Translational regulation of Arabidopsis XIPOTL1 is modulated by phosphocholine levels via the phylogenetically conserved upstream open reading frame 30

Journal of Experimental Botany

Volumn 63, Issue 14, 2012, Pages 5203-5221

  Alatorre Cobos, Fulgencio ^a   Cruz Ramírez, Alfredo ^a   Hayden, Celine A ^b   Pérez Torres, Claudia Anahí ^a   Chauvin, Anne Laure ^a   Ibarra Laclette, Enrique ^a   Alva Cortés, Erika ^a   Jorgensen, Richard A ^a   Herrera Estrella, Luis ^a  

^a Laboratorio Nacional de Genómica para la Biodiversidad Cinvestav Irapuato   (Mexico)

^b CALIFORNIA POLYTECHNIC STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis; mORF; phosphatidylcholine; phosphocholine; root development; translational control; uORF30; XIPOTL1

Indexed keywords

ARABIDOPSIS PROTEIN; CHOLINE; METHYLTRANSFERASE; PHOSPHOETHANOLAMINE METHYLTRANSFERASE; PHOSPHORYLCHOLINE; PLANT DNA;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NICK END LABELING; OPEN READING FRAME; POINT MUTATION;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHOLINE; DNA, PLANT; GENE EXPRESSION REGULATION, PLANT; IN SITU NICK-END LABELING; METHYLTRANSFERASES; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHOSPHORYLCHOLINE; POINT MUTATION;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84865757184     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers180     Document Type: Article

References (66)

