Skip to main content
SpringerLink
Log in

In tobacco BY-2 cells xyloglucan oligosaccharides alter the expression of genes involved in cell wall metabolism, signalling, stress responses, cell division and transcriptional control

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Xyloglucan oligosaccharides (XGOs) are breakdown products of XGs, the most abundant hemicelluloses of the primary cell walls of non-Poalean species. Treatment of cell cultures or whole plants with XGOs results in accelerated cell elongation and cell division, changes in primary root growth, and a stimulation of defence responses. They may therefore act as signalling molecules regulating plant growth and development. Previous work suggests an interaction with auxins and effects on cell wall loosening, however their mode of action is not fully understood. The effect of an XGO extract from tamarind (Tamarindus indica) on global gene expression was therefore investigated in tobacco BY-2 cells using microarrays. Over 500 genes were differentially regulated with similar numbers and functional classes of genes up- and down-regulated, indicating a complex interaction with the cellular machinery. Up-regulation of a putative XG endotransglycosylase/hydrolase-related (XTH) gene supports the mechanism of XGO action through cell wall loosening. Differential expression of defence-related genes supports a role for XGOs as elicitors. Changes in the expression of genes related to mitotic control and differentiation also support previous work showing that XGOs are mitotic inducers. XGOs also affected expression of several receptor-like kinase genes and transcription factors. Hence, XGOs have significant effects on expression of genes related to cell wall metabolism, signalling, stress responses, cell division and transcriptional control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Acosta A, González L, Porta H, Sánchez L, Rocha M (2007a) Preliminary results on the morphogenetic development of roots of Arabidopsis thaliana when was treated with Xyloglucan. In: XXIII reunión Latinoamericana de Rizobiología. RELAR, Los Cocos, Córdova, p 146

  2. Acosta A, González L, Valdés M, González C, Sánchez L (2007) Efecto de dos oligosacarinas sobre la expresión isoenzimática al ser aplicadas sobre dos variedades de tabaco (Nicotiana tabacum L.). Cultiv Trop 28:5–12

    Google Scholar 

  3. Aziz A, Heyraud A, Lambert B (2004) Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea. Planta 218:767–774

    Article  CAS  PubMed  Google Scholar 

  4. Bedhomme M, Mathieu C, Pulido A, Henry Y, Bergounioux C (2009) Arabidopsis monomeric G-proteins, markers of early and late events in cell differentiation. Int J Dev Biol 53:177–185

    Article  CAS  PubMed  Google Scholar 

  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  6. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107:9452–9457

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Buckeridge MS, Rocha DC, Reid JSG, Dietrich SMC (1992) Xyloglucan structure and post-germinative metabolism in seeds of Copaifera langsdorfii from savanna and forest populations. Physiol Plant 86:145–151

    Article  CAS  Google Scholar 

  8. Cabrera JC, Boland A, Messiaen J, Cambier P, Van Cutsem P (2008) Egg box conformation of oligogalacturonides: the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18:473–482

    Article  CAS  PubMed  Google Scholar 

  9. Cabrero J, Teruel M, Carmona FD, Camacho JPM (2007) Histone H2AX phosphorylation is associated with most meiotic events in grasshopper. Cytogenomic Genome Res 116:311–315

    Article  CAS  Google Scholar 

  10. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  CAS  PubMed  Google Scholar 

  11. Catalá C, Rose JKC, Bennett AB (1997) Auxin regulation and spatial localization of an endo-1,4-β-d-glucanase and a xyloglucan endotransglycosylase in expanding tomato hypocotyls. Plant J 12:417–426

    Article  PubMed  Google Scholar 

  12. Cheng Z, Sun L, Qi T, Zhang B, Peng W, Liu Y, Xie D (2011) The bHLH transcription factor MYC3 interacts with the jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis. Mol Plant 4:279–288

    Article  CAS  PubMed  Google Scholar 

  13. Chung HS, Howe GA (2009) A Critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 21:131–145

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  15. Cutillas-Iturralde A, Fulton DC, Fry SC, Lorences EP (1998) Xyloglucan-derived oligosaccharides induce ethylene synthesis in persimmon (Diospyros kaki L.) fruit. J Exp Bot 49:701–706

    CAS  Google Scholar 

  16. Cutillas-Iturralde A, Peña MJ, Zarra I, Lorences EP (1998) A xyloglucan from persimmon fruit cell walls. Phytochemistry 48:607–610

