Differing structures of galactoglucomannan in eudicots and non-eudicot angiosperms

PLoS One. 2023 Dec 21;18(12):e0289581. doi: 10.1371/journal.pone.0289581. eCollection 2023.

Abstract

The structures of cell wall mannan hemicelluloses have changed during plant evolution. Recently, a new structure called β-galactoglucomannan (β-GGM) was discovered in eudicot plants. This galactoglucomannan has β-(1,2)-Gal-α-(1,6)-Gal disaccharide branches on some mannosyl residues of the strictly alternating Glc-Man backbone. Studies in Arabidopsis revealed β-GGM is related in structure, biosynthesis and function to xyloglucan. However, when and how plants acquired β-GGM remains elusive. Here, we studied mannan structures in many sister groups of eudicots. All glucomannan structures were distinct from β-GGM. In addition, we searched for candidate mannan β-galactosyltransferases (MBGT) in non-eudicot angiosperms. Candidate AtMBGT1 orthologues from rice (OsGT47A-VII) and Amborella (AtrGT47A-VII) did not show MBGT activity in vivo. However, the AtMBGT1 orthologue from rice showed MUR3-like xyloglucan galactosyltransferase activity in complementation analysis using Arabidopsis. Further, reverse genetic analysis revealed that the enzyme (OsGT47A-VII) contributes to proper root growth in rice. Together, gene duplication and diversification of GT47A-VII in eudicot evolution may have been involved in the acquisition of mannan β-galactosyltransferase activity. Our results indicate that β-GGM is likely to be a eudicot-specific mannan.

MeSH terms

  • Arabidopsis* / genetics
  • Galactosyltransferases / genetics
  • Humans
  • Magnoliopsida*
  • Mannans / chemistry
  • Phylogeny
  • Plants

Substances

  • galactoglucomannan
  • Mannans
  • Galactosyltransferases

Grants and funding

This work was supported by the ERC Advanced Grant EVOCATE to P.D. funded by the United Kingdom Research and Innovation (UKRI) grant number EP/X027120/1 (www.ukri.org). The Japan Society for the Promotion of Science KAKENHI (Grant Nos. 23K05487 and 20K05950 www.jsps.go.jp) to H.I. and the 31st and 32nd Botanical Research Grant of ICHIMURA Foundation for New Technology (www.sgkz.or.jp) to H.I supported the work of H.I. and U.O. K.I. was supported by the Masayoshi-Son foundation scholarship (masason-foundation.org). A Broodbank Research Fellowship of the University of Cambridge (www.cam.ac.uk) no. PD16178 supported Y.Y. The University of Cambridge Herchel Smith scholarship supported A.E (www.cam.ac.uk). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.