The redox-sensitive chloroplast trehalose-6-phosphate phosphatase AtTPPD regulates salt stress tolerance

Antioxidants and Redox Signaling

Volumn 21, Issue 9, 2014, Pages 1289-1304

  Krasensky, Julia ^a   Broyart, Caroline ^a   Rabanal, Fernando A ^a   Jonak, Claudia ^a  

^a GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DISULFIDE; ISOENZYME; PHOSPHATASE; STARCH; TREHALOSE; TREHALOSE 6 PHOSPHATE PHOSPHATASE; UNCLASSIFIED DRUG; SODIUM CHLORIDE; TREHALOSE-PHOSPHATASE;

CARBOHYDRATE METABOLISM; CELL NUCLEUS; CHLOROPLAST; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC CONSERVATION; INTRACELLULAR SPACE; MUTATIONAL ANALYSIS; NONHUMAN; OXIDATION REDUCTION REACTION; PLANT METABOLISM; REGULATORY MECHANISM; REVIEW; SALT STRESS; SALT TOLERANCE; SEED PLANT; TRANSLATION REGULATION; ARABIDOPSIS; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGICAL STRESS;

ARABIDOPSIS; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; OXIDATION-REDUCTION; PHOSPHORIC MONOESTER HYDROLASES; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL;

EID: 84964313812     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5693     Document Type: Review

References (93)