    Article  CAS  Google Scholar 

  17. Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 38:366–379

    Article  CAS  PubMed  Google Scholar 

  18. Darvill JE, McNeil M, Darvill AG, Albersheim P (1980) Structure of plant cell walls: XI. Glucuronoarabinoxylan, a second hemicellulose in the primary cell walls of suspension-cultured sycamore cells. Plant Physiol 66:1135–1139

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46:268–278

    Article  CAS  PubMed  Google Scholar 

  20. Deng WW, Liu CY, Pei YX, Deng X, Niu LF, Cao XF (2007) Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLOWERING LOCUS C in Arabidopsis. Plant Physiol 143:1660–1668

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Devaiah BN, Nagarajan VK, Raghothama KG (2007) Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 145:147–159

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88:685–694

    Article  CAS  PubMed  Google Scholar 

  23. Edwards K, Bombarely A, Story G, Allen F, Mueller L, Coates S, Jones L (2010) TobEA: an atlas of tobacco gene expression from seed to senescence. BMC Genomics 11:142

    Article  PubMed Central  PubMed  Google Scholar 

  24. Ehlting J, Mattheus N, Aeschliman DS, Li E, Hamberger B, Cullis IF, Zhuang J, Kaneda M, Mansfield SD, Samuels L, Ritland K, Ellis BE, Bohlmann J, Douglas CJ (2005) Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. Plant J 42:618–640

    Article  CAS  PubMed  Google Scholar 

  25. Eklöf JM, Brumer H (2010) The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiol 153:456–466

    Article  PubMed Central  PubMed  Google Scholar 

  26. Francis D, Davies MS, Braybrook C, James NC, Herbert RJ (1995) An effect of zinc on M-phase and G1 of the plant cell cycle in the synchronous TBY-2 tobacco cell suspension. J Exp Bot 46:1887–1894

    Article  CAS  Google Scholar 

  27. Fry SC (1995) Polysaccharide-modifying enzymes in the plant cell wall. Annu Rev Plant Physiol Plant Mol Biol 46:497–520

    Article  CAS  Google Scholar 

  28. Fry SC, York WS, Albersheim P, Darvill A, Hayashi T, Joseleau J-P, Kato Y, Lorences EP, Maclachlan GA, McNeil M, Mort AJ, Grant Reid JS, Seitz HU, Selvendran RR, Voragen AGJ, White AR (1993) An unambiguous nomenclature for xyloglucan-derived oligosaccharides. Physiol Plant 89:1–3

    Article  CAS  Google Scholar 

  29. Fry SC, Aldington S, Hetherington PR, Aitken J (1993) Oligosaccharides as signals and substrates in the plant cell wall. Plant Physiol 103:1–5

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. González Pérez L, Vázquez Glaría A, Perrotta L, Acosta Maspons A, Scriven SA, Herbert R, Cabrera JC, Francis D, Rogers HJ (2012) Oligosaccharins and Pectimorf® stimulate root elongation and shorten the cell cycle in higher plants. Plant Growth Regul 68:211–221

    Article  Google Scholar 

  31. Hubbell E, Liu W-M, Mei R (2002) Robust estimators for expression analysis. Bioinformatics 18:1585–1592

    Article  CAS  PubMed  Google Scholar 

  32. Hyodo H, Yamakawa S, Takeda Y, Tsuduki M, Yokota A, Nishitani K, Kohchi T (2003) Active gene expression of a xyloglucan endotransglucosylase/hydrolase gene, XTH9, in inflorescence apices is related to cell elongation in Arabidopsis thaliana. Plant Mol Biol 52:473–482

    Article  CAS  PubMed  Google Scholar 

  33. Iglesias N, Abelenda JA, Rodiño M, Sampedro J, Revilla G, Zarra I (2006) Apoplastic glycosidases active against xyloglucan oligosaccharides of Arabidopsis thaliana. Plant Cell Physiol 47:55–63

    Article  CAS  PubMed  Google Scholar 

  34. Inzé D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40:77–105

    Article  PubMed  Google Scholar 

  35. Ishida S, Takahashi Y, Nagata T (1993) Isolation of cDNA of an auxin-regulated gene encoding a G protein, B subunit-like protein from tobacco BY-2 cells. Proc Natl Acad Sci USA 90:11152–11156

