The trehalose pathway in maize: Conservation and gene regulation in response to the diurnal cycle and extended darkness

Journal of Experimental Botany

Volumn 65, Issue 20, 2014, Pages 5959-5973

  Henry, Clémence ^a   Bledsoe, Samuel W ^a   Siekman, Allison ^a   Kollman, Alec ^a   Waters, Brian M ^a   Feil, Regina ^a,b   Stitt, Mark ^a,b   Lagrimini, L Mark ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

diurnal cycle; Maize; quantitative RT PCR; shade stress; trehalose gene family; trehalose 6 phosphate

Indexed keywords

ZEA MAYS;

GLUCOSYLTRANSFERASE; PHOSPHATASE; PROTEIN SERINE THREONINE KINASE; SNF1-RELATED PROTEIN KINASES; STARCH; SUCROSE; SUGAR PHOSPHATE; TREHALOSE; TREHALOSE-6-PHOSPHATE; TREHALOSE-6-PHOSPHATE SYNTHASE; TREHALOSE-PHOSPHATASE; VEGETABLE PROTEIN;

ANALOGS AND DERIVATIVES; CARBOHYDRATE METABOLISM; CIRCADIAN RHYTHM; DARKNESS; GENE EXPRESSION REGULATION; GENETICS; MAIZE; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGY; RADIATION RESPONSE; SEEDLING; TRANSGENIC PLANT;

CARBOHYDRATE METABOLISM; CIRCADIAN RHYTHM; DARKNESS; GENE EXPRESSION REGULATION, PLANT; GLUCOSYLTRANSFERASES; MULTIGENE FAMILY; PHOSPHORIC MONOESTER HYDROLASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEIN-SERINE-THREONINE KINASES; SEEDLING; STARCH; SUCROSE; SUGAR PHOSPHATES; TREHALOSE; ZEA MAYS;

EID: 84913558366     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru335     Document Type: Article

References (69)