1. Alonso J, Stepanova A, Leisse T, et al. 2003. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
2. Baluska F, Mancuso S, Volkmann D, Barlow PW. 2010. Root apex transition zone: a signaling-response nexus in the root. Trends in Plant Science 15, 402-408.
3. Bayer TS, Booth LN, Knudsen SM, Ellington AD. 2005. Arginine-rich motifs present multiple interfaces for specific binding by RNA. RNA 11, 1848-1857.
4. Beemster GTS, Baskin TI. 1998. Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiology 116, 1515-1526.
5. Begora MD, Macleod MJR, McCarry BE, Summers PS, Weretilnyk EA. 2010. Identification of phosphoethanolamine N-methyltransferase from Arabidopsis and its role in choline and phospholipid metabolism. The Journal of Biological Chemistry 285, 29147-29155.
6. Bligny R, Foray M-F, Roby C, Douce R. 1989. Transport and phosphorylation of choline in higher plant cells. The Journal of Biological Chemistry 264, 4888-4895.
7. Calvo SE, Pagliarini DJ, Mootha VK. 2009. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proceeding of the National Academy of Sciences, USA 106, 7507-7512.
8. Chatterjee S, Pal JK. 2009. Role of 5'-and 3'-untranslated regions of mRNAs in human diseases. Biology of the Cell 101, 251-262.
9. Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P. 1999. Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. The Plant Journal 20, 503-508.
10. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Research 14, 1188-1190.
11. Cruz-Ramírez A, López-Bucio J, Ramírez-Pimentel G, Zurita-Silva A, Sánchez-Calderon L, Ramírez-Chávez E, González-Ortega E, Herrera-Estrella L. 2004. The xipotl mutant of Arabidopsis reveals a critical role for phospholipid metabolism in root system development and epidermal cell integrity. The Plant Cell 16, 2020-2034.
12. Czechowski T, Bari RP, Stitt M, Scheible W-R, Udvardi MK. 2004. Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unexpected sensitivity reveals novel root-and shoot-specific genes. The Plant Journal 38, 366-379.
13. Eastmond PJ, Quettier A-L, Kroon JTM, Craddock C, Adams N, Slabas AR. 2010. PHOSPHATIDIC ACID PHOSPHOHYDROLASE1 and 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidopsis. The Plant Cell 22, 2796-2811.
14. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792-1797.
15. Floris M, Mahgoub H, Lanet E, Robaglia C, Menand B. 2009. Post-transcriptional regulation of gene expression in plants during abiotic stress. International Journal of Molecular Sciences 10, 3168-3185.
16. Franceschetti M, Hanfrey C, Scaramagli S, Torrigiani P, Bagni N, Burtin D, Michael AJ. 2001. Characterization of monot and dicot plant S-adenosyl-l-methionine decarboxylase gene families including in the mRNA of a highly conserved pair of upstream overlapping open reading frames. The Biochemical Journal 353, 403-409.
17. Gallager S. 1992. Quantitation of GUS activity by fluorometry. In: Gallager S, ed. GUS protocols: using the GUS gene as a reporter of gene expression. San Diego, CA: Academic Press, pp 47-59.
18. Galtier N, Gouy M, Gautier C.1996. SEAVIEW and PHYLO-WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences 12, 543-548.
19. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server. In: Walker JM, ed. The proteomics protocols handbook. Totowa, NJ: Humana Press, p 571.
20. Gawer M, Guern N, Chervin D, Mazliak P. 1991. Choline kinase activities in choline-sensitive and choline-resistant tobacco cells or callus grown on high choline concentrations. Effects on phosphatidylcholine synthesis. Plant Science 75, 167-176.
21. Gibellini F, Smith T. 2010. The Kennedy pathway-de novo synthesis of phosphatidylethanolamine and phosphotidylcholine. IUBMB Life 62, 414-428.
22. Guindon S, Gascuel O. 2003. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696-704.
23. Gout E, Bligny R, Roby C, Douce R. 1990. Transport of phosphocholine in higher plant cells: 31P nuclear magnetic resonance studies. Proceeding of the National Academy of Sciences, USA 87, 4280-4283.
24. Hanfrey C, Elliott KA, Franceschetti M, Mayer MJ, Illingworth C, Michael AJ. 2005. A dual upstream open reading frame-based autoregulatory circuit controlling polyamine-responsive translation. The Journal of Biological Chemistry 280, 39229-39237.
25. Hayden CA, Bosco G. 2008. Comparative genomic analysis of novel conserved peptide upstream open reading frames in Drosophila melanogaster and other dipteran species. BMC Genomics 9, 61.
26. Hayden CA, Jorgensen RA. 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 Biology 5, 32.
27. Hedges SB. 2002. The origin and evolution of model organisms. Nature Reviews Genetics 3, 838-849.
28. Hocquellet A, Joubès J, Perret A-M, Lessire R, Moreau P. 2005. Evidence for a different metabolism of PC and PE in shoots and roots. Plant Physiology and Biochemistry 43, 938-946.
29. Hood HM, Neafsey DE, Galagan J, Sachs MS. 2009. Evolutionary roles of upstream open reading frames in mediating gene regulation in fungi. Annual Review of Microbiology 63, 385-409.
30. Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T. 2006. The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133, 3575-3585.
31. Jackowski S. 1996. Cell cycle regulation of membrane phospholipid metabolism. The Journal of Biological Chemistry 271, 20219-20222.
32. Karimi M, Inzé D, Depicker A. 2002. GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193-195.
33. Keogh MR, Courtney PD, Kinney AJ, Dewey RE. 2009. Functional characterization of phospholipid N-methyltransferases from Arabidopsis and soybean. The Journal of Biological Chemistry 284, 15439-15447.