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Kaida R, Sugawara S, Negoro K, Maki H, Hayashi T, Kaneko TS (2010) Acceleration of cell growth by xyloglucan oligosaccharides in suspension-cultured tobacco cells. Mol Plant 3:549–554

    Article  CAS  PubMed  Google Scholar 

  37. Kaku T, Tabuchi A, Wakabayashi K, Hoson T (2004) Xyloglucan oligosaccharides cause cell wall loosening by enhancing xyloglucan endotransglucosylase/hydrolase activity in azuki bean epicotyls. Plant Cell Physiol 45:77–82

    Article  CAS  PubMed  Google Scholar 

  38. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938

    Article  CAS  PubMed  Google Scholar 

  39. Lienart Y (2000) Use of xyloglucan polymers and oligomers, and derivative compounds, as phytosanitary products and biofertilizers. EP 1359802 B1

  40. Linsmaier EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18:100–127

    Article  CAS  Google Scholar 

  41. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2_DDCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  42. Madson M, Dunand C, Li X, Verma R, Vanzin GF, Caplan J, Shoue DA, Carpita NC, Reiter W-D (2003) The MUR3 Gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15:1662–1670

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Marcus S, Verhertbruggen Y, Hervé C, Ordaz-Ortiz J, Farkas V, Pedersen H, Willats W, Knox J (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:1–12

    Article  Google Scholar 

  44. Matsui K, Collings D, Asada T (2001) Identification of a novel plant-specific kinesin-like protein that is highly expressed in interphase tobacco BY-2 cells. Protoplasma 215:105–115

    Article  CAS  PubMed  Google Scholar 

  45. Matsuoka K, Demura T, Galis I, Horiguchi T, Sasaki M, Tashiro G, Fukuda H (2004) A Comprehensive gene expression analysis toward the understanding of growth and differentiation of tobacco BY-2 cells. Plant Cell Physiol 45:1280–1289

    Article  PubMed  Google Scholar 

  46. Mazumder S, Lerouge P, Loutelier-Bourhis C, Driouich A, Ray B (2005) Structural characterisation of hemicellulosic polysaccharides from Benincasa hispida using specific enzyme hydrolysis, ion exchange chromatography and MALDI-TOF mass spectroscopy. Carbohydr Polym 59:231–238

    Article  CAS  Google Scholar 

  47. McDougall GJ, Fry SC (1989) Structure–activity relationships for xyloglucan oligosaccharides with antiauxin activity. Plant Physiol 89:883–887

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. McDougall GJ, Fry SC (1990) Xyloglucan oligosaccharides promote growth and activate cellulase: evidence for a role of cellulase in cell expansion. Plant Physiol 93:1042–1048

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. McDougall GJ, Fry SC (1991) Purification and analysis of growth-regulating xyloglucan-derived oligosaccharides by high-pressure liquid chromatography. Carbohydr Res 219:123–132

    Article  CAS  PubMed  Google Scholar 

  50. Moghaddam MRB, Van den Ende W (2012) Sugars and plant innate immunity. J Exp Bot 63:3989–3998

    Article  Google Scholar 

  51. Müller D, Schmitz G, Theres K (2006) Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18:586–597

    Article  PubMed Central  PubMed  Google Scholar 

  52. Neuteboom LW, Ng JMY, Kuyper M, Clijdesdale OR, Hooykaas PJJ, van der Zaal BJ (1999) Isolation and characterization of cDNA clones corresponding with mRNAs that accumulate during auxin-induced lateral root formation. Plant Mol Biol 39:273–287

    Article  CAS  PubMed  Google Scholar 

  53. Ogawa T, Nishimura K, Aoki T, Takase H, Tomizawa K-I, Ashida H, Yokota A (2009) A phosphofructokinase B-type carbohydrate kinase family protein, NARA5, for massive expressions of plastid-encoded photosynthetic genes in Arabidopsis. Plant Physiol 151:114–128

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. Ohashi-Ito K, Bergmann DC (2006) Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18:2493–2505

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  55. Park YW, Tominaga R, Sugiyama J, Furuta Y, Tanimoto E, Samejima M, Sakai F, Hayashi T (2003) Enhancement of growth by expression of poplar cellulase in Arabidopsis thaliana. Plant J 33:1099–1106

