Alternative splicing at the o2Italian locus in maize: one mutation, two proteins
Tóm tắt
Opaque2 is a basic leucine-zipper transcription factor that regulates the expression of several genes involved in the development of maize endosperm. Among the different mutations so far characterized, the o2Italian (o2It) allele has a genomic deletion of 10 bp that interrupts the open reading frame by a premature stop codon. Curiously, the o2It allele still encodes a long o2 isoform (o2It-L) that is recognized by an O2 carboxy-terminal antibody, evidencing that this protein is similar to the wild type isoform. To clarify this phenomenon, we characterized the transcripts generated from the o2It allele and found two transcripts that are produced in a 1:1 ratio. The first transcript carried the 10 bp deletion and matched the genomic sequence of the o2It allele, whereas the second one carried a 15 bp deletion as a result of a 3’ alternative splicing site. The lack of five additional nucleotides restored the correct reading frame and explained the nature of the o2It-L polypeptide. The production of two distinct transcripts from the o2It allele was probably due to the recruitment of different splicing factors as suggested by in silico analysis of the o2It-mutated region. This finding evidences how the recruitment of splicing factors is tightly linked to nucleotide motives that should be present in correct neighboring contexts.
Tài liệu tham khảo
Baum, M., Beier, H.: Wheat cytoplasmic arginine tRNA isoacceptor with a U*CG anticodon is an efficient UGA suppressor in vitro. - Nucl. Acids Res. 26: 1390–1395, 1998.
Bernard, L., Ciceri, P., Viotti, A.: Molecular analysis of wildtype and mutant alleles at the Opaque-2 regulatory locus reveals different mutations and types of O2 products. - Plant mol. Biol. 24: 949–959, 1994.
Cartegni, L., Chew, S.L., Krainer, A.R.: Listening to silence and understanding nonsense: exonic mutations that affect splicing. - Natur. Rev. 3: 285–298, 2002.
Cartegni, L., Wang. J., Zhu, Z., Zhang, M.Q., Krainer, A.R.: ESEfinder: a web resource to identify exonic splicing enhancers. - Nucl. Acids Res. 31: 3568–3571, 2003.
Chodavarapu, R.K., Feng, S., Bernatavichute, Y.V., Chen, P.Y., Stroud, H., Yu, Y., Hetzel, J., Kuo, F., Kim, J., Cokus, S.J., Casero, D., Bernal, M., Huijser, P., Clark, A.T., Krämer, U., Merchant, S.S., Zhang, X., Jacobsen, S.E., Pellegrini, M.: Relationship between nucleosome positioning and DNA methylation. - Nature 446: 388392, 2010.
Ciceri, P., Castelli, S., Lauria, M., Lazzari, B., Genga, A., Bernard, L., Sturaro, M., Viotti, A.: Specific combinations of zein genes and genetic backgrounds influence the transcription of the heavy-chain zein genes in maize opaque-2 endosperms. - Plant Physiol. 124: 451–460, 2000.
Defenouillère, Q., Fromont Racine, M.: The ribosome bound quality control complex: from aberrant peptide clearance to proteostasis maintenance. - Curr. Genet. 63: 997–1005, 2017.
Dubrovina, A.S., Kiselev, K.V., Zhuravlev, Y.N.: The role of canonical and noncanonical pre-mRNA splicing in plant stress responses. - BioMed Res. Int. 2013: 1–14, 2013.
Faustino, N.A., Cooper, T.A.: Pre-mRNA splicing and human disease. - Genes Develop. 17: 419–437, 2003.
Gavazzi, F., Lazzari, B., Ciceri, P., Gianazza, E., Viotti, A.: Wild-type Opaque2 and defective opaque2 polypeptides form complexes in maize endosperm cells and bind the Opaque2-zein target site. - Plant Physiol. 145: 933–945, 2007.
Golovko, A., Sitbon, F., Tillberg, E., Nicander, B.: Identification of a tRNA isopentenyltransferase gene from Arabidopsis thaliana. - Plant mol. Biol. 49: 161–169, 2002.
Gruntman, E., Qi, Y., Slotkin, R.K., Roeder, T., Martienssen, R.A., Sachidanandam, R.: Kismeth: analyzer of plant methylation states through bisulfite sequencing. - BMC Bioinform. 9: 371, 2008.
