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Trehalose metabolism is activated upon chilling in grapevine and might participate in Burkholderia phytofirmans induced chilling tolerance

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Abstract

During the last decade, there has been growing interest in the role of trehalose metabolism in tolerance to abiotic stress in higher plants, especially cold stress. So far, this metabolism has not yet been studied in Vitis vinifera L., despite the economic importance of this crop. The goal of this paper was to investigate the involvement of trehalose metabolism in the response of grapevine to chilling stress, and to compare the response in plants bacterised with Burkholderia phytofirmans strain PsJN, a plant growth-promoting rhizobacterium that confers grapevine chilling tolerance, with mock-inoculated plants. In silico analysis revealed that the V. vinifera L. genome contains genes encoding the enzymes responsible for trehalose synthesis and degradation. Transcript analysis showed that these genes were differentially expressed in various plant organs, and we also characterised their response to chilling. Both trehalose and trehalose 6-phosphate (T6P) were present in grapevine tissues and showed a distinct pattern of accumulation upon chilling. Our results suggest a role for T6P as the main active molecule in the metabolism upon chilling, with a possible link with sucrose metabolism. Furthermore, plants colonised by B. phytofirmans and cultivated at 26°C accumulated T6P and trehalose in stems and leaves at concentrations similar to non-bacterised plants exposed to chilling temperatures for 1 day. Overall, our data suggest that T6P and trehalose accumulate upon chilling stress in grapevine and might participate in the resistance to chilling stress conferred by B. phytofirmans.

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Abbreviations

HAD:

l-2-Haloacid dehalogenase

PGPR:

Plant growth-promoting rhizobacteria

SnRK1:

Sucrose-non-fermenting-1-related kinase 1

T6P:

Trehalose-6-phosphate

TPS:

Trehalose phosphate synthase

TPP:

Trehalose phosphate phosphatase

TRE:

Trehalase

References

  • Ait Barka E, Belarbi A, Hachet C, Nowak J, Audran J-C (2000) Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera co-cultured with plant growth-promoting rhizobacteria. FEMS Microbiol Lett 186:91–95

    Article  Google Scholar 

  • Ait Barka E, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72:7246–7252

    Article  PubMed  Google Scholar 

  • Argüelles JC (2000) Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 174:217–224

    Article  PubMed  Google Scholar 

  • Avonce N, Leyman B, Mascorro-Gallardo JO, van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136:3649–3659

    Article  PubMed  CAS  Google Scholar 

  • Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G (2006) Insights on the evolution of trehalose biosynthesis. BMC Evol Biol 6:109

    Article  PubMed  Google Scholar 

  • Bae H, Herman E, Bailey B, Bae H-J, Sicher R (2005a) Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. Physiol Plant 125:114–126

    Article  CAS  Google Scholar 

  • Bae H, Herman E, Sicher R (2005b) 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

    Article  CAS  Google Scholar 

  • Bertamini M, Muthuchelian K, Rubinigg M, Zorer R, Nedunchezhian N (2005) Low-night temperature (LNT) induced changes of photosynthesis in grapevine (Vitis vinifera L.) plants. Plant Physiol Biochem 43:693–699

    Article  PubMed  CAS  Google Scholar 

  • Bertamini M, Muthuchelian K, Rubinigg M, Zorer R, Velasco R, Nedunchezhian N (2006) Low-night temperature increased the photoinhibition of photosynthesis in grapevine (Vitis vinifera L. cv. Riesling) leaves. Environ Exp Bot 57:25–31

    Article  CAS  Google Scholar 

  • Blázquez MA, Santos E, C-l Flores, Martínez Zapater JM, Salinas J, Gancedo C et al (1998) Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J 13:685–689

    Article  PubMed  Google Scholar 

  • Bordiec S, Paquis S, Lacroix H, Dhondt S, Ait Barka E, Kauffmann S, Jeandet P, Mazeyrat-Gourbeyre F, Clément C, Baillieul F, Dorey S et al (2010) Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot 62:595–603

    Article  PubMed  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  PubMed  CAS  Google Scholar 

  • Bray E, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiology, Rockville, pp 1158–1203

    Google Scholar 

  • Brodmann D, Schuller A, Ludwig-Muller J, Aeschbacher RA, Wiemken A, Boller T, Wingler A (2002) Induction of trehalase in Arabidopsis plants infected with the trehalose-producing pathogen Plasmodiophora brassicae. Mol Plant Microbe Interact 15:693–700

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Wang Y, Dai B, Wang B, Zhang H, Zhu Z, Xu Y, Cao Y, Jiang Y, Zhang G (2008) Trehalose is an important mediator of Cap1p oxidative stress response in Candida albicans. Biol Pharm Bull 31:421–425

