Skip to main content
Log in

Pectic galactan affects cell wall architecture during secondary cell wall deposition

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

β-(1,4)-galactan determines the interactions between different matrix polysaccharides and cellulose during the cessation of cell elongation.

Abstract

Despite recent advances regarding the role of pectic β-(1,4)-galactan neutral side chains in primary cell wall remodelling during growth and cell elongation, little is known about the specific function of this polymer in other developmental processes. We have used transgenic Arabidopsis plants overproducing chickpea βI-Gal β-galactosidase under the 35S CaMV promoter (35S::βI-Gal) with reduced galactan levels in the basal non-elongating floral stem internodes to gain insight into the role of β-(1,4)-galactan in cell wall architecture during the cessation of elongation and the beginning of secondary growth. The loss of galactan mediated by βI-Gal in 35S::βI-Gal plants is accompanied by a reduction in the levels of KOH-extracted xyloglucan and an increase in the levels of xyloglucan released by a cellulose-specific endoglucanase. These variations in cellulose–xyloglucan interactions cause an altered xylan and mannan deposition in the cell wall that in turn results in a deficient lignin deposition. Considering these results, we can state that β-(1,4)-galactan plays a key structural role in the correct organization of the different domains of the cell wall during the cessation of growth and the early events of secondary cell wall development. These findings reinforce the notion that there is a mutual dependence between the different polysaccharides and lignin polymers to form an organized and functional cell wall.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Andersen MC, Boos I, Marcus SE, Kracun SK, Rydahl MG, Willats WG, Knox JP, Clausen MH (2016) Characterization of the LM5 pectic galactan epitope with synthetic analogues of β-1,4-d-galactotetraose. Carbohydr Res 436:36–40

    Article  CAS  PubMed  Google Scholar 

  • Brett CT, Healy SA, McDonald MS, Macgregor C, Baydoun EA (1997) Binding of nascent glucuronoxylan to the cell walls of pea seedlings. Int J Biol Macromol 21:169–173

    Article  CAS  PubMed  Google Scholar 

  • Broxterman SE, Schols HA (2018) Interactions between pectin and cellulose in primary plant cell walls. Carbohyd Polym 192:263–272

    Article  CAS  Google Scholar 

  • 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 

  • Chong SL, Virkki L, Maaheimo H, Juvonen M, Derba-Maceluch M, Koutaniemi S, Roach M, Sundberg B, Tuomainen P, Mellerowicz EJ, Tenkanen M (2014) O-Acetylation of glucuronoxylan in Arabidopsis thaliana wild type and its change in xylan biosynthesis mutants. Glycobiol 24:494–506

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cornuault V, Buffetto F, Rydahl MG, Marcus SE, Torode TA, Xue J, Crépeau MJ, Faria-Blanc N, Willats WGT, Dupree P, Ralet MC, Knox JP (2015) Monoclonal antibodies indicate low-abundance links between heteroxylan and other glycans of plant cell walls. Planta 242:1321–1334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cornuault V, Posé S, Knox JP (2018) Disentangling pectic homogalacturonan and rhamnogalacturonan-I polysaccharides: evidence for sub-populations in fruit parenchyma systems. Food Chem 246:275–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove DJ (2005) Growth of the cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • Cumming CM, Rizkallah HD, McKendrick KA, Abdel-Massih RM, Baydoun E, Brett CT (2005) Biosynthesis and cell-wall deposition of a pectin-xyloglucan complex in pea. Planta 222:546–555

    Article  CAS  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Fry SC, York WS, Albersheim P, Darvill A, Hayashi T, Joseleau J-P, 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

    Article  CAS  Google Scholar 

  • Gorshkova T, Morvan C (2006) Secondary cell-wall assembly in flax phloem fibres: role of galactans. Planta 223:149–158

    Article  CAS  PubMed  Google Scholar 

  • Gorshkova T, Mokshina N, Chernova T, Ibragimova N, Salnikov V, Mikshina P, Tryfona T, Banasiak A, Immerzeel P, Dupree P, Mellerowicz EJ (2015) Aspen tension wood fibers contain β-(1,4)-galactans and acidic arabinogalactans retained by cellulose microfibrils in gelatinous walls. Plant Physiol 169:2048–2063

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hao ZY, Mohnen D (2014) A review of xylan and lignin biosynthesis: foundation for studying Arabidopsis irregular xylem mutants with pleiotropic phenotypes. Crit Rev Biochem Mol 49:212–241

    Article  CAS  Google Scholar 

  • Hao Z, Avci U, Tan L, Zhu X, Glushka J, Pattathil S, Eberhard S, Sholes T, Rothstein GE, Lukowitz W, Orlando R, Hahn MG, Mohnen D (2014) Loss of Arabidopsis GAUT12/IRX8 causes anther indehiscence and leads to reduced G lignin associated with altered matrix polysaccharide deposition. Front Plant Sci 5:357

