An upstream open reading frame is essential for feedback regulation of ascorbate biosynthesis in arabidopsis

Plant Cell

Volumn 27, Issue 3, 2015, Pages 772-786

  Laing, William A ^a   Martínez Sánchez, Marcela ^a   Wright, Michele A ^a   Bulley, Sean M ^a   Brewster, Di ^a   Dare, Andrew P ^a   Rassam, Maysoon ^a   Wang, Daisy ^a   Storey, Roy ^a   Macknight, Richard C ^a,b   Hellens, Roger P ^a,b,c  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; BRYOPHYTA; MAGNOLIOPHYTA;

5' UNTRANSLATED REGION; ASCORBIC ACID; CODON; GALACTOSE; LUCIFERASE; PEPTIDE; PHOSPHOTRANSFERASE;

5' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ARABIDOPSIS; BIOSYNTHESIS; CHEMISTRY; CODON; DOWN REGULATION; DRUG EFFECTS; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; OPEN READING FRAME; PLANT LEAF; PROMOTER REGION; PROTEIN SYNTHESIS; RIBOSOME;

5' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; ARABIDOPSIS; ASCORBIC ACID; BIOSYNTHETIC PATHWAYS; CODON; DOWN-REGULATION; FEEDBACK, PHYSIOLOGICAL; GALACTOSE; GENE EXPRESSION REGULATION, PLANT; LUCIFERASES; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PEPTIDES; PHOSPHOTRANSFERASES; PLANT LEAVES; PROMOTER REGIONS, GENETIC; PROTEIN BIOSYNTHESIS; RIBOSOMES;

EID: 84927747928     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.133777     Document Type: Article

References (57)