    Article  PubMed  CAS  Google Scholar 

  • Chen D-C, Yang B-C, Kuo T–T (1992) One-step transformation of yeast in stationary phase. Curr Genet 21:83–84

    Article  PubMed  CAS  Google Scholar 

  • Compant S, Reiter B, Sessitsch A, Nowak J, Clement C, Ait Barka E et al (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693

    Article  PubMed  CAS  Google Scholar 

  • Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459

    Article  PubMed  Google Scholar 

  • Crowe JH (2007) Trehalose as a “chemical chaperone” fact and fantasy. In: Back N, Cohen IR, Lajtha A, Lambris JD, Paoletti R (eds) Molecular aspects of the stress response: chaperones, membranes and networks. Springer, New York, pp 143–158

    Chapter  Google Scholar 

  • Drennan PM, Smith MT, Goldsworth D, Van Staden J (1993) The occurence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius welw. J Plant Physiol 142:493–496

    Article  CAS  Google Scholar 

  • Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17–27

    Article  Google Scholar 

  • Farias-Rodriguez R, Mellor RB, Arias C, Pena-Cabriales JJ (1998) The accumulation of trehalose in nodules of several cultivars of common bean (Phaseolus vulgaris) and its correlation with resistance to drought stress. Physiol Plant 102:353–359

    Article  CAS  Google Scholar 

  • Fernandez O, Béthencourt L, Quero A, Sangwan RS, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417

    Article  PubMed  CAS  Google Scholar 

  • Gibon Y, Bessieres MA, Larher F (1997) Is glycine betaine a non-compatible solute in higher plants that do not accumulate it? Plant Cell Environ 20:329–340

    Article  Google Scholar 

  • Goddijn OJM, van Dun K (1999) Trehalose metabolism in plants. Trends Plant Sci 4:315–319

    Article  PubMed  Google Scholar 

  • Gravot A, Grillet L, Wagner G, Jubault M, Lariagon C, Baron C, Deleu C, Delourme R, Bouchereau A, Manzanares-Dauleux MJ (2011) Genetic and physiological analysis of the relationship between partial resistance to clubroot and tolerance to trehalose in Arabidopsis thaliana. New Phytol 191:1083–1094

    Article  PubMed  CAS  Google Scholar 

  • Hendrickson L, Ball MC, Wood JT, Chow WS, Furbank RT (2004) Low temperature effects on photosynthesis and growth of grapevine. Plant Cell Environ 27:795–809

    Article  CAS  Google Scholar 

  • Hirsh AG (1987) Vitrification in plants as a natural form of cryoprotection. Cryobiology 24:214–228

    Article  PubMed  CAS  Google Scholar 

  • Hohmann S, Neves MJ, Koning W, Alijo R, Ramos J, Thevelein JM (1993) The growth and signalling defects of the ggs1 (fdp1/byp1) deletion mutant on glucose are suppressed by a deletion of the gene encoding hexokinase PII. Curr Genet 23:281–289

    Google Scholar 

  • Iordachescu M, Imai R (2008) Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol 50:1223–1229

    Article  PubMed  CAS  Google Scholar 

  • Jaillon O, Aury J-M, Noel B, for The French-Italian Public Consortium for Grapevine Genome Characterization, et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Google Scholar 

  • Janská A, Maršík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation—what is important for metabolic adjustment? Plant Biol 12:395–405

    Article  PubMed  Google Scholar 

  • Kandror O, DeLeon A, Goldberg AL (2002) Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99:9727–9732

    Article  PubMed  CAS  Google Scholar 

  • Kandror O, Bretschneider N, Kreydin E, Cavalieri D, Goldberg AL (2004) Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependent induction of trehalose synthesis and certain molecular chaperones. Mol Cell 13:771–781

    Article  PubMed  CAS  Google Scholar 

  • Karim S, Aronsson H, Ericson H, Pirhonen M, Leyman B, Welin B, Mäntylä E, Palva E, van Dijck P, Holmström K-O (2007) Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol Biol 64:371–386

    Article  PubMed  CAS  Google Scholar 

  • Leyman B, van Dijck P, Thevelein JM (2001) An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. Trends Plant Sci 6:510–513

    Article  PubMed  CAS  Google Scholar 

  • Li H-W, Zang B-S, Deng X-W, Wang X-P (2011) Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234:1007–1018

    Article  PubMed  CAS  Google Scholar 

  • Liu M-S, Chien C-T, Lin T-P (2008) Constitutive components and induced gene expression are involved in the desiccation tolerance of Selaginella tamariscina. Plant Cell Physiol 49:653–663

    Article  PubMed  CAS  Google Scholar 

  • López MF, Männer P, Willmann A, Hampp R, Nehls U (2007) Increased trehalose biosynthesis in Hartig net hyphae of ectomycorrhizas. New Phytol 174:389–398

