Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

β-(1,4)-Galactan remodelling in Arabidopsis cell walls affects the xyloglucan structure during elongation

  • 669 Accesses

  • 3 Citations


Main conclusion

Galactan turnover occurs during cell elongation and affects the cell wall xyloglucan structure which is involved in the interaction between cellulose and xyloglucan.

β-(1,4)-Galactan is one of the main side chains of rhamnogalacturonan I. Although the specific function of this polymer has not been completely established, it has been related to different developmental processes. To study β-(1,4)-galactan function, we have generated transgenic Arabidopsis plants overproducing chickpea βI-Gal β-galactosidase under the 35S CaMV promoter (35S::βI-Gal) to reduce galactan side chains in muro. Likewise, an Arabidopsis double loss-of-function mutant for BGAL1 and BGAL3 Arabidopsis β-galactosidases (bgal1/bgal3) has been obtained to increase galactan levels. The characterization of these plants has confirmed the role of β-(1,4)-galactan in cell growth, and demonstrated that the turnover of this pectic side chain occurs during cell elongation, at least in Arabidopsis etiolated hypocotyls and floral stem internodes. The results indicate that BGAL1 and BGAL3 β-galactosidases act in a coordinate way during cell elongation. In addition, this work indicates that galactan plays a role in the maintenance of the cell wall architecture during this process. Our results point to an involvement of the β-(1,4)-galactan in the xyloglucan structure and the interaction between cellulose and xyloglucan.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. Ahn YO, Zheng M, Bevan DR, Esen A, Shiu SH, Benson J, Peng HP, Miller JT, Cheng CL, Poulton JE, Shih MC (2007) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 35. Phytochemistry 68:1510–1520

  2. Albersheim P, Nevins DJ, English PD (1967) A method for the analysis of sugars in plant cell wall polysaccharides by gas liquid chromatography. Carbohydr Res 5:340–345

  3. Albornos L, Martín I, Pérez P, Marcos R, Dopico B, Labrador E (2012) Promoter activities of genes encoding β-galactosidases from Arabidopsis a1 subfamily. Plant Physiol Biochem 60:223–232

  4. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

  5. Bret-Harte MS, Talbott LD (1993) Changes in composition of the outer epidermal cell wall of pea stems during auxin-induced growth. Planta 190:369–378

  6. 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

  7. Chambat G, Karmous M, Costes M, Picard M, Joseleau JP (2005) Variation of xyloglucan substitution pattern affects the sorption on celluloses with different degrees of crystallinity. Cellulose 12:117–125

  8. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

  9. Cornuault V, Manfield IW, Ralet M-C, Knox JP (2014) Epitope detection chromatography: a method to dissect the structural heterogeneity and inter-connections of plant cell–wall matrix glycans. Plant J 78:715–722

  10. Cosgrove DJ (2016) Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall modifying enzymes. J Exp Bot 67:463–476

  11. Dick-Pérez M, Zhang Y, Hayes J, Salazar A, Zabotina OA, Hong M (2011) Structure and interactions of plant cell-wall polysaccharides by two-and three-dimensional magic-angle-spinning solidstate NMR. Biochemistry 50:989–1000

  12. Esteban R, Labrador E, Dopico B (2005) A family of β-galactosidase cDNAs related to development of vegetative tissue in Cicer arietinum. Plant Sci 168:457–466

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

  14. Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol 40:139–168

  15. Kakegawa K, Edashige Y, Ishii T (2000) Metabolism of cell wall polysaccharides in cell suspension cultures of Populus alba in relation to cell growth. Physiol Plant 105:420–425

  16. Karimi M, Depicker A, Hilson P (2007) Recombinational cloning with plant gateway vectors. Plant Physiol 145:1144–1154

  17. Levy S, Maclachlan G, Staehelin LA (1997) Xyloglucan sidechains modulate binding to cellulose during in vitro binding assays as predicted by conformational dynamics simulations. Plant J 11:373–386

  18. Lima DU, Loh W, Buckeridge MS (2004) Xyloglucan–cellulose interaction depends on the sidechains and molecular weight of xyloglucan. Plant Physiol Biochem 42:389–394

  19. Lin D, Lopez-Sanchez P, Gidley MJ (2015) Binding of arabinan or galactan during cellulose synthesis is extensive and reversible. Carbohydr Polym 126:108–121

  20. Martín I, Dopico B, Muñoz FJ, Esteban R, Oomen RJFJ, Driouich A, Vincken JP, Visser R, Labrador E (2005) In vivo expression of a Cicer arietinum β-galactosidase in potato tubers leads to a reduction of the galactan side-chains in cell wall pectin. Plant Cell Physiol 46:1613–1622

  21. Martín I, Jiménez T, Esteban R, Dopico B, Labrador E (2008) Immunolocalization of a cell wall β-galactosidase reveals its developmentally regulated expression in Cicer arietinum and its relationship to vascular tissue. J Plant Growth Regul 27:181–191

  22. Martín I, Jiménez T, Hernández-Nistal J, Labrador E, Dopico B (2009) The location of the chickpea cell wall βV-galactosidase suggests involvement in the transition between cell proliferation and cell elongation. J Plant Growth Regul 28:1–11

  23. Martín I, Jiménez T, Hernández-Nistal J, Dopico B, Labrador E (2011) The βI-galactosidase of Cicer arietinum is located in thickened cell walls such as those of collenchyma, sclerenchyma and vascular tissue. Plant Biol 13:777–783

  24. Martín I, Hernández-Nistal J, Albornos L, Labrador E, Dopico B (2013) βIII-Gal is involved in galactan reduction during phloem element differentiation in chickpea stems. Plant Cell Physiol 54:960–970