1. Andrews, S.J., and Rothnagel, J.A. (2014). Emerging evidence for functional peptides encoded by short open reading frames. Nat. Rev. Genet. 15: 193–204.
2. Asensi-Fabado, M.A., and Munné-Bosch, S. (2010). Vitamins in plants: occurrence, biosynthesis and antioxidant function. Trends Plant Sci. 15: 582–592.
3. Baboo, S., Bhushan, B., Jiang, H., Grovenor, C.R.M., Pierre, P., Davis, B.G., and Cook, P.R. (2014). Most human proteins made in both nucleus and cytoplasm turn over within minutes. PLoS ONE 9: e99346.
4. Badejo, A.A., Eltelib, H.A., Fukunaga, K., Fujikawa, Y., and Esaka, M. (2009). Increase in ascorbate content of transgenic tobacco plants overexpressing the acerola (Malpighia glabra) phosphomannomutase gene. Plant Cell Physiol. 50: 423–428.
5. Bartoli, C.G., Tambussi, E.A., Diego, F., and Foyer, C.H. (2009). Control of ascorbic acid synthesis and accumulation and glutathione by the incident light red/far red ratio in Phaseolus vulgaris leaves. FEBS Lett. 583: 118–122.
6. Bartoli, C.G., Yu, J., Gómez, F., Fernández, L., McIntosh, L., and Foyer, C.H. (2006). Inter-relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves. J. Exp. Bot. 57: 1621–1631.
7. Bocobza, S.E., and Aharoni, A. (2008). Switching the light on plant riboswitches. Trends Plant Sci. 13: 526–533.
8. Bonin, C.P., Potter, I., Vanzin, G.F., and Reiter, W.-D. (1997). The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-D-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucose. Proc. Natl. Acad. Sci. USA 94: 2085–2090.
9. Bulley, S., Wright, M., Rommens, C., Yan, H., Rassam, M., Lin-Wang, K., Andre, C., Brewster, D., Karunairetnam, S., Allan, A.C., and Laing, W.A. (2012). Enhancing ascorbate in fruits and tubers through over-expression of the L-galactose pathway gene GDP-L-galactose phosphorylase. Plant Biotechnol. J. 10: 390–397.
10. Bulley, S.M., Rassam, M., Hoser, D., Otto, W., Schünemann, N., Wright, M., MacRae, E., Gleave, A., and Laing, W. (2009). Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-L-galactose guanyltransferase is a major control point of vitamin C biosynthesis. J. Exp. Bot. 60: 765–778.
11. Calvo, S.E., Pagliarini, D.J., and Mootha, V.K. (2009). Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc. Natl. Acad. Sci. USA 106: 7507–7512.
12. Charneski, C.A., and Hurst, L.D. (2013). Positively charged residues are the major determinants of ribosomal velocity. PLoS Biol. 11: e1001508.
13. Davey, M.W., Kenis, K., and Keulemans, J. (2006). Genetic control of fruit vitamin C contents. Plant Physiol. 142: 343–351.
14. Dowdle, J., Ishikawa, T., Gatzek, S., Rolinski, S., and Smirnoff, N. (2007). Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J. 52: 673–689.
15. Dvir, S., Velten, L., Sharon, E., Zeevi, D., Carey, L.B., Weinberger, A., and Segal, E. (2013). Deciphering the rules by which 59-UTR sequences affect protein expression in yeast. Proc. Natl. Acad. Sci. USA 110: E2792–E2801.
16. Fang, P., Spevak, C.C., Wu, C., and Sachs, M.S. (2004). A nascent polypeptide domain that can regulate translation elongation. Proc. Natl. Acad. Sci. USA 101: 4059–4064.
17. Ferguson, A.R., and MacRae, E.A. (1992). Vitamin C in Actinidia. Acta Hortic. 297: 481–487.
18. Ferreira, J.P., Overton, K.W., and Wang, C.L. (2013). Tuning gene expression with synthetic upstream open reading frames. Proc. Natl. Acad. Sci. USA 110: 11284–11289.
19. Foyer, C.H., and Noctor, G. (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 155: 2–18.
20. Gao, Y., Badejo, A.A., Shibata, H., Sawa, Y., Maruta, T., Shigeoka, S., Page, M., Smirnoff, N., and Ishikawa, T. (2011). Expression analysis of the VTC2 and VTC5 genes encoding GDP-L-galactose phosphorylase, an enzyme involved in ascorbate biosynthesis, in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 75: 1783–1788.
21. Gatzek, S., Wheeler, G.L., and Smirnoff, N. (2002). Antisense suppression of l-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated l-galactose synthesis. Plant J. 30: 541–553.
22. Gleave, A.P. (1992). A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20: 1203–1207.
23. Goecks, J., Nekrutenko, A., and Taylor, J., Galaxy Team. (2010). Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol. 11: R86.
24. Hakmaoui, A., Pérez-Bueno, M.L., García-Fontana, B., Camejo, D., Jiménez, A., Sevilla, F., and Barón, M. (2012). Analysis of the antioxidant response of Nicotiana benthamiana to infection with two strains of Pepper mild mottle virus. J. Exp. Bot. 63: 5487–5496.
25. Hayden, C.A., and Jorgensen, R.A. (2007). Identification of novel conserved peptide uORF homology groups in Arabidopsis and rice reveals ancient eukaryotic origin of select groups and preferential association with transcription factor-encoding genes. BMC Biol. 5: 32.
26. Hellens, R.P., Allan, A.C., Friel, E.N., Bolitho, K., Grafton, K., Templeton, M.D., Karunairetnam, S., Gleave, A.P., and Laing, W.A. (2005). Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1: 13.
27. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and Mullineaux, P.M. (2000). pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42: 819–832.
28. Ito, K., and Chiba, S. (2013). Arrest peptides: cis-acting modulators of translation. Annu. Rev. Biochem. 82: 171–202.