1. Ali Q, Ash raf M. 2011. Induction of drought tolerance in maize (Zea mays L.) due to exogenous application of trehalose: growth, photosynthesis, water relations and oxidative defence mechanism. Journal of Agronomy and Crop Science 197, 258 -271.
2. Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G. 2006. Insights on the evolution of trehalose biosynthesis. BMC Evolutionary Biology 6, 109-124.
3. Avonce N, Wuyts J, Verscho oten K, Vandesteene L, Van Dijck P. 2010. The Cytophaga hutchinsonii ChTPSP: first characterized bifunctional TPS-TPP protein as putative ancestor of all eukaryotic trehalose biosynthesis proteins. Molecular Biology and Evolution 27 , 359-369.
4. Baena-Gonzá lez E, Rolland F, Thevelein JM, Sheen J. 2007. A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938-942.
5. Bläs ing O, Gibon Y, Gü nther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible W-R, Stitt M. 2005. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expres sion in Arabidopsis. Plant Cell 17, 3257-3281.
6. Brouquisse R, Gaudillere J, Raymond P. 1998. Induction of a carbonstarvation-related proteolysis in whole maize plants submitted to light/dark cycles and to ext ended darkness. Plant Physiology 117, 1281-91.
7. Carillo P, Feil R, Gibon Y, Satoh-Nagasawa N, Jackson D, Blä sing OE, Stitt M, Lunn JE. 2013. A fluorometric assay for trehalose in the picomole range. Plant Methods 9, 21.
8. Chary SN, Hicks GR, Choi YG, Carter D, Raikhel N. V. 2008. Trehalose-6-phosph ate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis. Plant Physiology 146, 97-107.
9. Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL. 2008. Global transcriptome analysis re veals circadian regtion of key pathways in plant growth and development. Genome Biology 9, R130.
10. Davidson RM, Hansey CN, Gowda M, et al. 2011. Utility of RNA sequencing for analysis of maize reproductive transcriptomes. Plant Genome Journal 4, 191.
11. Debast S, Nunes-nesi A, Hajirezaei MR, Hofmann J, Sonnewald U, Fernie AR, Bornke F. 2011. Altering trehalose-6-phosphate content in transgenic pot ato tubers affects tuber growth and alters responsiveness to hormones during sprouting 1. Plant Physiology 156, 1754-1771.
12. Delatte TL, Sedijani P, Kondou Y, Matsui M, de Jong GJ, Somsen GW, Wiese-Klinkenb erg 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 Physiology 157, 160-174.
13. Doherty CJ Kay SA 2010 Circadian control of global gene expression patterns. Annual Review of Genetics 44 419-44.
14. Earley EB, Miller RJ, Reichert GL, Hageman RH. 1966. Effects of shade on maize production under field conditions. 6, 1-7.
15. Ghillebert R, Swinnen E, Wen J, Vandesteene L, Ramon M, Norga K, Rolland F, Winderickx J. 2011. The AMPK/SNF1/SnRK1 fuel gauge and energ y regulator: structure, function and regulation. FEBS Journal 278, 3978-3990.
16. Gibon Y, Blä sing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Höhne M, Gü nther M, Stitt M. 2004. Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-gluc ose pyrophosphorylase in the followin. The Plant Journal 39, 847-862.
17. Gibon Y, Pyl E-T, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M. 2009. Adjustment of growth, starch turnover, protein c ontent and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant, Cell & Environment 32, 859-74.
18. Gibson RP, Turkenburg JP, Charnock SJ, Lloyd R, Davies GJ. 2002. Insights into trehalose synthesis provided by the structure of the retaining glucosyltransferase OtsA. Chemistry & Biology 9, 1337-46.
19. Glinski M, Weckwerth W. 2005. Differential multisite phosphorylation of the trehalose-6-phosphate synthase gene family in Arabidopsis thaliana: a mass spectrometry-based process for multiparallel peptide library phosphorylation analysis. Molecular & Cellular Proteomics 4, 1614 -1625.
20. Harmer SL, Hogenesch JB, Straume M, Chang H-S, Han B, Zhu T, Wang X, Kreps JA, Kay SA. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113.
21. Harthill JE, Meek SEM, Morrice N, Peggie MW, Borch J, Wong BHC, Mackintosh C. 20 06. Phosphorylation and 14-3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose. The Plant Journal 47, 211-223.
22. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandeso mpele J. 2007. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 8, R19.
23. Jiang W, Fu F-L, Zhang S-Z, Wu L, Li W-C. 2010. Cloning and characterization of functional trehalose-6-phosphate synthase gene in maize. Journal of Plant Biology 53, 134-141.
24. Khan S, Rowe SC, Harmon FG. 2010. Coordination of the maize transcriptome by a conserved circadian clock. BMC Plant Biology 10, 126-141.
25. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P. 2005. Trehalose 6-phosphate regulates starch synthe sis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proceedings of the National Academy of Sciences, USA 102, 11118-11123.
26. Li P, Ma S, Bohnert HJ. 2008. Coexpression characteristics of trehalose-6-phosphate phosphatase subfamily genes reveal different functions in a network context. Physiologia Plantarum 133, 544-56.
27. Lunn JE. 2007. Gene families and evolution of trehalose metabolism in plants. Functional Plant Biology 34, 550.
28. Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M. 2014. Trehalose metabolism in plants. The Plant Journal 49, n/a-n/a.
29. 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. Biochemical Journal 397, 139-148.
30. Ma J, Hanssen M, Lundgren K, et al. 2011. The sucrose-regulated Arabidopsis transcription factor bZIP11 reprograms metabolism and regulates trehalose metabolism. N ew Phytologist 191, 733-45.
31. Martí nez-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 Physiology 156, 373-381.
32. Mutisya J, Sun C, Jansson C. 2009. Circadian oscillation of starch branching enzyme gene expression in the sorghum endosperm. Plant Signaling & Behavior 4, 871-872.