    Article  PubMed  Google Scholar 

  • López M, Tejera NA, Iribarne C, Lluch C, Herrera-Cervera JA (2008) Trehalose and trehalase in root nodules of Medicago truncatula and Phaseolus vulgaris in response to salt stress. Physiol Plant 134:575–582

    Article  PubMed  Google Scholar 

  • Lunn JE (2007) Gene families and evolution of trehalose metabolism in plants. Funct Plant Biol 34:550–563

    Article  CAS  Google Scholar 

  • 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 ADP-glucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397:139–148

    Article  PubMed  CAS  Google Scholar 

  • Luo Y, Li W-M, Wang W (2008) Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? Environ Exp Bot 63:378–384

    Article  CAS  Google Scholar 

  • Miranda J, Avonce N, Suárez R, Thevelein J, van Dijck P, Iturriaga G (2007) A bifunctional TPS–TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226:1411–1421

    Article  PubMed  CAS  Google Scholar 

  • Mollo L, Martins MCM, Olivera VF, Nievola CC, Figuereido-Ribeiro RCL (2011) Effects of low temperature on growth and non-structural carbohydrates of the imperial bromeliad Alcantarea imperialis cultured in vitro. Plant Cell Tissue Organ Cult. doi:10.1007/s11240-011-9966-y

    Google Scholar 

  • Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441

    Article  PubMed  CAS  Google Scholar 

  • Pillay VK, Nowak J (1997) Inoculum density, temperature, and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato (Lycopersicon esculentum L.) seedlings inoculated with a pseudomonad bacterium. Can J Microbiol 43:354–361

    Article  CAS  Google Scholar 

  • Pramanik MHR, Imai R (2005) 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

    Article  PubMed  CAS  Google Scholar 

  • Purvis JE, Yomano LP, Ingram LO (2005) Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl Environ Microbiol 71:3761–3769

    Article  PubMed  CAS  Google Scholar 

  • Ramon M, De Smet IVE, Vandesteene L, Naudts M, Leyman B, van Dijck P, Rolland F, Beeckman TOM, Thevelein JM (2009) Extensive expression regulation and lack of heterologous enzymatic activity of the class II trehalose metabolism proteins from Arabidopsis thaliana. Plant Cell Environ 32:1015–1032

    Article  PubMed  CAS  Google Scholar 

  • Rao KN, Kumaran D, Seetharaman J, Bonanno JB, Burley SK, Swaminathan S (2006) Crystal structure of trehalose-6-phosphate phosphatase–related protein: biochemical and biological implications. Protein Sci 15:1735–1744

    Article  PubMed  CAS  Google Scholar 

  • Reignault PH, Cogan A, Muchembled J, Lounes-Hadj Sahraoui A, Durand R, Sancholle M et al (2001) Trehalose induces resistance to powdery mildew in wheat. New Phytol 149:519–529

    Article  CAS  Google Scholar 

  • Renard-Merlier D, Randoux B, Nowak E, Farcy F, Durand R, Reignault PH (2007) Iodus 40, salicylic acid, heptanoyl salicylic acid and trehalose exhibit different efficacies and defence targets during a wheat/powdery mildew interaction. Phytochemistry 68:1156–1164

    Article  PubMed  CAS  Google Scholar 

  • Ruelland E, Vaultier M-N, Zachowski A, Hurry V, Kader J-C, Delseny M (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150

    Article  CAS  Google Scholar 

  • Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543–584

    Article  CAS  Google Scholar 

  • Streeter JG, Gomez ML (2006) Three enzymes for trehalose synthesis in Bradyrhizobium cultured bacteria and in bacteroids from soybean nodules. Appl Environ Microbiol 72:4250–4255

    Article  PubMed  CAS  Google Scholar 

  • Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C, Ageorges A, Atanassova R, Léon C, Renaudin J-P, Dédaldéchamp F, Romieu C, Delrot S, Hamdi S (2005) Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222:832–847

    Article  PubMed  CAS  Google Scholar 

  • van Dijck P, Mascorro-Gallardo JO, De Bus M, Royackers K, Iturriaga G, Thevelein JM (2002) Truncation of Arabidopsis thaliana and Selaginella lepidophylla trehalose-6-phosphate synthase unlocks high catalytic activity and supports high trehalose levels on expression in yeast. Biochem J 366:63–71

    PubMed  Google Scholar 

  • Vandesteene L (2009) Functional analysis of the trehalose metabolism gene family in Arabidopsis thaliana. PhD thesis, Katholieke Universiteit Leuven, Belgium

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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, Sangwan RS (2008) The Arabidopsis sweetie mutant is affected in carbohydrate metabolism and defective in the control of growth, development and senescence. Plant J 55:665–686