    Article  CAS  PubMed  Google Scholar 

  56. Park YW, Baba K, Furuta Y, Iida I, Sameshima K, Arai M, Hayashi T (2004) Enhancement of growth and cellulose accumulation by overexpression of xyloglucanase in poplar. FEBS Lett 564:183–187

    Article  CAS  PubMed  Google Scholar 

  57. Pavlova ZN, Loskutova NA, Vnuchkova VA, Muromtsev GS, Usov AI, Shibaev VN (1996) Xyloglucan oligosaccharins as elicitors of plant defense responses. Russ J Plant Physiol 43:242–246

    CAS  Google Scholar 

  58. Rose JKC, Braam J, Fry SC, Nishitani K (2002) The XTH Family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435

    Article  CAS  PubMed  Google Scholar 

  59. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  60. Shani Z, Dekel M, Tsabary G, Goren R, Shoseyov O (2004) Growth enhancement of transgenic poplar plants by overexpression of Arabidopsis thaliana endo-1,4–β-glucanase (cel1). Mol Breed 14:321–330

    Article  Google Scholar 

  61. Shiu S-H, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci Signal Signal Transduct Knowl 2001:re22

    CAS  Google Scholar 

  62. Siciliano I (2006) Effect of plant WEE1 on the cell cycle and development in Arabidopsis thaliana and Nicotiana tabacum. PhD Thesis, Cardiff University

  63. Silipo A, Erbs G, Shinya T, Dow JM, Parrilli M, Lanzetta R, Shibuya N, Newman M-A, Molinaro A (2010) Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology 20:406–419

    Article  CAS  PubMed  Google Scholar 

  64. Slováková L, Subíková V, Farkas V (1993) Influence of xyloglucan oligosaccharides on some enzymes involved in the hypersensitive reaction to TNV (tobacco necrosis virus) of cucumber cotyledons. Z Pflanzenkrankh Pflanzenschutz 101:278–285

    Google Scholar 

  65. Sorrell DA, Menges M, Healy JMS, Deveaux Y, Amano C, Su Y, Nakagami H, Shinmyo A, Doonan JH, Sekine M, Murray JAH (2001) Cell cycle regulation of cyclin-dependent kinases in tobacco cultivar bright yellow-2 cells. Plant Physiol 126:1214–1223

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. Šubíková V, Slovikova I, Farkas V (1994) Inhibition of tobacco necrosis virus infection by xyloglucan fragments. Z Pflanzenkrankh Pflanzenschutz 101:128–131

    Google Scholar 

  67. Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQP, Kadota A, Wada M (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:8860–8865

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Suzuki T, Nakajima S, Inagaki S, Hirano-Nakakita M, Matsuoka K, Demura T, Fukuda H, Morikami A, Nakamura K (2005) TONSOKU is expressed in S phase of the cell cycle and its defect delays cell cycle progression in Arabidopsis. Plant Cell Physiol 46:736–742

    Article  CAS  PubMed  Google Scholar 

  69. Suzuki T, Nakajima S, Morikami A, Nakamura K (2005) An Arabidopsis protein with a novel calcium-binding repeat sequence interacts with TONSOKU/MGOUN3/BRUSHY1 Involved in meristem maintenance. Plant Cell Physiol 46:1452–1461

    Article  CAS  PubMed  Google Scholar 

  70. Takeda T, Furuta Y, Awano T, Mizuno K, Mitsuishi Y, Hayashi T (2002) Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments. Proc Natl Acad Sci USA 99:9055–9060

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Tedman-Jones JD, Lei R, Jay F, Fabro G, Li X, Reiter W-D, Brearley C, Jones JDG (2008) Characterization of Arabidopsis mur3 mutations that result in constitutive activation of defence in petioles, but not leaves. Plant J 56:691–703

    Article  CAS  PubMed  Google Scholar 

  72. Thomma BPHJ, Eggermont K, Tierens KFM-J, Broekaert WF (1999) Requirement of functional Ethylene-Insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol 121:1093–1101

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  73. van der Knaap E, Song W-Y, Ruan D-L, Sauter M, Ronald PC, Kende H (1999) Expression of a gibberellin-induced leucine-rich repeat receptor-like protein kinase in deepwater rice and its interaction with kinase-associated protein phosphatase. Plant Physiol 120:559–570