    Article  PubMed  PubMed Central  Google Scholar 

  • Hernández-Gómez MC, Runavot JL, Guo X, Bourot S, Benians TAS, Willats WGT, Meulewaeter F, Knox JP (2015) Heteromannan and heteroxylan cell wall polysaccharides display different dynamics during the elongation and secondary cell wall deposition phases of cotton fiber cell development. Plant Cell Physiol 56:1786–1797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Izquierdo L, Martín I, Albornos L, Hernández-Nistal J, Hueso P, Dopico B, Labrador E (2018) Overexpression of Cicer arietinum βIII-Gal but not βIV-Gal in Arabidopsis causes a reduction of cell wall β-(1,4)-galactan compensated by an increase in homogalacturonan. J Plant Physiol 231:135–146

    Article  CAS  PubMed  Google Scholar 

  • Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1[→]4)-[beta]-d-galactan. Plant Physiol 113:1405–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerr EM, Fry SC (2004) Extracellular cross-linking of xylan and xyloglucan in maize cell-suspension cultures: the role of oxidative coupling. Planta 219:73–83

    Article  CAS  PubMed  Google Scholar 

  • Li M, Pu Y, Ragauskas AJ (2016) Current understanding of the correlation of lignin structure with biomass recalcitrance. Front Chem 4:1–8

    Article  CAS  Google Scholar 

  • Marcus SE, Verhertbruggen Y, Hervé C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WGT, Knox JP (2008) Pectic homogalacturonan mask abundant set of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marcus SE, Blake AW, Benians TA, Lee KJ, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, Gilbert HJ, Willats WG, Knox JP (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 64:191–203

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • McCartney L, Marcus SE, Knox JP (2005) Monoclonal Antibodies to Plant Cell Wall Xylans and Arabinoxylans. J Histochem Cytochem 53:543–546

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Moneo-Sánchez M, Alonso-Chico A, Knox JP, Dopico B, Labrador E, Martín I (2019) β-(1,4)-Galactan remodelling in Arabidopsis cell walls alters cellulose/xyloglucan interactions during cell elongation. Planta 249:351–362

    Article  PubMed  CAS  Google Scholar 

  • Mortimer JC, Miles GP, Brown DM, Zhang Z, Segura MP, Weimar T, Yu X, Seffen KA, Stephens E, Turner SR (2010) Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass. Proc Natl Acad Sci USA 107:17409–17414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pattathil S, Avci U, Baldwin D, Swennes AG, McGill JA, Popper Z, Bootten T, Albert A, Davis RH, Chennareddy C, Dong R, O'Shea B, Rossi R, Leoff C, Freshour G, Narra R, O'Neil M, York WS, Hahn MG (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153:514–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen HL, Fangel JU, McCleary B, Ruzanski C, Rydahl MG, Ralet M-C, Farkas V, von Schantz L, Marcus SE, Andersen MCF, Field R, Ohlin M, Knox JP, Clausen MH, Willats WGT (2012) Versatile high resolution oligosaccharide microarrays for plant glycobiology and cell wall research. J Biol Chem 287:39429–39438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peralta AG, Venkatachalam S, Stone SC, Pattathil S (2017) Xylan epitope profiling: an enhanced approach to study organ development-dependent changes in xylan structure, biosynthesis, and deposition in plant cell walls. Biotechnol Biofuels 10:245–255

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pichon M, Journet E-P, de Billy F, Dedleu A, Huguet T, Truchet G, Barker DG (1994) ENOD12 gene expression as a molecular marker for comparing rhizobium-dependent and -independent nodulation in alfalfa. Mol Plant Microbe Interact 7:740–747

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Puhlmann J, Bucheli E, Swain MJ, Dunning N, Albersheim P, Darvill AG, Hahn MG (1994) Generation of monoclonal antibodies against plant cell wall polysaccharides. I. Characterization of a monoclonal antibody to a terminal α-(1→2)-linked fucosyl-containing epitope. Plant Physiol 104:699–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ralet MC, Crépeau MJ, Vigouroux J, Tran J, Berger A, Sallé C, Granier F, Botran L, North HM (2016) Xylans provide the structural driving force for mucilage adhesion to the Arabidopsis seed coat. Plant Physiol 171:165–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ralph SA, Ralph J, Landucci L (2009) NMR database of lignin and cell wall model compounds. www.glbrc.org/databases_and_software/nmrdatabase/. Accessed 10 Feb 2020

  • Rizk SE, Abdel-Massih RM, Baydoun EAH, Brett CT (2000) Protein and pH dependent binding of nascent pectin and glucuronoarabinoxylan to xyloglucan in pea. Planta 211:423–429

