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Arabidopsis lignins, which are genetically p-coumaroylated up to the grass lignin level, display dramatic structural changes that make them more amenable to solubilization in alkali at room temperature.
Grass lignins can contain up to 10% to 15% by weight of
p
-coumaric esters. This acylation is performed on monolignols under the catalysis of
p
-coumaroyl-coenzyme A monolignol transferase (PMT). To study the impact of
p
-coumaroylation on lignification, we first introduced the
Brachypodium distachyon Bradi2g36910
(
BdPMT1
) gene into Arabidopsis (
Arabidopsis thaliana
) under the control of the constitutive maize (
Zea mays
) ubiquitin promoter. The resulting
p
-coumaroylation was far lower than that of lignins from mature grass stems and had no impact on stem lignin content. By contrast, introducing either the
BdPMT1
or the
Bradi1g36980
(
BdPMT2
) gene into Arabidopsis under the control of the Arabidopsis cinnamate-4-hydroxylase promoter boosted the
p
-coumaroylation of mature stems up to the grass lignin level (8% to 9% by weight), without any impact on plant development. The analysis of purified lignin fractions and the identification of diagnostic products confirmed that
p
-coumaric acid was associated with lignins. BdPMT1-driven
p
-coumaroylation was also obtained in the
fah1
(deficient for ferulate 5-hydroxylase) and
ccr1g
(deficient for cinnamoyl-coenzyme A reductase) lines, albeit to a lower extent. Lignins from
BdPMT1-
expressing
ccr1g
lines were also found to be feruloylated. In Arabidopsis mature stems, substantial
p
-coumaroylation of lignins was achieved at the expense of lignin content and induced lignin structural alterations, with an unexpected increase of lignin units with free phenolic groups. This higher frequency of free phenolic groups in Arabidopsis lignins doubled their solubility in alkali at room temperature. These findings suggest that the formation of alkali-leachable lignin domains rich in free phenolic groups is favored when
p
-coumaroylated monolignols participate in lignification in a grass in a similar manner.