    Article  PubMed Central  PubMed  Google Scholar 

  74. Vanstraelen M, Van Damme D, De Rycke R, Mylle E, Inzé D, Geelen D (2006) Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16:308–314

    Article  CAS  PubMed  Google Scholar 

  75. Wilkinson JQ, Lanahan MB, Yen H-C, Giovannoni JJ, Klee HJ (1995) An ethylene-inducible component of signal transduction encoded by Never-ripe. Science 270:1807–1809

    Article  CAS  PubMed  Google Scholar 

  76. York WS, van Halbeek H, Darvill AG, Albersheim P (1990) Structural analysis of xyloglucan oligosaccharides by 1H-n.m.r. spectroscopy and fast-atom-bombardment mass spectrometry. Carbohydr Res 200:9–31

    Article  CAS  PubMed  Google Scholar 

  77. Zablackis E, York WS, Pauly M, Hantus S, Reiter W-D, Chapple CCS, Albersheim P, Darvill A (1996) Substitution of l-fucose by l-galactose in cell walls of Arabidopsis mur1. Science 272:1808–1810

    Article  CAS  PubMed  Google Scholar 

  78. Zabotina OA (2005) Oligosaccharin—a new systemic factor in the acquisition of freeze tolerance in winter plants. Plant Biosyst 139:36–41

    Article  Google Scholar 

  79. Zabotina OA, Ayupova DA, Larskaya IA, Nikolaeva OG, Petrovicheva GA, Zabotin AI (1998) Physiologically active oligosaccharides, accumulating in the roots of winter wheat during adaptation to low temperature. Russ J Plant Physiol 45:221–226

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Royal Society (International Joint Project—2008/R4 to LGP), by the University of Sassari (LP) and the University of Calabria (NDS and LB). We thank the Nottingham Arabidopsis Stock Centre (NASC) for the microarray service, Professor J.A.H. Murray and Dr. J. Nieuwland (Cardiff School of Biosciences) for advice and assistance on using Real time PCR and LGP thanks Dr. M.R.S. (Biotechnology Institute, Mexico) for advice in preparing the final version of the manuscript.

Author information

Authors and Affiliations

  1. Plant Biology Department, Faculty of Biology, University of Havana, Havana City, Cuba

    Lien González-Pérez

  2. Facultad de Ingeniería y Ciencias Agropecuarias, Universidad de las Américas (UDLA), Quito, Ecuador

    Lien González-Pérez

  3. Department of Science for Nature and Environmental Resources, University of Sassari, Sassari, Italy

    Lara Perrotta & Diego Albani

  4. Biotechnology Institute, National Autonomous University of Mexico (UNAM), Cuernavaca, Morelos, Mexico

    Alexis Acosta

  5. Escuela de Ciencias Biológicas, Pontificia Universidad Católica del Ecuador (PUCE), Quito, Ecuador

    Esteban Orellana

  6. School of Biosciences, Cardiff University, Main Building, Cardiff, CF10 3AT, UK

    Lara Perrotta, Natasha Spadafora, Dennis Francis & Hilary J. Rogers

  7. Dipartimento di Ecologia, Università della Calabria, Arcavacata di Rende, 87030, Cosenza, Italy

    Natasha Spadafora, Leonardo Bruno & Beatrice M. Bitonti

  8. Unité de Biotechnologie, Materia Nova, Rue des Foudriers, 1, 7822, Ghislenghien, Belgium

    Juan Carlos Cabrera

Authors
  1. Lien González-Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lara Perrotta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexis Acosta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Esteban Orellana
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Natasha Spadafora
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Leonardo Bruno
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Beatrice M. Bitonti
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Diego Albani
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Juan Carlos Cabrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dennis Francis
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hilary J. Rogers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hilary J. Rogers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PPT 114 kb)

Supplementary Table 3

Results of microarray analysis: probes that were up or down regulated by ≥2-fold and putative functions where data are available (DOC 105 kb)

(DOC 43 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-Pérez, L., Perrotta, L., Acosta, A. et al. In tobacco BY-2 cells xyloglucan oligosaccharides alter the expression of genes involved in cell wall metabolism, signalling, stress responses, cell division and transcriptional control. Mol Biol Rep 41, 6803–6816 (2014). https://doi.org/10.1007/s11033-014-3566-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-014-3566-y

Keywords

Search

Navigation