1. Almeida AM, Santos M, Villalobos E, Araujo SS, van Dijck P, Leyman B, Cardoso LA, Santos D, Fevereiro PS, and Torne JM. Immunogold localization of trehalose-6-phosphate synthase in leaf segments of wild-type and transgenic tobacco plants expressing the AtTPS1 gene from Arabidopsis thaliana. Protoplasma 230: 41-49, 2007.
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, and Lipman DJ. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402, 1997.
3. Arnold K, Bordoli L, Kopp J, and Schwede T. The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201, 2006.
4. Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, and Iturriaga G. The Arabidopsis trehalose- 6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136: 3649-3659, 2004.
5. Avonce N, Mendoza-Vargas A, Morett E, and Iturriaga G. Insights on the evolution of trehalose biosynthesis. BMC Evol Biol 6: 109, 2006.
6. Babbs CF, Pham JA, and Coolbaugh RC. Lethal hydroxyl radical production in paraquat-treated plants. Plant Physiol 90: 1267-1270, 1989.
7. Bae H, Herman E, and Sicher R. Exogenous trehalose promotes non-structural carbohydrate accumulation and induces chemical detoxification and stress response proteins in Arabidopsis thaliana grown in liquid culture. Plant Sci 168: 1293-1301, 2005.
8. Balmer Y, Koller A, del Val G, Manieri W, Schurmann P, and Buchanan BB. Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci U S A 100: 370-375, 2003.
9. Bianchi G, Gamba A, Limiroli R, Pozzi N, Elster R, Salamini F, and Bartels D. The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiol Plant 87: 223-226, 1993.
10. Birol I, Raymond A, Jackman SD, Pleasance S, Coope R, Taylor GA, Yuen MM, Keeling CI, Brand D, Vandervalk BP, Kirk H, Pandoh P, Moore RA, Zhao Y, Mungall AJ, Jaquish B, Yanchuk A, Ritland C, Boyle B, Bousquet J, Ritland K, Mackay J, Bohlmann J, and Jones SJ. Assembling the 20 Gb white spruce (Picea glauca) genome from whole-genome shotgun sequencing data. Bioinformatics 29: 1492-1497, 2013.
11. Caldana C, Fernie AR, Willmitzer L, and Steinhauser D. Unraveling retrograde signaling pathways: finding candidate signaling molecules via metabolomics and systems biology driven approaches. Front Plant Sci 3: 267, 2012.
12. Chary SN, Hicks GR, Choi YG, Carter D, and Raikhel NV. Trehalose-6-phosphate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis. Plant Physiol 146: 97-107, 2008.
13. Cheng NH, Liu JZ, Brock A, Nelson RS, and Hirschi KD. AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage. J Biol Chem 281: 26280-26288, 2006.
14. Chibani K, Couturier J, Selles B, Jacquot JP, and Rouhier N. The chloroplastic thiol reducing systems: dual functions in the regulation of carbohydrate metabolism and regeneration of antioxidant enzymes, emphasis on the poplar redoxin equipment. Photosynth Res 104: 75-99, 2010.
15. Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB, and Miginiac-Maslow M. The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278: 23747-23752, 2003.
16. Cortina C and Culiáñez-Macià FA. Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169: 75-82, 2005.
17. Czechowski T, Stitt M, Altmann T, Udvardi MK, and Scheible WR. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17, 2005.
18. Debast S, Nunes-Nesi A, Hajirezaei MR, Hofmann J, Sonnewald U, Fernie AR, and Bornke F. Altering trehalose-6-phosphate content in transgenic potato tubers affects tuber growth and alters responsiveness to hormones during sprouting. Plant Physiol 156: 1754-1771, 2011.
19. Delatte TL, Sedijani P, Kondou Y, Matsui M, de Jong GJ, Somsen GW, Wiese-Klinkenberg A, Primavesi LF, Paul MJ, and Schluepmann H. 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, 2011.
20. Drennan PM, Smith MT, Goldsworthy D, and van Staden J. The occurence of trehalose in the leaves of the desiccationtolerant angiosperm Myrothamnus flabellifolius welw. J Plant Physiol 142: 493, 1993.
21. Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JD, Smeekens SC, and Graham IA. Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29: 225-235, 2002.
22. Elbein AD, Pan YT, Pastuszak I, and Carroll D. New insights on trehalose: a multifunctional molecule. Glycobiology 13: 17R-27R, 2003.
23. Fernandez O, Bethencourt L, Quero A, Sangwan RS, and Clement C. Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15: 409-417, 2010.
24. Fernandez O, Vandesteene L, Feil R, Baillieul F, Lunn J, and Clément C. Trehalose metabolism is activated upon chilling in grapevine and might participate in Burkholderia phytofirmans induced chilling tolerance. Planta 236: 355-369, 2012.
25. Fougere F, Le Rudulier D, and Streeter JG. Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of Alfalfa (Medicago sativa L.). Plant Physiol 96: 1228-1236, 1991.
26. Foyer CH, Neukermans J, Queval G, Noctor G, and Harbinson J. Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63: 1637-1661, 2012.
27. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, and Wu RJ. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci U S A 99: 15898-15903, 2002.
28. Ge LF, Chao DY, Shi M, Zhu MZ, Gao JP, and Lin HX. Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228: 191-201, 2008.
29. Gomez LD, Baud S, Gilday A, Li Y, and Graham IA. 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, 2006.
30. Gomez LD, Gilday A, Feil R, Lunn JE, and Graham IA. 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, 2010.
31. Guy C, Kaplan F, Kopka J, Selbig J, and Hincha DK. Metabolomics of temperature stress. Physiol Plant 132: 220-235, 2008.
