The auronidin flavonoid pigments of the liverwort Marchantia polymorpha form polymers that modify cell wall properties

• Published in: The Plant journal : for cell and molecular biology 2024-11, Vol.120 (3), p.1159-1175
• Main Authors: Jibran, Rubina, Hill, Stefan J., Lampugnani, Edwin R., Hao, Pengfei, Doblin, Monika S., Bacic, Antony, Vaidya, Alankar A., O'Donoghue, Erin M., McGhie, Tony K., Albert, Nick W., Zhou, Yanfei, Raymond, Laura G., Schwinn, Kathy E., Jordan, Brian R., Bowman, John L., Davies, Kevin M., Brummell, David A.
• Format: Article
• Language: English
• Subjects: adaptation; ancestry; Angiosperms; Aquatic environment; Aquatic plants; auronidin; cell wall; Cell walls; Environmental stress; flavonoid; Flavonoids; Fractionation; genetically modified organisms; Hydrophobicity; lifestyle; lignin; liverwort; Marchantia; Marchantia polymorpha; Molecular weight; mosses and liverworts; Phenolic compounds; Phenols; Photodegradation; Pigments; plant adaptation; Plant layout; Polymers; polyphenolic; polyphenols; Polysaccharides; Structure-function relationships; Terrestrial environments; terrestrial transition; Transgenic plants
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.17045

SUMMARY Plant adaptation from aquatic to terrestrial environments required modifications to cell wall structure and function to provide tolerance to new abiotic and biotic stressors. Here, we investigate the nature and function of red auronidin pigment accumulation in the cell wall of the liverwort Marchantia polymorpha. Transgenic plants with auronidin production either constitutive or absent were analysed for their cell wall properties, including fractionation of polysaccharide and phenolic components. While small amounts of auronidin and other flavonoids were loosely associated with the cell wall, the majority of the pigments were tightly associated, similar to what is observed in angiosperms for polyphenolics such as lignin. No evidence of covalent binding to a polysaccharide component was found: we propose auronidin is present in the wall as a physically entrapped large molecular weight polymer. The results suggested auronidin is a dual function molecule that can both screen excess light and increase wall strength, hydrophobicity and resistance to enzymatic degradation by pathogens. Thus, liverworts have expanded the core phenylpropanoid toolkit that was present in the ancestor of all land plants, to deliver a lineage‐specific solution to some of the environmental stresses faced from a terrestrial lifestyle. Significance Statement In seed plants, phenolic polymers contribute to the cell wall properties required for a terrestrial lifestyle; however, knowledge is lacking on the contribution of phenolics to cell walls in other plant lineages. Here, we show the auronidin flavonoid pigments of liverworts are likely present in the wall as an entrapped polymer that increases wall hydrophobicity and resistance to enzymatic degradation.