    Article  CAS  PubMed  Google Scholar 

  • Ruprecht C, Bartetzko MP, Senf D, Dallabernadina P, Boos I, Andersen MCF, Kotake T, Knox JP, Hahn MG, Clausen MH, Fabian Pfrenglea F (2017) A synthetic glycan microarray enables epitope mapping of plant cell wall glycan-directed antibodies. Plant Physiol 175:1094–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sainsbury F, Thuenemann EC, Lomonossoff GP (2009) PEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J 7:682–693

    Article  CAS  PubMed  Google Scholar 

  • Singh B, Avci U, Inwood S, Grimson MJ, Landgraf J, Mohnen D, Sørensen I, Wilkerson C, Willats WGT, Haigler CH (2009) A specialized outer layer of the primary cell wall joins elongating cotton fibers into tissue-like bundles. Plant Physiol 150:684–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srebotnik E, Messner K (1994) A simple method that uses differential staining and light microscopy to assess the selectivity of wood delignification by white rot fungi. Appl Environ Microbiol 60:1383–1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan L, Eberhard S, Pattathil S (2013) An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell 25:270–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Acker R, Leple JC, Aerts D, Storme V, Goeminne G, Ivens B, Legee F, Lapierre C, Piens K, Van Montagu MC, Santoro N, Foster CE, Ralph J, Soetaert W, Pilate G, Boerjan W (2014) Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase. Proc Natl Acad Sci USA 111:845–850

    Article  PubMed  CAS  Google Scholar 

  • Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344:1858–1862

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Samsulrizal NH, Yan C, Allcock NS, Craigon J, Blanco-Ulate B, Ortega-Salazar I, Marcus SE, Bagheri HM, Perez Fons L, Fraser PD, Foster T, Fray R, Knox JP, Seymour GB (2019) Characterization of CRISPR mutants targeting genes modulating pectin degradation in ripening tomato. Plant Physiol 179:544–557

    CAS  PubMed  Google Scholar 

  • Yan L, Liu S, Zhao S, Kang Y, Wang D, Gu T, Xin Z, Xia G, Huang Y (2012) Identification of differentially expressed genes in sorghum (Sorghum bicolor) brown midrib mutants. Physiol Plant 146:375–387

    Article  CAS  PubMed  Google Scholar 

  • Yuan TQ, Sun SN, Xu F, Sun RC (2011) Characterization of lignin structures and lignin-carbohydrate complex (LCC) linkages by quantitative C-13 and 2D HSQC NMR spectroscopy. J Agric Food Chem 59:10604–10614

    Article  CAS  PubMed  Google Scholar 

  • Zabotina OA, Avci U, Cavalier D, Pattathil S, Chou YH, Eberhard S, Danhof L, Keegstra K, Hahn MG (2012) Mutations in multiple XXT genes of Arabidopsis reveal the complexity of xyloglucan biosynthesis. Plant Physiol 159:1367–1384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zykwinska A, Thibault JF, Ralet MC (2008) Competitive binding of pectin and xyloglucan with primary cell wall cellulose. Carbohydr Polym 74:957–961

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the Spanish Ministry of Economics and Competitiveness (MINECO) (BFU2013-44793-P) and by the Regional Government of Castile and Leon [SA027G18]. MM-S was supported by FPI grant from the Basque Government. LA was supported by an FPU grant from the Spanish Ministry of Education, Culture and Sport. Generation of the CCRC series of monoclonal antibodies was supported by a grant from the National Science Foundation (NSF) Plant Genome Program (DBI-0421683). We thank Dr. Toshihisa Kotake, from the Division of Life Science of Saitama University (Japan), for kindly gifting the galactoside substrates. Dr. George Lomonossoff (John Innes Centre, Norwich, UK) for pEAQ vectors development and Plant Bioscience Ltd. (Norwich, UK) for kindly providing these vectors. Dr. Purificación Corchete (Departamento de Botánica y Fisiología Vegetal, University of Salamanca) for helping with lignin isolation. Dr. Anna Lithgow (General Service of NMR of the University of Salamanca) and Drs. Rafael Peláez and Manuel Medarde (Departamento de Química Orgánica, University of Salamanca) for helping with 2D NMR analyses.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ignacio Martín.

Ethics declarations

Conflict of interest

No conflict of interest has been declared.

Additional information

Communicated by Anastasios Melis.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 315 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moneo-Sánchez, M., Vaquero-Rodríguez, A., Hernández-Nistal, J. et al. Pectic galactan affects cell wall architecture during secondary cell wall deposition. Planta 251, 100 (2020). https://doi.org/10.1007/s00425-020-03394-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-020-03394-2

Keywords

Navigation