    Article  PubMed  CAS  Google Scholar 

  • Xiao H, Tattersall EAR, Siddiqua MK, Cramer GR, Nassuth A (2008) CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. Plant Cell Environ 31:1–10

    PubMed  CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu C-M (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhuang Y, Ren G, Yue G, Li Z, Qu X, Hou G, Zhu Y, Zhang J (2007) Effects of water-deficit stress on the transcriptomes of developing immature ear and tassel in maize. Plant Cell Rep 26:2137–2147

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Region Champagne-Ardennes. Vitis vinifera L. Chardonnay clone 7535 was a gift from Moët et Chandon. B. phytofirmans strain PsJN was kindly provided by Dr. Essaid Ait Barka. We thank Pr. Petronia Carillo for her help in optimisation of the trehalose assay for grapevine.

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Authors and Affiliations

  1. Unité de Recherche Vignes et Vins de Champagne (EA 2069), Laboratoire de Stress, Défense et Reproduction des Plantes, UFR Sciences Exactes et Naturelles, Université de Reims Champagne-Ardenne, BP 1039, 51687, Reims Cedex 2, France

    Olivier Fernandez, Fabienne Baillieul & Christophe Clément

  2. Laboratory of Functional Biology, Plant Metabolic Signaling Group, Institute of Botany and Microbiology, KU Leuven, Kasteelpark Arenberg 31, bus 2438, 3001, Heverlee, Belgium

    Lies Vandesteene

  3. Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany

    Regina Feil & John Edward Lunn

Authors
  1. Olivier Fernandez
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  2. Lies Vandesteene
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  3. Regina Feil
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  4. Fabienne Baillieul
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  5. John Edward Lunn
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  6. Christophe Clément
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Correspondence to Christophe Clément.

Electronic supplementary material

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425_2012_1611_MOESM1_ESM.ppt

Fig. S1 Phylogenetic tree of TPSs isoforms in V. vinifera L. and A. thaliana. A phylip phylogenetic tree was constructed using Clustwal W2—Phylogeny program. The neighbour-joining algorithm was used to construct tree from the distance matrix. Sequences were obtained from the NCBI Gene Bank. Tree was drawn in a radial form using TreeView software (http://www.taxonomy.zoology.gla.ac.uk/rod/treeview.html) (PPT 55 kb)

425_2012_1611_MOESM2_ESM.ppt

Fig. S2 Alignment of VvTPS1, AtTPS1, OsTPS1 and SlTPS1 protein sequences. Amino acid residues that are similar in all sequences are shaded in grey and the ones that are predicted to be important for substrate binding (according to Lunn 2007; Vandesteene et al. 2010) in catalytically active TPS are shaded in red. All of these residues are perfectly conserved in the four sequences (PPT 139 kb)

425_2012_1611_MOESM3_ESM.ppt

Fig. S3 Alignment of VvTPPA-F and TaTPP (from Thermoplasma acidophilum). Amino acid residues that are similar in all sequences are shaded in grey and the ones that are predicted to be important for substrate binding in catalytically active TPP enzymes (according to Lunn 2007) are shaded in red. All of these residues are perfectly conserved in the 6 VvTPP sequences (except one conservative substitution of Lys to Arg in four isoforms VvTPPA, VvTPPB, VvTPPC and VvTPPE) (PPT 105 kb)

425_2012_1611_MOESM4_ESM.ppt

Fig. S4 Relative transcript number of VvTPPs non-chilled (a) and chilled (b) grapevine plants. Transcript number was calculated using the standard curve method and normalized with the Ef1α gene as internal control. Results represent the mean (± SD) of transcript number analysed from three independent experiments. Plants were exposed to chilling during 9 h, a time point when all VvTPPs gene induction peaked. n.d not detected; ds: detected only in stems; dl : detected only in leaves (PPT 59 kb)

425_2012_1611_MOESM5_ESM.doc

Fig. S5 Protein coding region of the V. vinifera L. cv. Chardonnay TPPA cDNA and the deduced protein sequence. Differences from the orthologous V. vinifera L. cv. Pinot Noir cDNA and protein are highlighted in red (DOC 25 kb)

425_2012_1611_MOESM6_ESM.ppt

Fig. S6 Correlation between T6P and sucrose in roots, stems and leaves of V. vinifera L. plants. Correlation was evaluated in all samples (a), in non-chilled samples (b), in chilled samples (c) and in bacterised samples (d). All R² values are significant (P < 0.05) (PPT 59.5 kb)

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Fernandez, O., Vandesteene, L., Feil, R. et al. Trehalose metabolism is activated upon chilling in grapevine and might participate in Burkholderia phytofirmans induced chilling tolerance. Planta 236, 355–369 (2012). https://doi.org/10.1007/s00425-012-1611-4

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