The trehalose 6-phosphate/snRK1. signaling pathway primes growth recovery following relief of sink limitation

Plant Physiology

Volumn 162, Issue 3, 2013, Pages 1720-1732

  Nunes, Cátia ^a,b,c   O'Hara, Liam E ^e   Primavesi, Lucia F ^a   Delatte, Thierry L ^d   Schluepmann, Henriette ^d   Somsen, Govert W ^d   Silva, Anabela B ^b,c   Fevereiro, Pedro S ^b,c   Wingler, Astrid ^e   Paul, Matthew J ^a  

^a ROTHAMSTED RESEARCH   (United Kingdom)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c Departamento de Biologia Vegetal   (Portugal)

^d UTRECHT UNIVERSITY   (Netherlands)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84879727015     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.220657     Document Type: Article

References (30)

1. Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20: 2117-2129.
2. Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448: 938-942.
3. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17.
4. Debast S, Nunes-Nesi A, Hajirezaei MR, Hofmann J, Sonnewald U, Fernie AR, Börnke F (2011) Altering trehalose-6-phosphate content in transgenic potato tubers affects tuber growth and alters responsiveness to hormones during sprouting. Plant Physiol 156: 1754-1771.
5. Delatte TL, Sedijani P, Kondou Y, Matsui M, de Jong GJ, Somsen GW, Wiese-Klinkenberg A, Primavesi LF, Paul MJ, Schluepmann H (2011) Growth arrest by trehalose-6-phosphate: an astonishing case of primary metabolite control over growth by way of the SnRK1 signaling pathway. Plant Physiol 157: 160-174.
6. Delatte TL, Selman MHJ, Schluepmann H, Somsen GW, Smeekens SC, de Jong GJ (2009) Determination of trehalose-6-phosphate in Arabidopsis seedlings by successive extractions followed by anion exchange chromatography-mass spectrometry. Anal Biochem 389: 12-17.
7. Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JD, Smeekens SC, Graham IA (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29: 225-235.
8. Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13: 17R-27R
9. Gómez LD, Gilday A, Feil R, Lunn JE, Graham IA (2010) AtTPS1- mediated trehalose 6-phosphate synthesis is essential for embryogenic and vegetative growth and responsiveness to ABA in germinating seeds and stomatal guard cells. Plant J 64: 1-13.
10. Gómez LD, Baud S, Gilday A, Li Y, Graham IA (2006) Delayed embryo development in the ARABIDOPSIS TREHALOSE-6-PHOSPHATE SYNTHASE 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation. Plant J 46: 69-84.
11. Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8: 774-785.
12. Hoffmann WA, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Ann Bot (Lond) 90: 37-42.
13. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102: 11118-11123.
14. Krouk G, Ruffel S, Gutiérrez RA, Gojon A, Crawford NM, Coruzzi GM, Lacombe B (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16: 178-182.
15. Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R, Osuna D, Scheible W-R, Carillo P, Hajirezaei M-R, Stitt M (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397: 139-148.
16. Martínez-Barajas E, Delatte T, Schluepmann H, de Jong GJ, Somsen GW, Nunes C, Primavesi LF, Coello P, Mitchell RAC, Paul MJ (2011) Wheat grain development is characterized by remarkable trehalose 6-phosphate accumulation pregrain filling: tissue distribution and relationship to SNF1-related protein kinase1 activity. Plant Physiol 156: 373-381.
17. Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ, Sagar R, Fevereiro PS, Davis BG, Paul MJ (2013) Inhibition of SnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol Biochem 63: 89-98.
18. Paul MJ, Jhurreea D, Zhang Y, Primavesi LF, Delatte T, Schluepmann H, Wingler A (2010) Upregulation of biosynthetic processes associated with growth by trehalose 6-phosphate. Plant Signal Behav 5: 386-392.
19. Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59: 417-441.
20. Paul MJ, Stitt M (1993) Effects of nitrogen and phosphorus deficiencies on levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose. Plant Cell Environ 16: 1047-1057.
21. Pellny TK, Ghannoum O, Conroy JP, Schluepmann H, Smeekens S, Andralojc J, Krause K-P, Goddijn O, Paul MJ (2004) Genetic modification of photosynthesis with E. coli genes for trehalose synthesis. Plant Biotechnol J 2: 71-82.
22. Ramon M, Rolland F (2007) Plant development: introducing trehalose metabolism. Trends Plant Sci 12: 185-188.
23. Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 6849-6854.
24. Toroser D, Plaut Z, Huber SC (2000) Regulation of a plant SNF1-related protein kinase by glucose-6-phosphate. Plant Physiol 123: 403-412.
25. Usadel B, Bläsing OE, Gibon Y, Poree F, Höhne M, Günter M, Trethewey R, Kamlage B, Poorter H, Stitt M (2008) Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the nonfreezing range. Plant Cell Environ 31: 518-547.
26. Vandesteene L, López-Galvis L, Vanneste K, Feil R, Maere S, Lammens W, Rolland F, Lunn JE, Avonce N, Beeckman T, Van Dijck P (2012) Expansive evolution of the trehalose-6-phosphate phosphatase gene family in Arabidopsis. Plant Physiol 160: 884-896.
27. Vandesteene L, Ramon M, Le Roy K, Van Dijck P, Rolland F (2010) A single active trehalose-6-P synthase (TPS) and a family of putative regulatory TPS-like proteins in Arabidopsis. Mol Plant 3: 406-419
28. van Dijken AJH, Schluepmann H, Smeekens SC (2004) Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135: 969-977.
29. Wingler A, Delatte TL, O'Hara LE, Primavesi LF, Jhurreea D, Paul MJ, Schluepmann H (2012) Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol 158: 1241-1251.
30. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149: 1860-1871