Hoschek, G., Kelly, A.R., Schmidt, R.J.: Characterization of the molecular defect in a null allele of the opaque-2 locus of maize. - Plant Mol. Biol. 32: 1159–1161, 1996.
Lazzari, B., Cosentino,. C, Viotti A.: Gene products and structure analysis of wild-type and mutant alleles at the Opaque-2 locus of Zea mays. - Maydica 47: 253–265, 2002.
Lecointe, F., Namy, O., Hatin, I., Simos, G., Rousset, J.P., Grosjean H.: Lack of pseudouridine 38/39 in the anticodon arm of yeast cytoplasmic tRNA decreases in vivo recoding efficiency. - J. biol. Chem. 277: 30445–30453, 2002.
Li, C., Qiao, Z., Qi, W., Wang, Q., Yuan, Y., Yang, X., Tang, Y., Mei, B., Lv, Y., Zhao, H., Xiao, H., Song, R.: Genomewide characterization of cis-acting DNA targets reveals the transcriptional regulatory framework of Opaque2 in maize. - Plant Cell 27: 532–545, 2015.
Lopato, S., Forstner, C., Kalyna, M., Hilscher, J., Langhammer, U., Indrapichate, K., Lorkovic, Z.J., Barta, A.: Network of interactions of a novel plant-specific arg/ser-richpProtein, atRSZ33, with atSC35-like splicing factors. - J.biol. Chem. 277: 39989–39998, 2002.
Luco, R.F., Pan, Q., Tominaga, K., Blencowe, B.J., Pereira-Smith, O.M., Misteli, T.: Regulation of alternative splicing by histone modifications. - Science 327: 996–1000., 2010.
Luco, R.F., Allo, M., Schor, I.E., Kornblihtt, A.R., Misteli, T.: Epigenetic in alternative pre-mRNA splicing. - Cell 144: 16–26, 2011.
Maor, G.L., Yearim, A., Ast, G.: The alternative role of DNA methylation in splicing regulation. - Trends Genet. 31: 274–280, 2015.
Motto, M., Maddaloni, M., Ponziani, G., Brembilla, M., Marotta., R., Di Fonzo, N., Soave, C., Thompson, R., Salamini, F.: Molecular cloning of the o2-m5 allele of Zea mays using transposon marking. - Mol. gen. Genet. 212: 488–494, 1988.
Pirona, R., Hartings, H., Lauria, M., Rossi, V., Motto.: Genetic control of endosperm development and of storage products accumulation in maize seeds. - Maydica 50: 515–530, 2005.
Schmidt, R.J., Burr, F.A., Burr, B.: Transposon tagging and molecular analysis of the maize regulatory locus opaque-2. - Science 238: 960–963, 1987.
Schmidt, R.J., Burr, F.A., Aukerman, M.J., Burr, B.: Maize regulatory gene opaque-2 encodes a protein with a “leucine-zipper” motif that binds to zein DNA. - Proc. nat. Acad. Sci. USA 87: 46–50, 1990.
Shang, X., Cao, Y., Ma, L.: Alternative splicing in plant genes: a means of regulating the environmental fitness of plants. - Int. J. mol. Sci. 18: 432, 2017.
Song, R., Llaca. V., Linton. E., Messing, J.: Sequence, regulation, and evolution of the maize 22-kD a zein gene family. - Genome Res. 11: 1817–1825, 2001.
Wang, B.B., Brendel, V.: The ASRG database: identification and survey of Arabidopsis thaliana genes involved in premRNA splicing. - Genome Biol. 5: R102, 2004.
Xiao, X., Wang, Z., Jang. M., Burge, C.B.: Coevolutionary networks of splicing cis-regulatory elements. - Proc. nat. Acad. Sci. USA 47: 18583–18588, 2007.
Yearim, A., Gelfman, S., Shayevitch, R., Melcer, S., Glaich, O., Mallm, J.P., Nissim-Rafinia, M., Cohen, A.H.S, Rippe, K., Meshorer, E., Ast, G.: HP1 is involved in regulating the global impact of DNA methylation on alternative splicing. - Cell Rep. 10: 1–13, 2015.