32. Hasegawa P, Bressan R, Zhu JK, and Bohnert H. Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51: 463-499, 2000.
33. Iordachescu M and Imai R. Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol 50: 1223-1229, 2008.
34. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, and Guy CL. Exploring the temperaturestress metabolome of Arabidopsis. Plant Physiol 136: 4159-4168, 2004.
35. Karim S, Aronsson H, Ericson H, Pirhonen M, Leyman B, Welin B, Mantyla E, Palva ET, Van Dijck P, and Holmstrom KO. Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol Biol 64: 371-386, 2007.
36. Kempa S, Krasensky J, Dal Santo S, Kopka J, and Jonak C. A central role of abscisic acid in stress-regulated carbohydrate metabolism. PLoS One 3: e3935, 2008.
37. Keryer E, Collin V, Lavergne D, Lemaire S, and Issakidis-Bourguet E. Characterization of Arabidopsis mutants for the variable subunit of ferredoxin:thioredoxin reductase. Photosynth Res 79: 265-274, 2004.
38. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, and Geigenberger P. Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADPglucose pyrophosphorylase. Proc Natl Acad Sci U S A 102: 11118-11123, 2005.
39. Kondrák M, Marincs F, Kalapos B, Juhász Z, and Bánfalvi Z. Transcriptome Analysis of potato leaves expressing the trehalose-6-phosphate synthase 1 gene of yeast. PLoS One 6: e23466, 2011.
40. Krasensky J and Jonak C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63: 1593-1608, 2012.
41. Larcher W. Responses of Plants to Environmental Stresses. San Diego, CA: Academic Press, Inc., II, 2nd Ed., 1980.
42. Lee S-B, Kwon H-B, Kwon S-J, Park S-C, Jeong M-J, Han S-E, Byun M-O, and Daniell H. Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Mol Breed 11: 1-13, 2003.
43. Li H-W, Zang B-S, Deng X-W, Wang X-P. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234: 1007-1018, 2011.
44. Li P, Ma S, and Bohnert HJ. Coexpression characteristics of trehalose-6-phosphate phosphatase subfamily genes reveal different functions in a network context. Physiol Plant 133: 544-556, 2008.
45. Livak KJ and Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 - ΔΔCT method. Methods 25: 402-408, 2001.
46. Lunn JE, Feil R, Hendriks JH, Gibon Y, Morcuende R, Osuna D, Scheible WR, Carillo P, Hajirezaei MR, and Stitt M. 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, 2006.
47. Martins MC, Hejazi M, Fettke J, Steup M, Feil R, Krause U, Arrivault S, Vosloh D, Figueroa CM, Ivakov A, Yadav UP, Piques M, Metzner D, Stitt M, and Lunn JE. Feedback inhibition of starch degradation in Arabidopsis leaves mediated by trehalose 6-phosphate. Plant Physiol 163: 1142-1163, 2013.
48. Meyer Y, Buchanan BB, Vignols F, and Reichheld JP. Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 43: 335-367, 2009.
49. Mikkelsen R, Suszkiewicz K, and Blennow A. A novel type carbohydrate-binding module identified in alpha-glucan, water dikinases is specific for regulated plastidial starch metabolism. Biochemistry 45: 4674-4682, 2006.
50. Miller G, Suzuki N, Ciftci-Yilmaz S, and Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33: 453-467, 2010.
51. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410, 2002.
52. Munne-Bosch S, Queval G, and Foyer CH. The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161: 5-19, 2013.
53. Munns R and Tester M. Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: 651-681, 2008.
54. Nunes C, O'Hara LE, Primavesi LF, Delatte TL, Schluepmann H, Somsen GW, Silva AB, Fevereiro PS, Wingler A, and Paul MJ. The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiol 162: 1720-1732, 2013.
55. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A, Vicedomini R, Sahlin K, Sherwood E, Elfstrand M, Gramzow L, Holmberg K, Hallman J, Keech O, Klasson L, Koriabine M, Kucukoglu M, Kaller M, Luthman J, Lysholm F, Niittyla T, Olson A, Rilakovic N, Ritland C, Rossello JA, Sena J, Svensson T, Talavera-Lopez C, Theissen G, Tuominen H, Vanneste K, Wu ZQ, Zhang B, Zerbe P, Arvestad L, Bhalerao R, Bohlmann J, Bousquet J, Garcia Gil R, Hvidsten TR, de Jong P, MacKay J, Morgante M, Ritland K, Sundberg B, Thompson SL, Van de Peer Y, Andersson B, Nilsson O, Ingvarsson PK, Lundeberg J, and Jansson S. The Norway spruce genome sequence and conifer genome evolution. Nature 497: 579-584, 2013.
56. Paul MJ, Primavesi LF, Jhurreea D, and Zhang Y. Trehalose metabolism and signaling. Annu Rev Plant Biol 59: 417-441, 2008.
57. Perez-Ruiz JM, Spinola MC, Kirchsteiger K, Moreno J, Sahrawy M, and Cejudo FJ. Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18: 2356-2368, 2006.
58. Pogson BJ, Woo NS, Forster B, and Small ID. Plastid signalling to the nucleus and beyond. Trends Plant Sci 13: 602-609, 2008.
59. Porra RJ, Thompson WA, and Kriedemann PE. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384-394, 1989.
60. Pramanik MH and Imai R. Functional identification of a trehalose 6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Mol Biol 58: 751-762, 2005.
61. Ramon M, Rolland F, Thevelein JM, Van Dijck P, and Leyman B. ABI4 mediates the effects of exogenous trehalose on Arabidopsis growth and starch breakdown. Plant Mol Biol 63: 195-206, 2007.
62. Rao KN, Kumaran D, Seetharaman J, Bonanno JB, Burley SK, and Swaminathan S. Crystal structure of trehalose-6-phosphate phosphatase-related protein: biochemical and biological implications. Protein Sci 15: 1735-1744, 2006.
63. Rey P, Cuine S, Eymery F, Garin J, Court M, Jacquot JP, Rouhier N, and Broin M. Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J 41: 31-42, 2005.
64. Rizhsky L, Liang HJ, Shuman J, Shulaev V, Davletova S, and Mittler R. When Defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134: 1683-1696, 2004.
65. Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, and Jackson D. A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441: 227-230, 2006.
66. Scheibe R and Dietz KJ. Reduction-oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant Cell Environ 35: 202-216, 2012.
67. Schluepmann H, Pellny T, van Dijken A, Smeekens S, and Paul M. Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci U S A 100: 6849-6854, 2003.
68. Schurmann P and Buchanan BB. The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal 10: 1235-1274, 2008.
69. Serrato AJ, Perez-Ruiz JM, Spinola MC, and Cejudo FJ. A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 279: 43821-43827, 2004.
70. Seung D, Thalmann M, Sparla F, Abou Hachem M, Lee SK, Issakidis-Bourguet E, Svensson B, Zeeman SC, and Santelia D. Arabidopsis thaliana AMY3 is a unique redoxregulated chloroplastic alpha-amylase. J Biol Chem 288: 33620-33633, 2013.
71. Shima S, Matsui H, Tahara S, and Imai R. Biochemical characterization of rice trehalose-6-phosphate phosphatases supports distinctive functions of these plant enzymes. FEBS J 274: 1192-1201, 2007.
72. Sierla M, Rahikainen M, Salojarvi J, Kangasjarvi J, and Kangasjarvi S. Apoplastic and chloroplastic redox signaling networks in plant stress responses. Antioxid Redox Signal 18: 2220-2239, 2013.
73. Singh V, Louis J, Ayre BG, Reese JC, Pegadaraju V, and Shah J. Trehalose phosphate synthase11-dependent trehalose metabolism promotes Arabidopsis thaliana defense against the phloem-feeding insect Myzus persicae. Plant J 67: 94-104, 2011.
74. Sparla F, Costa A, Lo Schiavo F, Pupillo P, and Trost P. Redox regulation of a novel plastid-targeted beta-amylase of Arabidopsis. Plant Physiol 141: 840-850, 2006.
75. Sparla F, Pupillo P, and Trost P. The C-terminal extension of glyceraldehyde-3-phosphate dehydrogenase subunit B acts as an autoinhibitory domain regulated by thioredoxins and nicotinamide adenine dinucleotide. J Biol Chem 277: 44946-44952, 2002.
76. Sulpice R, Flis A, Ivakov AA, Apelt F, Krohn N, Encke B, Abel C, Feil R, Lunn JE, and Stitt M. Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol Plant 7: 137-155, 2014.
77. Suzuki N, Bajad S, Shuman J, Shulaev V, and Mittler R. The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem 283: 9269-9275, 2008.
78. van Dijken AJ, Schluepmann H, and Smeekens SC. Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135: 969-977, 2004.
79. Van Houtte H, Lopez-Galvis L, Vandesteene L, Beeckman T, and Van Dijck P. Redundant and non-redundant roles of the trehalose-6-phosphate phosphatases in leave growth, root hair specification and energy-responses in Arabidopsis. Plant Signal Behav 8, 2013.
80. Van Houtte H, Vandesteene L, Lopez-Galvis L, Lemmens L, Kissel E, Carpentier S, Feil R, Avonce N, Beeckman T, Lunn JE, and Van Dijck P. Overexpression of the trehalase gene AtTRE1 leads to increased drought stress tolerance in Arabidopsis and is involved in abscisic acid-induced stomatal closure. Plant Physiol 161: 1158-1171, 2013.
81. Vandesteene L, Lopez-Galvis L, Vanneste K, Feil R, Maere S, Lammens W, Rolland F, Lunn JE, Avonce N, Beeckman T, and Van Dijck P. Expansive evolution of the trehalose-6-phosphate phosphatase gene family in Arabidopsis. Plant Physiol 160: 884-896, 2012.
82. Vandesteene L, Ramon M, Le Roy K, Van Dijck P, and Rolland F. A single active trehalose-6-P synthase (TPS) and a family of putative regulatory TPS-like proteins in Arabidopsis. Mol Plant 3: 406-419, 2010.
83. Veyres N, Danon A, Aono M, Galliot S, Karibasappa YB, Diet A, Grandmottet F, Tamaoki M, Lesur D, Pilard S, Boitel-Conti M, Sangwan-Norreel BS, and Sangwan RS. The Arabidopsis sweetie mutant is affected in carbohydrate metabolism and defective in the control of growth, development and senescence. Plant J 55: 665-686, 2008.
84. Vogel G, Aeschbacher RA, Muller J, Boller T, and Wiemken A. Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant J 13: 673-683, 1998.
85. Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M, and Schmid M. Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339: 704-707, 2013.
86. Wegrzyn JL, Lee JM, Tearse BR, and Neale DB. Tree-Genes: a forest tree genome database. Int J Plant Genomics 2008: 412875, 2008.
87. Wingler A, Delatte TL, O'Hara LE, Primavesi LF, Jhurreea D, Paul MJ, and Schluepmann H. Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol 158: 1241-1251, 2012.
88. Wingler A, Fritzius T, Wiemken A, Boller T, and Aeschbacher RA. Trehalose induces the ADP-glucose pyrophosphorylase gene, ApL3, and starch synthesis in Arabidopsis. Plant Physiol 124: 105-114, 2000.
89. Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten HM, Stitt M, and Lunn JE. The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65: 1051-1068, 2014.
90. Yemm EW and Willis AJ. The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57: 508-510, 1954.
91. Zaffagnini M, Bedhomme M, Groni H, Marchand CH, Puppo C, Gontero B, Cassier-Chauvat C, Decottignies P, and Lemaire SD. Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: a proteomic survey. Mol Cell Proteomics 11: M111.014142, 2012.
92. Zaffagnini M, Bedhomme M, Marchand CH, Couturier JR, Gao XH, Rouhier N, Trost P, and Lemaire SP. Glutaredoxin s12: unique properties for redox signaling. Antioxid Redox Signal 16: 17-32, 2012.
93. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RA, Powers SJ, Schluepmann H, Delatte T, Wingler A, and Paul MJ. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149: 1860-1871, 2009.