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Extracellular cross-linking of xylan and xyloglucan in maize cell-suspension cultures: the role of oxidative phenolic coupling

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Abstract

Cell-suspension cultures of maize (Zea mays L.) released soluble extracellular polysaccharides (SEPs) into their medium. Some or all of the SEPs had feruloyl ester groups. Pulse-labelling with [3H]arabinose was used to monitor changes in the SEPs’ M r (estimated by gel-permeation chromatography) with time after synthesis. Newly released 3H-SEPs were 1.3–1.6 MDa, but between 2 days and 3 days after radiolabelling (in one experiment) or between 5 days and 6 days (in another), the 3H-SEPs abruptly increased to ≈17 MDa, indicating extensive cross-linking. The cross-linking involved both [3H]xylan and [3H]xyloglucan components of the SEPs. The cross-links could be cleaved by alkali, returning the SEPs to their original M r. In 0.1 M NaOH at 37°C, 58% cleavage was effected within 24 h. The requirement for such prolonged alkali treatment indicates that ester-bonded (e.g. diferuloyl) groups were not solely responsible for the cross-linking. Bonds cleaved only by relatively severe alkali could include benzyl ether linkages formed between sugar residues and oxidised phenolics that had quinone methide structures. The ability of alkali to cleave the cross-links was independent of the age of the 3H-SEP molecules. Cross-linking of 3H-SEPs in vivo was delayed (up to approx. 7 days after radiolabelling) by exogenous sinapic acid, chlorogenic acid or rutin—agents predicted to compete with the oxidative coupling of feruloyl-polysaccharides. The cross-linking was promoted by exogenous ferulic acid or l-tyrosine, possibly because these compounds acted as precursors for polysaccharide feruloylation, thus providing additional partner substrates for the oxidative coupling of previously formed 3H-SEPs. The ability of certain phenolics to prevent the cross-linking of 3H-SEPs supports the idea that the cross-linking involved phenolic oxidation.

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Abbreviations

DTT :

Dithiothreitol

K av :

Elution volume relative to those of high-M r dextran (K av=0) and sucrose (K av=1)

MLG :

Mixed-linkage β-(1→3),(1→4)-d-glucan

M r :

Relative molecular mass

PCW :

Primary cell wall

SEP :

Soluble extracellular polysaccharide

TFA :

Trifluoroacetic acid

V 0 :

Void volume (centre of elution peak of high-M r dextran)

V i :

Totally included volume (centre of elution peak of sucrose)

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Acknowledgements

E.M.K. thanks the BBSRC for a research studentship. S.C.F. thanks the European Community for funding the ‘COPOL’ project, during the tenure of which this work was conducted.

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  1. The Edinburgh Cell Wall Group, Institute of Cell and Molecular Biology, The University of Edinburgh, Daniel Rutherford Building, The King’s Buildings, Edinburgh, EH9 3JH, UK

    Ellen M. Kerr & Stephen C. Fry

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  1. Ellen M. Kerr
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  2. Stephen C. Fry
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Correspondence to Stephen C. Fry.

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Kerr, E.M., Fry, S.C. Extracellular cross-linking of xylan and xyloglucan in maize cell-suspension cultures: the role of oxidative phenolic coupling. Planta 219, 73–83 (2004). https://doi.org/10.1007/s00425-004-1210-0

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