Convergent Emergence of Glucomannan β-Galactosyltransferase Activity in Asterids and Rosids

Plant Cell Physiol. 2024 Dec 21;65(12):2030-2039. doi: 10.1093/pcp/pcae118.

Abstract

β-Galactoglucomannan (β-GGM) is a primary cell wall polysaccharide in rosids and asterids. The β-GGM polymer has a backbone of repeating β-(1,4)-glucosyl and mannosyl residues, usually with mono-α-(1,6)-galactosyl substitution or β-(1,2)-galactosyl α-galactosyl disaccharide side chains on the mannosyl residues. Mannan β-galactosyltransferases (MBGTs) are therefore required for β-GGM synthesis. The single MBGT identified so far, AtMBGT1, lies in glycosyltransferase family 47A subclade VII and was identified in Arabidopsis. However, despite the presence of β-GGM, an orthologous gene is absent in tomato (Solanum lycopersicum), a model asterid. In this study, we screened candidate MBGT genes from the tomato genome, functionally tested the activities of encoded proteins and identified the tomato MBGT (SlMBGT1) in GT47A-III. Interestingly therefore, AtMBGT1 and SlMBGT1 are located in different GT47A subclades. Furthermore, phylogenetic and glucomannan structural analysis from different species raised the possibility that various asterids possess conserved MBGTs in an asterid-specific subclade of GT47A-III, indicating that MBGT activity has been acquired convergently among asterids and rosids. The present study highlights the promiscuous emergence of donor and acceptor preference in GT47A enzymes. The independent acquisition of the activity also suggests an adaptive advantage for eudicots to acquire β-GGM β-galactosylation and hence also suggests that the disaccharide side chains are important for β-GGM function.

Keywords: Solanum lycopersicum; Cell wall; Enzyme evolution; GT47; MBGT; Mannan.

MeSH terms

  • Cell Wall / enzymology
  • Cell Wall / metabolism
  • Galactosyltransferases / genetics
  • Galactosyltransferases / metabolism
  • Mannans* / metabolism
  • Phylogeny*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Solanum lycopersicum* / enzymology
  • Solanum lycopersicum* / genetics

Substances

  • Mannans
  • Galactosyltransferases
  • Plant Proteins
  • (1-6)-alpha-glucomannan