34. Lee OR, Kim SJ, Kim HJ, Hong JK, Ryu SB, Lee SH, Ganguly A, Cho H-T. 2010. Phospholipase A2 is required for PIN-FORMED protein trafficking to the plasma membrane in the Arabidopsis root. The Plant Cell 22, 1812-1825.
35. Li G, Xue H-W. 2007. Arabidopsis PLD?2 regulates vesicle trafficking and is required for auxin response. The Plant Cell 19, 281-295.
36. Long JC, Caceres JF. 2009. The SR protein family of splicing factors: master regulators of gene expression. Biochemical Journal 417, 15-27.
37. Malamy J, Benfey P. 1997. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124, 33-34.
38. Martin BA, Tolbert NE. 1983. Factors which affect the amount of inorganic phosphate, phosphorylcholine, and phosphorylethanolamine in xylem exudate of tomato plants. Plant Physiology 73, 464-470.
39. Martínez-Trujillo M, Limones-Briones V, Cabrera-Ponce JL, Herrera-Estrella L. 2004. Improving transformation efficiency of Arabidopsis thaliana by modifying the floral dip method. Plant Molecular Biology Reporter 22, 63-70.
40. Medenbach J, Seiler M, Hentzei MW. 2011. Translational control via protein-regulated upstream open reading frames. Cell 145, 902-913.
41. Morcuende R, Bari R, Gibon Y, et al. 2007. Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant, Cell and Environment 30, 85-112.
42. Moubayidin L, Perilli S, Dello loio R, Di Mambro R, Costantino P, Sabatini S. 2010. The rate of cell differenciation controls the Arabidopsis root meristem growth phase. Current Biology 20, 1138-1143.
43. Munnik T, Testerink C. 2009. Plant phospholipid signaling: 'in a nutshell'. The Journal of Phospholipid Research 50 (suppl), S260-S265.
44. Nagalakshmi U, Zhong W, Waern K, Shou C, Raha D, Gerstein M, Snyder M. 2008. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320, 1344-1349.
45. Nohturfft A, Zhang SC. 2009. Coordination of lipid metabolism in membrane biogenesis. Annual Review of Cell and Developmental Biology 25, 539-566.
46. Nuccio ML, Russell BL, Nolte KD, Rathinasabapathi B, Gage DA, Hanson AD. 1998. The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. The Plant Journal 16, 487-496.
47. Nyikó T, Sonkoly B, Mérai Z, Benkovics AH, Silhavy D. 2009. Plant upstream ORFs can trigger nonsense-mediated mRNA decay in a size-dependent manner. Plant Molecular Biology 71, 367-378.
48. Palavalli LH, Brendza KM, Haakenson W, Cahoon RE, McLaird M, Hicks LM, McCarter JP, Williams DJ, Hresko MC, Jez JM. 2006. Defining the role of phosphomethylethanolamine N-methyltransferase from Caenorhabditis elegans in phosphocholine biosynthesis by biochemical and kinetic analysis. Biochemistry 45, 6056-6065.
49. Pereira LAR, Todorova M, Cai X, Makaroff CA, Emery RJN, Moffatt BA. 2007. Methyl recycling activities are co-ordinately regulated during plant development. Journal of Experimental Botany 58, 1083-1098.
50. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817-818.
51. Rahmani F, Hummel M, Schuurmans J, Wiese-Klinkenberg A, Smeekens S, Hanson J. 2009. Sucrose control of translation mediated by an upstream open reading frame-encoded peptide. Plant Physiology 150, 1356-1367.
52. Rangan L, Vogel C, Srivastava A. 2008. Analysis of context sequence surrounding translation initiation site from genome of model plants. Molecular Biotechnology 39, 207-213.
53. Sabatini S, Beis D, Wolkenfelt H, et al. 1999. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463-472.
54. Smith DD, Summers PS, Weretilnyk EA. 2000. Phosphocholine synthesis in spinach: Characterization of phosphoethanolamine N-methyltransferase. Physiologia Plantarum 108, 286-294.
55. Tabuchi T, Okada T, Azuma T, Nanmori T, Yasuda T. 2006. Posttranscriptional regulation by the upstream open reading frame of the phosphoethanolamine N-methyltransferase gene. Bioscience, Biotechnology, and Biochemistry 70, 2330-2334.
56. Tan R, Frankel AD. 1995. Structural variety of arginine-rich RNA-binding peptides. Proceeding of the National Academy of Sciences, USA 92, 5282-5286.
57. Tasseva G, Richard L, Zachowski A. 2004. Regulation of phosphatidylcholine biosynthesis under salt stress involves choline kinases in Arabidopsis thaliana. FEBS Letters 566, 115-120.
58. Tercé F, Brun H, Vance DE. 1994. Requirement of phosphatidylcholine for normal progression through the cell cycle in CH3H/10T1/2 fibroblasts.?Journal of Lipid Research 35, 2130-2142.
59. Testerink N, van der Sanden MHM, Houweling M, Helms JB, Vaandrager AB. 2009. Depletion of phosphatidylcholine affects endoplasmic reticulum morphology and protein traffic at the Golgi complex. Journal of Lipid Research 50, 2182-2192.
60. Tran MK, Schultz CJ, Baumann U. 2008. Conserved upstream open reading frames in higher plants. BMC Genomics 9, 361.
61. Ubeda-Tomás S, Federici F, Casimiro I, Beemster GTS, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ. 2009. Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Current Biology 19, 1194-1199.
62. Wethmar K, Smink JJ, Leutz A. 2010. Upstream open reading frames: molecular switches in (patho)physiology. Bioessays 32, 885-893.
63. Wiese A, Elzinga N, Wobbes B, Smeekens S. 2004. A conserved upstream open reading frame mediates sucrose-induced repression of translation. The Plant Cell 16, 1717-1729.
64. Xue H-W, Xu C, Mei Y. 2009. Function and regulation of phospholipid signalling in plants. Biochemical Journal 421, 145-156.
65. Zhang G, Guo G, Hu X, et al. 2010. Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Research 20, 646-654.
66. Zhang Z, Li J, Yu J. 2006. Computing Ka and Ks with a consideration of unequal transitional substitutions. BMC Evolutionary Biology 6, 44.