29. Ivanov, I.P., Firth, A.E., Michel, A.M., Atkins, J.F., and Baranov, P.V. (2011). Identification of evolutionarily conserved non-AUG-initiated N-terminal extensions in human coding sequences. Nucleic Acids Res. 39: 4220–4234.
30. Ivanov, I.P., Loughran, G., and Atkins, J.F. (2008). uORFs with unusual translational start codons autoregulate expression of eukaryotic ornithine decarboxylase homologs. Proc. Natl. Acad. Sci. USA 105: 10079–10084.
31. Juntawong, P., Girke, T., Bazin, J., and Bailey-Serres, J. (2014). Translational dynamics revealed by genome-wide profiling of ribosome footprints in Arabidopsis. Proc. Natl. Acad. Sci. USA 111: E203–E212.
32. 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.
33. Laing, W.A., Bulley, S., Wright, M., Cooney, J., Jensen, D., Barraclough, D., and MacRae, E. (2004). A highly specific L-galactose- 1-phosphate phosphatase on the path to ascorbate biosynthesis. Proc. Natl. Acad. Sci. USA 101: 16976–16981.
34. Laing, W.A., Wright, M.A., Cooney, J., and Bulley, S.M. (2007). The missing step of the L-galactose pathway of ascorbate biosynthesis in plants, an L-galactose guanyltransferase, increases leaf ascorbate content. Proc. Natl. Acad. Sci. USA 104: 9534–9539.
35. Liu, H., Yin, J., Xiao, M., Gao, C., Mason, A.S., Zhao, Z., Liu, Y., Li, J., and Fu, D. (2012). Characterization and evolution of 59 and 39 untranslated regions in eukaryotes. Gene 507: 106–111.
36. Liu, M.-J., Wu, S.-H., Wu, J.-F., Lin, W.-D., Wu, Y.-C., Tsai, T.-Y., Tsai, H.-L., and Wu, S.-H. (2013). Translational landscape of photomorphogenic Arabidopsis. Plant Cell 25: 3699–3710.
37. Mandl, J., Szarka, A., and Bánhegyi, G. (2009). Vitamin C: update on physiology and pharmacology. Br. J. Pharmacol. 157: 1097–1110.
38. Massot, C., Stevens, R., Génard, M., Longuenesse, J.-J., and Gautier, H. (2012). Light affects ascorbate content and ascorbate-related gene expression in tomato leaves more than in fruits. Planta 235: 153–163.
39. Medenbach, J., Seiler, M., and Hentze, M.W. (2011). Translational control via protein-regulated upstream open reading frames. Cell 145: 902–913.
40. Müller-Moulé, P. (2008). An expression analysis of the ascorbate biosynthesis enzyme VTC2. Plant Mol. Biol. 68: 31–41.
41. Rassam, M., and Laing, W. (2005). Variation in ascorbic acid and oxalate levels in the fruit of Actinidia chinensis tissues and genotypes. J. Agric. Food Chem. 53: 2322–2326.
42. Rozen, S., and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132: 365–386.
43. Schepetilnikov, M., Dimitrova, M., Mancera-Martínez, E., Geldreich, A., Keller, M., and Ryabova, L.A. (2013). TOR and S6K1 promote translation reinitiation of uORF-containing mRNAs via phosphorylation of eIF3h. EMBO J. 32: 1087–1102.
44. Schleich, S., Strassburger, K., Janiesch, P.C., Koledachkina, T., Miller, K.K., Haneke, K., Cheng, Y.-S., Küchler, K., Stoecklin, G., Duncan, K.E., and Teleman, A.A. (2014). DENR-MCT-1 promotes translation re-initiation downstream of uORFs to control tissue growth. Nature 512: 208–212.
45. Serganov, A., and Nudler, E. (2013). A decade of riboswitches. Cell 152: 17–24.
46. Shulaev, V., et al. (2011). The genome of woodland strawberry (Fragaria vesca). Nat. Genet. 43: 109–116.
47. Simpson, G.G., Laurie, R.E., Dijkwel, P.P., Quesada, V., Stockwell, P.A., Dean, C., and Macknight, R.C. (2010). Noncanonical translation initiation of the Arabidopsis flowering time and alternative polyadenylation regulator FCA. Plant Cell 22: 3764–3777.
48. Snowden, K.C., Simkin, A.J., Janssen, B.J., Templeton, K.R., Loucas, H.M., Simons, J.L., Karunairetnam, S., Gleave, A.P., Clark, D.G., and Klee, H.J. (2005). The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17: 746–759.
49. Tabata, K., Takaoka, T., and Esaka, M. (2002). Gene expression of ascorbic acid-related enzymes in tobacco. Phytochemistry 61: 631–635.
50. Takahashi, H., Takahashi, A., Naito, S., and Onouchi, H. (2012). BAIUCAS: a novel BLAST-based algorithm for the identification of upstream open reading frames with conserved amino acid sequences and its application to the Arabidopsis thaliana genome. Bioinformatics 28: 2231–2241.
51. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876–4882.
52. Tran, M.K., Schultz, C.J., and Baumann, U. (2008). Conserved upstream open reading frames in higher plants. BMC Genomics 9: 361.
53. von Arnim, A.G., Jia, Q., and Vaughn, J.N. (2014). Regulation of plant translation by upstream open reading frames. Plant Sci. 214: 1–12.
54. Wamboldt, Y., Mohammed, S., Elowsky, C., Wittgren, C., de Paula, W.B.M., and Mackenzie, S.A. (2009). Participation of leaky ribosome scanning in protein dual targeting by alternative translation initiation in higher plants. Plant Cell 21: 157–167.
55. Yabuta, Y., Mieda, T., Rapolu, M., Nakamura, A., Motoki, T., Maruta, T., Yoshimura, K., Ishikawa, T., and Shigeoka, S. (2007). Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis. J. Exp. Bot. 58: 2661–2671.
56. Zhang, J., Lau, M.W., and Ferré-D’Amaré, A.R. (2010). Ribozymes and riboswitches: modulation of RNA function by small molecules. Biochemistry 49: 9123–9131.
57. Zhou, Y., Tao, Q.C., Wang, Z.N., Fan, R., Li, Y., Sun, X.F., and Tang, K.X. (2012). Engineering ascorbic acid biosynthetic pathway in Arabidopsis leaves by single and double gene transformation. Biol. Plant. 56: 451–457.