33. Nunes C, O?Hara LE, Primavesi LF, Delatte TL, Schluepm ann H, Somsen GW, Silva AB, Fevereiro PS, Wingler A, Paul MJ. 2013. The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiology 162, 1720-32.
34. Osuna D, Usadel B, Morcuende R, et al. 2007. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. The Plant Journal 49, 463-91.
35. Paul M. 2007. Trehalose 6-phosphate. Current Opinion in Plant Biology 10, 303-9.
36. Paul MJ, Primavesi LF, Jhurreea D, Zhang Y. 2008. Trehalose metabolism and signaling. Annual Review of Plant Biology 59, 417-441.
37. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.
38. Polge C, Thomas M. 2007. SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy controlfi Trends in Plant Science 12, 20-28.
39. Ponnu J, Wahl V, Schmid M. 2011. Trehalose-6-phosphate: connecting plant metabolism and development. Frontiers in Plant Science 2, 70.
40. Ramon M, De Smet I, Vandesteene L, Naudts M, Leyman B , Van Dijck P, Rolland F, Beeckman T, Thevelein JM. 2009. Extensive expression regulation and lack of heterologous enzymatic activity of the Class II trehalose metabolism proteins from Arabidopsis thaliana. Plant, Cell & Environment 32, 1015-1032.
41. Rodrí guez-Salazar J, Suárez R, Caballero-Mellado J, Iturriaga G. 2009. Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiology Letters 296, 52-59.
42. Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D. 2006. A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441, 227-230.
43. Schluepmann H, Berke L, Sanchez-Perez GF. 2011. Metabolism control over growth: a case for trehalose-6-phosphate in plants. Journal of Experimental Botany 63, 3379-3390.
44. S chussler JR, Westgate ME. 1995. Assimilate flux determines kernel set at low water potential in maize. Crop Science 35, 1074-1080.
45. Sciences B, Zeid IM. 2009. Trehalose as osmoprotectant for maize under salinity-induced stress. Research Journal of Agriculture and Biological Sciences 5, 613-622.
46. Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, de Leon N, Kaeppler SM. 2011. Genome-wide atla s of transcription during maize development. The Plant Journal 66, 553-563.
47. Setter TL, Flannigan BA, Melkonian J. 2001. Loss of kernel set due to water deficit and shade in maize. Crop Science 41, 1530.
48. Sheen J. 2010. Discover and connect cellular signaling. Plant Physiology 154, 562-566.
49. Singh V, Louis J, Ayre BG, Reese JC, Shah J. 2011. TREHALOSE PHOSPHATE SYNTHASE1 1fidependent trehalose metabolism promotes Arabidopsis thaliana defense against the phloemfifeeding insect Myzus persicae. The Plant Journal 67, 94-104.
50. Smith S, Fulton D, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman S, Smith A. 2004. Diurnal Changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both trans criptional and posttranscriptional regulation of starch metabolism in Arabidopsis. Plant Physiology 136, 2687-2699.
51. Stitt M, Zeeman SC. 2012. Starch turnover: pathways, regulation and role in growth. Current Opinion in Plant Biology 15, 282-92.
52. Sulpice R, Flis A, Ivakov AA, Apelt F, Krohn N, Encke B, Abel C, Feil R, Lunn JE, Stitt M. 2014. Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Molecular Plant 7, 137-155.
53. Sulpice R, Trenkamp S, Steinfath M, et al. 2010. Network analysis of enzyme activities and metabolite levels an d their relationship to biomass in a large panel of Arabidopsis accessions. Plant Cell 22, 2872-2893.
54. Thimm O, Blä sing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Sti tt M. 2004. Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914-939.
55. Tiessen A, Prescha K, Branscheid A, Palacios N, McKibbin R, Halford NG, Geigenberger P. 2003. Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphor ylase in potato tubers. The Plant Journal 35, 490-500.
56. Usadel B Bläsing OE Gibon Y Retzlaff K Höhne M Günther M Stitt M. 2008 Global transcript levels respond to small changes of the c arbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes Plant Physiology 146 1834-61.
57. Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M. 2009. A guid e to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, maize. Plant, Cell & Environment 32, 1211-29.
58. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research0034.1-research0034.11.
59. Vandesteene L, López-Galvis L, Vanneste K, et al. 2012. Expansive evolution of the trehalose-6-phosphate phosphatase gene family in arabidopsis. Plant Physiology 160, 884-896.
60. Vandesteene L, Ramon M, Le Roy K, V an Dijck P, Rolland F. 2010. A single active trehalose-6-P synthase (TPS) and a family of putative regulatory TPS-like proteins in Arabidopsis. Molecular Plant 3, 406-19.
61. Wahl V, Ponnu J, Schlereth A, A rrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M, Schmid M. 2013. Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339, 704-7.
62. Wilson RA, Jenkinson JM, Gibson RP, Littlechild JA, Wang ZY, Talbot NJ. 2007. Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. EMBO Journal 26, 3673-85.
63. Wingler A. 2002. The function of trehalose biosynthesis in plants. Planta 60, 437-440.
64. 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 Physiology. doi: 10.1104/pp.111.191908.
65. Yadav UP, Ivakov A, Feil R, et al. 2014. The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. Journal of Experimental Botany 65, 1051-68.
66. Yang H- L, Liu Y-J, Wang C-L, Zeng Q-Y. 2012. Molecular evolution of trehalose-6-phosphate synthase (TPS) gene family in Populus, Arabidopsis and rice. PLoS One 7, e42438.
67. Zang B, Li H, Li W, Deng XW, Wang X. 2011. Analysis of trehalose-6-phosphate synthase (TPS) gene family suggests the formation of TPS complexes in rice. Plant Molecular Biology 76, 507-522.
68. Zeeman SC, Smith SM, Smith AM. 2007. The diurnal metabolism of leaf starch. Biochemical Journal 401, 13-28.
69. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ. 20 09. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiology 149, 1860-1871.