K.B., Nicholas, H.B.J. and Deerfield, D.W.I. 1997. GeneDoc: analysis and visualization of genetic variation. EMBNEW.NEWS 4: 14.
Page, R.D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12: 357-358.
Quesada, V., Macknight, R., Dean, C. and Simpson, G.G. 2003. Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. EMBO 22: 3142-3152.
Reddy, A.S.N. 2001. Nuclear pre-mRNA splicing in plants. Criti. Rev. Plant Sci. 20: 523-571.
Savaldi-Goldstein, S., Aviv, D., Davydov, O. and Fluhr, R. 2003. Alternative splicing modulation by a LAMMER kinase impinges on developmental and transcriptome expression. Plant Cell 15: 926-938.
Shimada, T., Yamashita, A. and Yamamoto, M. 2003. The fission yeast meiotic regulator Mei2p forms a dot structure in the horse-tail nucleus in association with the sme2 locus on chromosome II. Mol. Biol. Cell 14: 2461-2469.
Simpson, G.G. and Filipowicz, W. 1996. Splicing of precursors to mRNA in higher plants: mechanism, regulation and subnuclear organisation of the spliceosomal machinery. Plant Mol. Biol. 32: 1-41.
Small, I.D. and Peeters, N. 2000. The PPR motif — a TPRrelated motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25: 46-47.
Staiger, D., Zecca, L., Wieczorek Kirk, D.A., Apel, K. and Eckstein, L. 2003. The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J. 33: 361-371.
Taylor, C. and Green, P. 1995. Identification and characterization of genes with unstable transcripts (GUTs) in tobacco. Plant Mol. Biol. 28: 27-38.
Teramoto, H., Toyama, T., Takeba, G. and Tsuji, H. 1995. Changes in expression of two cytokinin-repressed genes, CR9 and CR20, in relation to aging, greening, and wounding in cucumber. Planta 196: 387-395.
Teramoto, H., Toyama, T., Takeba, G. and Tsuji, H. 1996. Noncoding RNA for CR20, a cytokinin-repressed gene of cucumber. Plant Mol. Biol. 32: 797-808.
van Hoof, A., J.P, K., C.B, T. and P.J, G. 1997. GUT15 cDNAs from tobacco (accession no. U84972) and Arabidopsis (accession no. U84973) correspond to transcripts with unusual metabolism and a short conserved ORF. Plant Physiol. 113: 1004.
Veit, B. 2004. Determination of cell fate in apical meristems. Curr. Opin. Plant Biol. 7: 57-64.
Veit, B., Briggs, S., Schmidt, R., Yanofsky, M. and Hake, S. 1998. Regulation of leaf initiation by the terminal ear 1 gene of maize. Nature 393: 166-168.
Volpe, T., Schramke, V., Hamilton, G.L., White, S.A., Teng, G., Martienssen, R.A. and Allshire, R.C. 2003. RNA interference is required for normal centromere function in fission yeast. Chromosome Res. 11: 137-146.
Watanabe, Y., Iino, Y., Furuhata, K., Shimoda, C. and Yamamoto, H. 1988. The S. pombe mei2+ gene encoding a crucial molecule for commitment to meiosis is under the regulation of cAMP. EMBO J. 7: 761-767.
Watanabe, Y., Shinozake-Yabana, S., Chikashige, Y., hiraoka, Y. and Yamamoto, M. 1997. Phosphorylation of RNAbinding protein controls cell cycle switch from mitotic to meiotic in fission yeast. Nature 387: 187-190.
Watanabe, Y. and Yamamoto, M. 1994. S. pombe mei2+ encodes an RNA-binding protein essential for premeiotic DNA synthesis and meiosis I, which cooperates with a novel RNA species meiRNA. Cell 78: 487-498.
Yamashita, A., Watanabe, Y., Nulina, N. and Yamamoto, M. 1998. RNA-assisted nuclear transport of the meiotic regulator Mei2p in fission yeast. Cell 95: 115-123.
Yu, J., Hu, S., Wang, J., Wong, G.K., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., Zhang, X., et al. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 79-92.
Zhang, X.C. and Gassmann, W. 2003. RPS4-mediated disease resistance requires the combined presence of RPS4 transcripts with full-length and truncated open reading frames. Plant Cell 15: 2333-2342.
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Anderson, G.H., Alvarez, N.D., Gilman, C. et al. Diversification of Genes Encoding Mei2-Like RNA Binding Proteins in Plants. Plant Mol Biol 54, 653–670 (2004). https://doi.org/10.1023/B:PLAN.0000040819.33383.b6
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DOI: https://doi.org/10.1023/B:PLAN.0000040819.33383.b6