Abstract

Seagrasses evolved from monocotyledonous land plants that returned to the marine habitat. This transition was accomplished by substantial changes in cell wall composition, revealing habitat-driven adaption to the new environment. Whether arabinogalactan-proteins (AGPs), important signalling molecules of land plants, are present in seagrass cell walls is of evolutionary and plant development interest. AGPs of Zostera marina L. were isolated and structurally characterised by analytical and bioinformatics methods as well as by ELISA with different anti-AGP antibodies. Calcium-binding capacity of AGPs was studied by isothermal titration calorimetry (ITC) and microscopy. Bioinformatic searches of the Z. marina proteome identified 9 classical AGPs and a large number of chimeric AGPs. The glycan structures exhibit unique features, including a high degree of branching and an unusually high content of terminating 4-O-methyl-glucuronic acid (4-OMe GlcA) residues. Although the common backbone structure of land plant AGPs is conserved in Z. marina, the terminating residues are distinct with high amounts of uronic acids. These differences likely result from the glycan-active enzymes (glycosyltransferases and methyltransferases) and are essential for calcium-binding properties. The role of this polyanionic surface is discussed with regard to adaption to the marine environment.

Highlights

  • Seagrasses evolved from early monocotyledonous land plants, returning to the sea around 140 million years ago

  • They are structurally characterised by large carbohydrate moieties comprised of arabinogalactans (AGs, normally >90% of the molecule) which are covalently linked via hydroxyproline (Hyp) to relatively small protein/peptide backbones

  • High molecular weight fractions (HMFs) were isolated from the whole plant and from the different organs by ethanol-precipitation of the supernatants prepared after centrifugation of the aqueous extracts

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Summary

Introduction

Seagrasses evolved from early monocotyledonous land plants, returning to the sea around 140 million years ago Today, these marine angiosperms are a polyphyletic group containing about 60 species in four families (Zosteraceae, Hydrocharitaceae, Posidoniaceae and Cymodoceaceae). Cell walls of seagrasses are characterised by new combinations of structural polysaccharides known from both marine macroalgae and angiosperm land plants. Members of the hydroxyproline-rich glycoprotein family (classified in6), AGPs are ubiquitous in seed land plants[7] and have been found in ferns, lycophytes and mosses[8] They are structurally characterised by large carbohydrate moieties comprised of arabinogalactans (AGs, normally >90% of the molecule) which are covalently linked via hydroxyproline (Hyp) to relatively small protein/peptide backbones (normally around 1–10% of the molecule). Massive upregulation of AGPs has been observed in salt-stressed tobacco cells, suggesting a role of AGPs in osmoregulation[14]

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