  25. McCann MC, Roberts K (1991) Architecture of the primary cell wall. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 109–129

  26. McCartney L, Steele-King CG, Jordan E, Knox JP (2003) Cell wall pectic (1–4)-β-d-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J 33:447–454

  27. Miedes E, Zarra I, Hoson T, Herbers K, Sonnewald U, Lorences EP (2011) Xyloglucan endotransglucosylase and cell wall extensibility. J Plant Physiol 168:196–203

  28. Moneo-Sánchez M, Izquierdo L, Martín I, Labrador E, Dopico B (2016) Subcellular location of Arabidopsis thaliana subfamily a1 β-galactosidases and developmental regulation of transcript levels of their coding genes. Plant Physiol Biochem 109:137–145

  29. Moneo-Sánchez M, Izquierdo L, Martín I, Hernández-Nistal J, Albornos L, Dopico B, Labrador E (2018) Knockout mutants of Arabidopsis thaliana β-galactosidase. Modifications in the cell wall saccharides and enzymatic activities. Biol Plant 62:80–88

  30. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

  31. O’Neill MA, York WS (2003) The composition and structure of plant primary cell walls. In: Rose JKC (ed) The plant cell wall. Blackwell Scientific Publications, Oxford, pp 1–54

  32. Obro J, Borkhardt B, Harholt J, Skjøt M, Willats WG, Ulvskov P (2009) Simultaneous in vivo truncation of pectic side chains. Transgenic Res 18:961–969

  33. Park YB, Cosgrove DJ (2015) Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol 56:180–194

  34. Pauly M, Albersheim P, Darvill A, York WS (1999) Molecular domains of the cellulose/xyloglucan network in the cell walls of higher plants. Plant J 20:629–639

  35. Pauly M, Qin Q, Greene H, Albersheim P, Darvill A, York WS (2001) Changes in the structure of xyloglucan during cell elongation. Planta 212:842–850

  36. Peaucelle A, Braybrook S, Höfte H (2012) Cell wall mechanics and growth control in plants: the role of pectins revisited. Front Plant Sci 3:121

  37. Popper ZA, Fry SC (2008) Xyloglucan–pectin linkages are formed intra-protoplasmically, contribute to wall assembly, and remain stable in the cell wall. Planta 227:781–794

  38. Sampedro J, Gianzo C, Iglesias N, Guitián E, Revilla G, Zarra I (2012) AtBGAL10 is the main xyloglucan β-galactosidase in arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiol 158:1146–1157

  39. Sorensen SO, Pauly M, Bush M, Skjot M, McCann MC, Borkhardt B, Ulvskov P (2000) Pectin engineering: modification of potato pectin by in vivo expression of an endo-1,4-β-d-galactanase. Proc Natl Acad Sci USA 97:7639–7644

  40. Talbott LD, Ray PM (1992) Changes in molecular size of previously deposited and newly synthesized pea cell wall matrix polysaccharides. Plant Physiol 98:369–379

  41. Tanimoto E (1988) Gibberellin regulation of root growth with change in galactose content of cell walls in Pisum sativum. Plant Cell Physiol 29:269–280

  42. Trainotti L, Spinello R, Piovan A, Spolaore S, Casadoro G (2001) β-Galactosidases with a lectin-like domain are expressed in strawberry. J Exp Bot 52:1635–1645

  43. Vincken JP, Schols HA, Oomen RJFJ, McCann MC, Ulvskov P, Voragen AGJ, Visser RGF (2003) If homogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiol 132:1781–1789

  44. Wang T, Park YB, Caporini MA, Rosay M, Zhong L, Cosgrove DJ, Hong M (2013) Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc Natl Acad Sci USA 110:16444–16449

  45. Wang T, Park YB, Cosgrove DJ, Hong M (2015) Cellulose-pectin spatial contacts are inherent to never-dried Arabidopsis thaliana primary cell walls: evidence from solid-state NMR. Plant Physiol 168:871–884

  46. White PB, Wang T, Park YB, Cosgrove DJ, Hong M (2014) Water-polysaccharide interactions in the primary cell wall of Arabidopsis thaliana from polarization transfer solid-state NMR. J Am Chem Soc 136:10399–10409

  47. Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27

  48. Wolf S, Greiner S (2012) Growth control by cell wall pectins. Protoplasma 249:169–175

  49. Zykwinska A, Thibault JF, Ralet MC (2007) Organization of pectic arabinan and galactan side chains in association with cellulose microfibrils in primary cell walls and related models envisaged. J Exp Bot 58:1795–1802

  50. Zykwinska A, Thibault J-F, Ralet M-C (2008) Competitive binding of pectin and xyloglucan with primary cell wall cellulose. Carbohydr Polym 74:957–961

Download references


The work was founding by the Spanish Ministerio de Economía y Competitividad (MINECO) (BFU2013-44793-P) and for the Junta de Castilla-León (SA027G18). M. Moneo-Sánchez was supported by Programa Predoctoral de Formación de Personal Investigador grant from the Basque Government. Generation of the CCRC series of monoclonal antibodies used in this work was supported by a grant from the National Science Foundation (NSF) Plant Genome Program (DBI-0421683).

Author information

Correspondence to Emilia Labrador.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Moneo-Sánchez, M., Alonso-Chico, A., Knox, J.P. et al. β-(1,4)-Galactan remodelling in Arabidopsis cell walls affects the xyloglucan structure during elongation. Planta 249, 351–362 (2019).

Download citation


  • β-Galactosidases
  • Growth
  • Pectin