Reducing cell wall feruloylation by expression of a fungal ferulic acid esterase in Festuca arundinacea modifies plant growth, leaf morphology and the turnover of cell wall arabinoxylans

PLoS One. 2017 Sep 21;12(9):e0185312. doi: 10.1371/journal.pone.0185312. eCollection 2017.

Abstract

A feature of cell wall arabinoxylan in grasses is the presence of ferulic acid which upon oxidative coupling by the action of peroxidases forms diferuloyl bridges between formerly separated arabinoxylans. Ferulate cross-linking is suspected of playing various roles in different plant processes. Here we investigate the role of cell wall feruloyaltion in two major processes, that of leaf growth and the turnover of cell wall arabinoxylans on leaf senescence in tall fescue using plants in which the level of cell wall ferulates has been reduced by targeted expression of the Aspergillus niger ferulic acid esterase A (FAEA) to the apoplast or Golgi. Analysis of FAE expressing plants showed that all the lines had shorter and narrower leaves compared to control, which may be a consequence of the overall growth rate being lower and occurring earlier in FAE expressing leaves than in controls. Furthermore, the final length of epidermal cells was shorter than controls, indicating that their expansion was curtailed earlier than in control leaves. This may be due to the observations that the deposition of both ether and ester linked monomeric hydroxycinnamic acids and ferulate dimerization stopped earlier in FAE expressing leaves but at a lower level than controls, and hydroxycinnamic acid deposition started to slow down when peroxidase levels increased. It would appear therefore that one of the possible mechanisms for controlling overall leaf morphology such as leaf length and width in grasses, where leaf morphology is highly variable between species, may be the timing of hydroxycinnamic acid deposition in the expanding cell walls as they emerge from cell division into the elongation zone, controlled partially by the onset of peroxidase activity in this region.

MeSH terms

  • Aspergillus niger / enzymology*
  • Aspergillus niger / genetics
  • Carboxylic Ester Hydrolases / genetics*
  • Cell Wall / metabolism*
  • Coumaric Acids / metabolism*
  • Festuca / anatomy & histology
  • Festuca / cytology
  • Festuca / genetics
  • Festuca / growth & development*
  • Gene Expression
  • Peroxidase / metabolism
  • Phenotype
  • Plant Leaves / growth & development*
  • Plants, Genetically Modified
  • Xylans / metabolism*

Substances

  • Coumaric Acids
  • Xylans
  • arabinoxylan
  • ferulic acid
  • Peroxidase
  • Carboxylic Ester Hydrolases
  • feruloyl esterase

Grants and funding

Funding for this work was provided by the National Research Initiative on Agriculture and Food Research Initiative Competitive Grants Program from the USDA National Institute of Food and Agriculture. Role: hiring personnel, purchase equipment and consumables and support to attend meetings to present results of study. Small part of funding support for this work was by the Elberly Endounment of Elberly College of Science, PSU. Role: covering part of salary for Research personnel. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.