Large-scale analysis of mRNA translation states during sucrose starvation in Arabidopsis cells identifies cell proliferation and chromatin structure as targets of translational control

Plant Physiology

Volumn 141, Issue 2, 2006, Pages 663-673

  Nicolai M ^a,b,c   Roncato, M A ^a   Canoy, A S ^b   Rouquie D ^b,d   Sarda, X ^b   Freyssinet, G ^b   Robaglia, C ^a  

^a CNRS   (France)

^b BIOGEMMA   (France)

^c Researches Center of Avignon   (France)

^d BAYER AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; SUGAR (SUCROSE);

ARABIDOPSIS CELLS; CHROMATIN STRUCTURE; DNA MICROARRAY ANALYSIS; SUCROSE STARVATION;

RNA;

ACETYLATION; NUCLEIC ACIDS; SUCROSE;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 33745663309     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.106.079418     Document Type: Article

References (45)

1. Aubert S, Gout E, Bligny R, Marty-Mazars D, Barrieu F, Alabouvette J, Marty F, Douce R (1996) Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. J Cell Biol 133: 1251-1263
2. Axelos M, Curie C, Mazzolini L, Bardet C, Lescure B (1992) A protocol for transient gene expression in Arabidopsis thaliana protoplast isolated cell suspension. Plant Physiol Biochem 30: 123-128
3. Bassham DC (2002) Golgi-independent trafficking of macromolecules to the plant vacuole. Adv Bot Res 38: 65-92
4. Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J (2005) Genomewide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot (Lond) 96: 647-660
5. Brouquisse R, James F, Raymond P, Pradet A (1991) Study of glucose starvation in excised maize root tips. Plant Physiol 96: 619-626
6. Chan MT, Yu S-M (1998) The 3′ untranslated region of a rice alpha-amylase gene functions as a sugar-dependent mRNA stability determinant. Proc Natl Acad Sci USA 95: 6543-6547
7. Chen M-H, Liu L-F, Chen Y-R, Wu HK, Yu S-M (1994) Expression of α-amylases, carbohydrate metabolism, and autophagy in cultured rice cells is coordinately regulated by sugar nutrient. Plant J 6: 626-636
8. Cheng WH, Taliercio EW, Chourey PS (1999) Sugars modulate an unusual mode of control of the cell-wall invertase gene (Incw1) through its 3′ untranslated region in a cell suspension culture of maize. Proc Natl Acad Sci USA 96: 10512-10517
9. Contento AL, Kim SJ, Bassham DC (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol 135: 2330-2347
10. Coruzzi G, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signalling in plants. Plant Physiol 125: 61-64
11. Coruzzi G, Zhou L (2001) Carbon and nitrogen sensing and signalling in plants: emerging matrix effect. Curr Opin Plant Biol 4: 247-253
12. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 15: 737-749
13. Dudoit P, Yang YH, Callow MJ, Speed TP (2000) Statistical methods for identifying differentially expressed genes in replicated cDNA microarray experiments. Technical report no. 578. Department of Statistics, University of California, Berkeley, CA
14. Finkelstein RR, Gibson SI (2002) ABA and sugar interactions regulating development: cross-talk or voices in a crowd? Curr Opin Plant Biol 5: 26-32
15. Fujiki Y, Ito M, Nishida I, Watanebe A (2001) Leucine and its keto acid enhance the coordinated expression of genes for branched-chain amino acid catabolism in Arabidopsis under sugar starvation. FEBS Lett 449: 161-165
16. Gazzarrini S, McCourt P (2001) Genetics interactions between ABA, ethylene and sugar signalling pathways. Curr Opin Plant Biol 4: 387-391
17. Ho S-L, Chao Y-C, Tong W-F, Yu S-M (2001) Sugar coordinately and differentially regulates growth and stress-related gene expression via a complex signal transduction network and multiple control mechanisms. Plant Physiol 125: 877-890
18. Journet EP, Bligny R, Douce R (1986) Biochemical changes during sucrose deprivation in higher plant cells. J Biol Chem 261: 3193-3199
19. Kim T-H, Kim B-H, Yahalom A, Chamovitz DA, Von Arnim AG (2004) Translational regulation via 5′ mRNA leader sequences revealed by mutational analysis of the Arabidopsis translation initiation factor subunit elF3h. Plant Cell 16: 3341-3356
20. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 509-540
21. Lloyd JC, Zakhleniuk OV (2004) Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot 55: 1221-1230
22. Martin DE, Hall MN (2005) The expanding TOR signalling network. Curr Opin Cell Biol 17: 159-166
23. Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C, Robaglia C (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA 99: 6422-6427
24. Menand B, Robaglia C (2004) Plant cell growth. In MN Hall, G Thomas, eds, Cell Growth: Control of Cell Size, Vol 42. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 625-637
25. Menges M, Murray JA (2002) Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J 30: 203-212
26. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300: 332-336
27. Moriyasu Y, Ohsumi Y (1996) Autophagy in tobacco suspension-cultured cell in response to sucrose starvation. Plant Physiol 111: 1233-1241
28. Preiss T, Baron-Benhamou J, Ansorge W, Hentze MW (2003) Homodirectional changes in transcriptome composition and mRNA translation induced by rapamycin and heat shock. Nat Struct Biol 10: 1039-1047
29. Price J, Laxmi A, St Martin SK, Jang J-C (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16: 2128-2150
30. Riou-Khamlichi C, Menges M, Healy JM, Murray JA (2000) Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell Biol 20: 4513-4521
31. Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2: 198-206
32. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signalling in plants. Plant Cell 14: 185-205
33. Rook F, Gerrits N, Kortstee A, van Kampen M, Borrias M, Weisbeek P, Smeekens S (1998) Sucrose-specific signalling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J 15: 253-263
34. Sheen J, Zhou L, Jang JC (1999) Sugars as signalling molecules. Curr Opin Plant Biol 2: 410-418
35. Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5: 430-436
36. Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol 51: 49-81
37. Smirnova JB, Selley JN, Sanchez-Cabo F, Carroll K, Eddy AA, McCarthy JE, Hubbard SJ, Pavitt GD, Grant CM, Ashe MP (2005) Global gene expression profiling reveals widespread yet distinctive translational responses to different eukaryotic translation initiation factor 2B-targeting stress pathways. Mol Cell Biol 25: 9340-9349
38. Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2: 178-186
39. Thiel G, Lietz M, Hohl M (2004) How mammalian transcriptional repressors work. Eur J Biochem 271: 2855-2862
40. Tian L, Chen ZJ (2001) Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc Natl Acad Sci USA 98: 200-205
41. Tian L, Fong MP, Wang JJ, Wei NE, Jiangs H, Doerge R, Chen ZJ (2005) Reversible histone acetylation and deacetylation mediate genome-wide promoter-dependent and locus-specific changes in gene expression during plant development. Genetics 169: 337-345
42. Tian L, Wang J, Fong MP, Chen M, Cao H, Gelvin SB, Chen ZJ (2003) Genetic control of developmental changes induced by disruption of Arabidopsis histone deacetylase 1 (AtHD1) expression. Genetics 165: 399-409
43. Wiese A, Elzinga N, Wobbes B, Smeekens S (2004) A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell 16: 1717-1729
44. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15
45. Yu SM (1999) Cellular and genetic responses of plants to sugar starvation. Plant Physiol 121: 687-693