Sugar composition of the pectic polysaccharides of charophytes, the closest algal relatives of land-plants: presence of 3-O-methyl-D-galactose residues

Stephen Fry, Christina M. O'Rourke, Timothy Gregson, Lorna Murray, Ian Sadler

Research output: Contribution to journalArticlepeer-review

Abstract

Background and Aims During evolution, plants have acquired and/or lost diverse sugar residues as cell-wall constituents. Of particular interest are primordial cell-wall features that existed, and in some cases abruptly changed, during the momentous step whereby land-plants arose from charophytic algal ancestors.

Methods Polysaccharides were extracted from four charophyte orders [Chlorokybales (Chlorokybus atmophyticus), Klebsormidiales (Klebsormidium fluitans, K. subtile), Charales (Chara vulgaris, Nitella flexilis), Coleochaetales (Coleochaete scutata)] and an early-diverging land-plant (Anthoceros agrestis). ‘Pectins’ and ‘hemicelluloses’, operationally defined as extractable in oxalate (100 °C) and 6 M NaOH (37 °C), respectively, were acid- or Driselase-hydrolysed, and the monosaccharides analysed chromatographically. One unusual monosaccharide, ‘U’, was characterized by 1H/13C-nuclear magnetic resonance spectroscopy and also enzymically.

Key Results ‘U’ was identified as 3-O-methyl-D-galactose (3-MeGal). All pectins, except in Klebsormidium, contained acid- and Driselase-releasable galacturonate, suggesting homogalacturonan. All pectins, without exception, released rhamnose and galactose on acid hydrolysis; however, only in ‘higher’ charophytes (Charales, Coleochaetales) and Anthoceros were these sugars also efficiently released by Driselase, suggesting rhamnogalacturonan-I. Pectins of ‘higher’ charophytes, especially Chara, contained little arabinose, instead possessing 3-MeGal. Anthoceros hemicelluloses were rich in glucose, xylose, galactose and arabinose (suggesting xyloglucan and arabinoxylan), none of which was consistently present in charophyte hemicelluloses.

Conclusions Homogalacturonan is an ancient streptophyte feature, albeit secondarily lost in Klebsormidium. When conquering the land, the first embryophytes already possessed rhamnogalacturonan-I. In contrast, charophyte and land-plant hemicelluloses differ substantially, indicating major changes during terrestrialization. The presence of 3-MeGal in charophytes and lycophytes but not in the ‘intervening’ bryophytes confirms that cell-wall chemistry changed drastically between major phylogenetic grades.
Original languageEnglish
Pages (from-to)225-236
JournalAnnals of Botany
Volume116
Issue number2
Early online date25 Jun 2015
DOIs
Publication statusE-pub ahead of print - 25 Jun 2015

Keywords

  • Charophytic algae
  • charophytes
  • Embryophyta
  • Streptophyta
  • Chlorokybus
  • Klebsormidium
  • Chara
  • Coleochaete
  • plant cell-wall evolution
  • pectin
  • pectic polysaccharides
  • rhamnogalacturonan-I
  • 3-O-methyl-D-galactose

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